Ammonia determines transcriptional profile of microorganisms in anaerobic digestion

array:23 ["pii" => "S1517838217309267" "issn" => "15178382" "doi" => "10.1016/j.bjm.2018.04.008" "estado" => "S300" "fechaPublicacion" => "2018-10-01" "aid" => "405" "copyrightAnyo" => "2018" "documento" => "article" "crossmark" => 1 "licencia" => "http://creativecommons.org/licenses/by-nc-nd/4.0/" "subdocumento" => "fla" "cita" => "Braz J Microbiol. 2018;49:770-6" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:2 [ "total" => 468 "formatos" => array:3 [ "EPUB" => 81 "HTML" => 186 "PDF" => 201 ] ] "itemSiguiente" => array:19 [ "pii" => "S151783821730802X" "issn" => "15178382" "doi" => "10.1016/j.bjm.2018.01.003" "estado" => "S300" "fechaPublicacion" => "2018-10-01" "aid" => "362" "copyright" => "Sociedade Brasileira de Microbiologia" "documento" => "article" "crossmark" => 1 "licencia" => "http://creativecommons.org/licenses/by-nc-nd/4.0/" "subdocumento" => "fla" "cita" => "Braz J Microbiol. 2018;49:777-84" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:2 [ "total" => 565 "formatos" => array:3 [ "EPUB" => 98 "HTML" => 247 "PDF" => 220 ] ] "en" => array:12 [ "idiomaDefecto" => true "cabecera" => "Veterinary Microbiology" "titulo" => "Molecular characterization of feline calicivirus variants from multicat household and public animal shelter in Rio de Janeiro, Brazil" "tienePdf" => "en" "tieneTextoCompleto" => "en" "tieneResumen" => "en" "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "777" "paginaFinal" => "784" ] ] "contieneResumen" => array:1 [ "en" => true ] "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 3834 "Ancho" => 3083 "Tamanyo" => 1376154 ] ] "descripcion" => array:1 [ "en" => "ML trees of feline calicivirus isolated in this study along with most of the FCV prototypes available so far based on the ORF2 nucleotide sequences. (A) Phylogenetic tree of a 467bp partial fragment of the capsid conserved region A-B; (B) phylogenetic tree of a 529bp partial fragment of the capsid variable region C-F. Isolates from this study are represented with black circles and prototypes from Southern Brazil are represented with*." ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Joylson de Jesus Pereira, Natasha Baumworcel, Júlia Monassa Fioretti, Cinthya Fonseca Domingues, Laís Fernandes de Moraes, Robson dos Santos Souza Marinho, Maria Clara Rodrigues Vieira, Ana Maria Viana Pinto, Tatiana Xavier de Castro" "autores" => array:9 [ 0 => array:2 [ "nombre" => "Joylson de Jesus" "apellidos" => "Pereira" ] 1 => array:2 [ "nombre" => "Natasha" "apellidos" => "Baumworcel" ] 2 => array:2 [ "nombre" => "Júlia Monassa" "apellidos" => "Fioretti" ] 3 => array:2 [ "nombre" => "Cinthya Fonseca" "apellidos" => "Domingues" ] 4 => array:2 [ "nombre" => "Laís Fernandes de" "apellidos" => "Moraes" ] 5 => array:2 [ "nombre" => "Robson dos Santos Souza" "apellidos" => "Marinho" ] 6 => array:2 [ "nombre" => "Maria Clara Rodrigues" "apellidos" => "Vieira" ] 7 => array:2 [ "nombre" => "Ana Maria Viana" "apellidos" => "Pinto" ] 8 => array:2 [ "nombre" => "Tatiana Xavier" "apellidos" => "de Castro" ] ] ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S151783821730802X?idApp=UINPBA00004N" "url" => "/15178382/0000004900000004/v1_201810050636/S151783821730802X/v1_201810050636/en/main.assets" ] "itemAnterior" => array:19 [ "pii" => "S1517838217304616" "issn" => "15178382" "doi" => "10.1016/j.bjm.2018.02.012" "estado" => "S300" "fechaPublicacion" => "2018-10-01" "aid" => "404" "copyright" => "Sociedade Brasileira de Microbiologia" "documento" => "article" "crossmark" => 1 "licencia" => "http://creativecommons.org/licenses/by-nc-nd/4.0/" "subdocumento" => "fla" "cita" => "Braz J Microbiol. 2018;49:757-69" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:2 [ "total" => 748 "formatos" => array:3 [ "EPUB" => 58 "HTML" => 470 "PDF" => 220 ] ] "en" => array:12 [ "idiomaDefecto" => true "cabecera" => "Environmental Microbiology" "titulo" => "Petroleum contamination and bioaugmentation in bacterial rhizosphere communities from Avicennia schaueriana" "tienePdf" => "en" "tieneTextoCompleto" => "en" "tieneResumen" => "en" "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "757" "paginaFinal" => "769" ] ] "contieneResumen" => array:1 [ "en" => true ] "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0010" "etiqueta" => "Fig. 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 2798 "Ancho" => 2492 "Tamanyo" => 394644 ] ] "descripcion" => array:1 [ "en" => "Comparison of the bacterial community structures by DGGE based on bacterial 16S rRNA. S: (S) Standard bacterial 16S rRNA; (1) controls, plants without inoculum and oil; (2) inoculated plants; (3) inoculated plants artificially contaminated with 1mL of emulsified crude oil in 10mL of sea water; (4) plant artificially contaminated with 1mL of emulsified crude oil in 10mL of sea water." ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Simone Dealtry, Angela Michelato Ghizelini, Leda C.S. Mendonça-Hagler, Ricardo Moreira Chaloub, Fernanda Reinert, Tácio M.P. de Campos, Newton C.M. Gomes, Kornelia Smalla" "autores" => array:8 [ 0 => array:2 [ "nombre" => "Simone" "apellidos" => "Dealtry" ] 1 => array:2 [ "nombre" => "Angela Michelato" "apellidos" => "Ghizelini" ] 2 => array:2 [ "nombre" => "Leda C.S." "apellidos" => "Mendonça-Hagler" ] 3 => array:2 [ "nombre" => "Ricardo Moreira" "apellidos" => "Chaloub" ] 4 => array:2 [ "nombre" => "Fernanda" "apellidos" => "Reinert" ] 5 => array:2 [ "nombre" => "Tácio M.P. de" "apellidos" => "Campos" ] 6 => array:2 [ "nombre" => "Newton C.M." "apellidos" => "Gomes" ] 7 => array:2 [ "nombre" => "Kornelia" "apellidos" => "Smalla" ] ] ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1517838217304616?idApp=UINPBA00004N" "url" => "/15178382/0000004900000004/v1_201810050636/S1517838217304616/v1_201810050636/en/main.assets" ] "en" => array:20 [ "idiomaDefecto" => true "cabecera" => "Environmental Microbiology" "titulo" => "Ammonia determines transcriptional profile of microorganisms in anaerobic digestion" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "770" "paginaFinal" => "776" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Nan Zhang, Huijuan Peng, Yong Li, Wenxiu Yang, Yuneng Zou, Huiguo Duan" "autores" => array:6 [ 0 => array:3 [ "nombre" => "Nan" "apellidos" => "Zhang" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 1 => array:3 [ "nombre" => "Huijuan" "apellidos" => "Peng" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 2 => array:3 [ "nombre" => "Yong" "apellidos" => "Li" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 3 => array:3 [ "nombre" => "Wenxiu" "apellidos" => "Yang" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 4 => array:3 [ "nombre" => "Yuneng" "apellidos" => "Zou" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 5 => array:4 [ "nombre" => "Huiguo" "apellidos" => "Duan" "email" => array:1 [ 0 => "duanhuiguo6@163.com" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] ] "afiliaciones" => array:2 [ 0 => array:3 [ "entidad" => "Neijiang Normal University, College of Life Sciences, Neijiang, China" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Department of Education, Key Laboratory of Regional Characteristic Agricultural Resources, Neijiang, China" "etiqueta" => "b" "identificador" => "aff0010" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author at: No. 705, Dongtong Road, Dongxing District, Neijiang 641100, China." ] ] ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1085 "Ancho" => 1605 "Tamanyo" => 120837 ] ] "descripcion" => array:1 [ "en" => "Fermentation performance under high (HN) and low (LN) NH4+ concentrations. All the data are presented as means±standard deviations (n=3)." ] ] ] "textoCompleto" => "IntroductionAnaerobic digestion (AD) is a promising technology in the field of waste treatment and renewable energy production. Livestock manure has been processed increasingly by AD to reduce pathogens and to generate bioenergy such as methane.<a class="elsevierStyleCrossRefs" href="#bib0150">1,2</a> Thus, the improvement of stability and efficiency of AD is crucial for the comprehensive application of this technology. Ammonia concentration is one of crucial factors regulating AD stability.<a class="elsevierStyleCrossRef" href="#bib0160">3</a> Optimal ammonia concentrations provide sufficient buffer capacity and nutrient for microbial growth, which improves the AD stability and efficiency. However, low or excessive ammonia concentrations usually result in the failure of AD. It is reported that low ammonia concentration (<500mgL−1) decreases methane production, biomass and the aceticlastic methanogenic activity.<a class="elsevierStyleCrossRef" href="#bib0165">4</a> The high ammonia (>4000mgL−1) results in the inhibition of microbial activity and accumulation of volatile fatty acids, which finally causes decreased stability and even failure of AD.<a class="elsevierStyleCrossRefs" href="#bib0160">3–6</a> Due to high protein content in manure, there are usually high ammonia concentrations in the AD of manure.<a class="elsevierStyleCrossRef" href="#bib0160">3</a> Thus, AD of livestock manure has to confront the inhibition from high ammonia. It is necessary to reveal the mechanisms underlying ammonia inhibition on the AD process.Temperature is considered as a prominent factor regulating ammonia toxicity on AD process.<a class="elsevierStyleCrossRefs" href="#bib0160">3,7,8</a> The thermophilic temperatures compared to mesophilic temperatures usually cause higher ammonia toxicity.<a class="elsevierStyleCrossRefs" href="#bib0180">7,8</a> The thermophilic temperatures enhance metabolic activities of microorganisms, which strengthens hydrolysis of substrates including proteins. This process increases ammonia concentration in the slurry, so that ammonia toxicity is undoubtedly strengthened. Thus, under mesophilic temperatures, the ammonia toxicity more depended on the initial ammonia concentration, which facilitates the understanding of the relationship between ammonia concentration and ammonia toxicity. Different methanogens are distinguishably sensitive to ammonia concentrations, which partly determines ammonia toxicity on AD process. Due to spherical Methanosarcina with higher ratio of volume/surface than that of rod-shaped Methanosaeta, the diffusion of ammonia is less into the Methanosarcina than Methanosaeta,<a class="elsevierStyleCrossRef" href="#bib0190">9</a> which results in their different sensitivities to ammonia concentrations. Thus, high ammonia more probably causes failure of AD where Methanosaeta are dominated in the methanogens than that where Methanosarcina are dominated. The recovery of AD from failure depends on a reconstruction of methanogenic species,<a class="elsevierStyleCrossRef" href="#bib0195">10</a> so that Methanosarcina as dominated methanogens replace Methanosaeta. This process probably causes the decrease of acetoclastic methanogenesis.<a class="elsevierStyleCrossRef" href="#bib0200">11</a> These studies of ammonia toxicity on AD process mainly focus on methanogens and methanogenic process.<a class="elsevierStyleCrossRefs" href="#bib0160">3,5,6,12,13</a>Although the ammonia toxicity on AD process has been comprehensively revealed mainly based on methanogenic microflora,<a class="elsevierStyleCrossRefs" href="#bib0160">3,5,12–14</a> the transcriptional profiles of specific pathways and genes in response to ammonia have rarely been discussed. The AD process consists of AD food web (hydrolysis, acidogenesis, acetogenesis and methanogenesis), so besides methanogenesis, the other three steps of the food web also play important roles in final methane production. Thus, the transcriptional profiles of methanogenesis-related processes are necessary to be revealed based on metatranscriptomic analysis, which can provide a new sight underlying ammonia toxicity on AD process.In this study, based on metatranscriptomic analysis, the transcriptional profiles of microbial community in response to low and high NH4+ concentrations, respectively, were revealed in AD. Specifically, we focused on the expressions of pathways and genes responsible for methane production under different NH4+ concentrations to further reveal the mechanism underlying ammonia toxicity on AD process.Materials and methodsSetup of AD systemThe AD experiment of swine manure was conducted with working volume of 2.5L digestion sludge containing 0.75L initial inoculum, and the total solid content was 7% (Supplement Table S1). The high ammonia treatment with NH4+ (5000mgL−1) (HN) and low ammonia treatment with NH4+ (1500mgL−1) (LN) were determined by adding NH4Cl at the beginning of AD, which was mainly based on previous report<a class="elsevierStyleCrossRef" href="#bib0175">6</a> and pre-experiments. All the treatments were conducted in triplicate at 37°C. Seed slurry was prepared by anaerobic digestion of swine manure (obtained from a pig farm in Neijiang, Sichuan Province, China) at 37°C, for one hydraulic retention time (HRT). After methane production reached the first peak (6th day) in the reactor, we performed a semi-continuous feeding mode that 500mL of digestate was exchanged every three days with HRT of 15 days and organic loading rate of 4.5g VS (volatile solid) L−1day−1. The anaerobic digestion was performed for two HRT. The feeding slurry was adjusted to the corresponding NH4+ concentration using NH4Cl. Details about parameters at the start of fermentation were shown in Supplement Table S1.Sampling and analysisAt each feeding, methane content in biogas, volatile fatty acids (VFA), NH4+ and pH were measured to monitor AD dynamic. The methane content in biogas was measured using an Agilent 6890 gas chromatography system (Agilent Technologies, USA), equipped with a thermal conductivity detector and carrier gas of argon. The injection port, column oven, and detector were operated at 100, 70, and 150°C, respectively. The daily volume of biogas was detected by water replacement method. The VFA in the slurry was detected using Agilent 1260 Infinity liquid chromatography (Agilent Technologies, USA), equipped with a differential refraction detector (RID) and mobile phase of H2SO4 (0.005M). Total solid and volatile solid were measured based on previous report.<a class="elsevierStyleCrossRef" href="#bib0220">15</a> NH4+ concentration was quantified with Nessler's reagent colorimetric method.<a class="elsevierStyleCrossRef" href="#bib0225">16</a> At the end of the second HRT, the digestate were sampled in triplicate for total RNA extraction with the RNeasy PowerMicrobiome Kit (Cat. No. 26000-50; MO BIO, USA). The quality of RNA was checked with a NanoDrop 2000 spectrophotometer (Thermo, USA). Ribosomal RNA was removed from the total RNA with the RiboMinusTM kit (Lot. No. 1539791; Invitrogen, USA). The metatranscriptomic (mRNA) sequencing was performed using an Illumina Hiseq 2000 (Illumina Inc., USA). The sequencing raw data from total 6 samples were uploaded to MG-RAST with assigned MG-RAST ID (mgs589946, mgs589949, mgs589952, mgs589955, mgs589958 and mgs589961) for further analysis.<a class="elsevierStyleCrossRef" href="#bib0230">17</a> Prior to the analysis, the quality control pipeline in MG-RAST<a class="elsevierStyleCrossRef" href="#bib0230">17</a> was performed to remove poor quality sequences. The annotation of functional profiles was based on the KEGG Orthologs database including 4 levels. The functional categories was presented as level 2. Level 3 reflected the KEGG pathways, and level 4 (gene expression level) showed expressions of specific genes.<a class="elsevierStyleCrossRef" href="#bib0235">18</a> During annotation analysis, the pipeline parameters were kept at default settings.Statistical analysisThe ammonia effect on the general changes of gene expressions was assessed by principal coordinates analysis (PCoA) in R (<a id="intr0005" class="elsevierStyleInterRef" href="http://www.r-project.org/">http://www.r-project.org/</a>), based on the Bray–Curtis dissimilarity index, using the vegan package. The normality and homoscedasticity of the raw data, and one way analysis of variance (ANOVA) were performed in SPSS 21 software (IBM USA). Spearman's correlation analysis, enrichment analysis and redundancy analysis (RDA) were calculated in R with the vegan package. The Spearman's p value was adjusted using the Benjamini and Hochberg methods.<a class="elsevierStyleCrossRef" href="#bib0240">19</a> The taxa with average relative abundance >0.1% and significantly different expression (p<0.05) between HN and LN were selected for network analysis to reveal co-response to ammonia. If the correlation p value was <0.05, the correlation between two taxa was considered statistically robust and shown in the network. The network was visualized in Cytoscape software.<a class="elsevierStyleCrossRef" href="#bib0245">20</a>ResultsAnaerobic digestion and global expressions of genesThere were significant differences of AD performances between LN and HN (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a> and Supplement Table S1). Methane production and content in the biogas were higher in LN than that in HN (p<0.01). The concentrations of acetic acid and propionic acid, and pH were higher in HN. It showed that high NH4+ concentration inhibited methane production and resulted in some accumulations of VFA. The global expressions of genes showed obvious differences between HN and LN (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>), which well corresponded with the significant differences of performances of AD. Compared with HN, the replicates in LN clustered more closely (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>), which implied that high NH4+ probably caused more randomness of gene expressions in AD.<elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia>Differentiated expressions of metabolic pathwaysIn the comparison between HN and LN based on pathways (level 2), most expressions of these pathways were higher in HN, but only signal transduction was significantly higher at HN (p<0.05) (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>). Surprisingly, only energy metabolism was higher in LN (p<0.01). At level 3, most expressions of pathways were not significantly distinguishable between HN and LN (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). The pathway of methane metabolism (ko00680) (usually indicating the methanogenesis in anaerobic digestion) has a higher expression in LN (p<0.01), but the pathways of RNA polymerase (ko03020) and Valine, leucine and isoleucine degradation (ko00280) had higher expressions in HN (p<0.05) (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). The relative abundances of arginine and proline metabolism (ko00330) and methane metabolism showed positive correlations with daily methane production (p<0.05), but those of RNA polymerase and cell cycle-caulobacter (ko04112) showed negative correlations with methane production (p<0.05) (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>).<elsevierMultimedia ident="fig0015"></elsevierMultimedia><elsevierMultimedia ident="tbl0005"></elsevierMultimedia>In redundancy analysis (RDA) of the relationship between the expressions of pathways (level 3) and the environmental variables (<a class="elsevierStyleCrossRef" href="#fig0020">Fig. 4</a>a), the expressions of the pathways including methane metabolism, arginine and proline metabolism, pentose phosphate pathway (ko00030), histidine metabolism (ko00340), oxidative phosphorylation (ko00190) and pyruvate metabolism (ko00620) positively correlated with methane production. The expressions of RNA degradation (ko030180), pentose and glucuronate interconversions (ko00040) and Citrate cycle (ko00020) positively correlated with acetic acid and pH. The expressions of DNA replication (ko03030) and peroxisome (ko04146) potentially contributed to propionic acid accumulation.<elsevierMultimedia ident="fig0020"></elsevierMultimedia>Gene differentiated expressionsBesides the overall difference of gene expressions (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>), the enrichment analysis was applied to further uncover differentiated expressions of individual genes between HN and LN. Probably attributed to significant difference of the expression of methane metabolism (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>), most of these genes with significant differentiated expressions (p<0.05) were involved in methane metabolism (Supplementary Table S2). These methanogenic genes mainly encode acetyl-CoA decarbonylase and methyl-coenzyme M reductase. Additionally, most of methanogenic genes showed significant positive correlations with methane production (p<0.05) (Supplementary Table S2). Besides methanogenic genes, two genes involved in the pathway of pyruvate metabolism showed higher expressions in LN, but three and two genes involved in aminoacyl-tRNA biosynthesis (ko00970) and ribosome (ko03010), respectively, showed higher expressions in HN (Supplementary Table S2). In the RDA of the relationship between gene expressions and environmental variables (<a class="elsevierStyleCrossRef" href="#fig0020">Fig. 4</a>b), it indicated that besides the methanogenic genes, the genes which encode glycerol kinase, phosphate acetyltransferase, transporting ATPase and pyruvate_orthophosphate dikinase positively contributed to methane production. The genes which encode ribosomal subunits, tRNA_synthetase and phosphoribosylamine_glycine ligase positively contributed to pH and acetic acid.Although there were 19 genes (each taxon with average relative abundance>0.1%) significantly distinguishingly expressed between LN and HN (Supplementary Table S2), the co-expressions of these genes should be further verified. Based on Spearman’ correlations, the co-expressions of these genes to different NH4+ concentrations were further revealed (<a class="elsevierStyleCrossRef" href="#fig0025">Fig. 5</a> and Supplementary Table S3). The expressions of the genes involved in methane metabolism, glycerolipid metabolism, pyruvate metabolism and oxidative phosphorylation showed a co-inhibition under the high ammonia condition. The expressions of methanogenic genes especially the genes which encode acetyl-CoA decarbonylase were comprehensively co-inhibited by high ammonia. However, the expressions of the genes involved in ribosome, aminoacyl-tRNA biosynthesis, purine metabolism, cell cycle-caulobacter and RNA degradation showed co-enhancement under the high ammonia condition. The expressions of more genes were co-inhibited under the high ammonia condition, which supported ammonia toxicity on AD process.<elsevierMultimedia ident="fig0025"></elsevierMultimedia>DiscussionAlthough the hydrolysis of substrates would cause variations of ammonia concentrations during AD, in this study the operations of ammonia addition in HN and LN created distinct ammonia pressures to differentiate AD performances and microbial gene expression (<a class="elsevierStyleCrossRefs" href="#fig0005">Figs. 1 and 2</a>). High ammonia significantly inhibited AD process by decreasing methane production and content in the biogas, and the accumulations of VFA. The decreased methane content in biogas not only resulted in a low methane production but also indicated a mass of byproducts. The accumulations of VFA, especially acetic acid, implied a potential inhibition of acetoclastic methanogenesis, which agreed well with previous reports.<a class="elsevierStyleCrossRefs" href="#bib0160">3,5</a> Although the accumulations of VFA were observed in HN, such accumulations unlikely caused excessive acidification in AD, which was further supported by the pH value (7.8±0.5). Additionally, the ammonia inhibition more probably occurred under thermophilic temperatures than mesophilic condition (37°C).<a class="elsevierStyleCrossRef" href="#bib0160">3</a> Thus, in this study, the inhibition of AD process was supposed to be directly attributed to ammonia toxicity on microbial activities, rather than other environmental factors regulated by ammonia.The microbial activities were obviously regulated by ammonia, which was supported by the PCoA result (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>). In level 2 pathways, the expressions of energy metabolism and signal transduction were significantly influenced (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>). The AD actually is an energy metabolism process during which energy is transferred and transformed through various metabolic pathways especially the methanogenic pathways. The energy metabolism mainly including methane metabolism usually couples to actual methane production,<a class="elsevierStyleCrossRefs" href="#bib0150">1,21</a> so the inhibited expression of energy metabolism mainly resulted in the low methane production in HN. Signal transduction is usually involved in modulating cell behaviors in response to environmental pressures such as pH and ammonia.<a class="elsevierStyleCrossRefs" href="#bib0255">22,23</a> Thus, a higher expression of this pathway in HN could be explained. The obviously higher expression of cell motility in HN coupled to that of signal transduction, which agreed with previous report.<a class="elsevierStyleCrossRef" href="#bib0265">24</a> This further supported microbial response to ammonia by behaviors or movements. Unexpectedly, in HN only the expression of energy metabolism was depressed, but other pathways had higher expressions compared to that in LN (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>). In consideration of that methanogens are not dominant microorganisms compared to bacteria such as Firmicutes, Bacteroidetes and Proteobacteria in AD,<a class="elsevierStyleCrossRef" href="#bib0270">25</a> it is reasonable to deduce that these pathways except energy metabolism were mainly conducted by bacteria. Thus, the higher expressions of these pathways in HN probably indicated high activities of bacteria under high ammonia condition. This was likely because ammonia could improve nutrient of nitrogen for bacterial growth.<a class="elsevierStyleCrossRef" href="#bib0165">4</a> In level 3, the most significantly differentiated expressions between HN and LN was methane metabolism (p=0.003) which positively correlated with methane production (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). Most of the other pathways had no significant expression differences. Interestingly, only the expressions of methane metabolism, oxidative phosphorylation and pyruvate metabolism were higher in LN and positively contributed to methane production (<a class="elsevierStyleCrossRef" href="#fig0020">Fig. 4</a> and <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>), but the other pathways had higher expressions in HN. This situation was similar with that of level 2. This further confirmed that high ammonia provided some improvements to substrate metabolisms mainly conducted by bacteria, but inhibited methanogenic activity. Consequently, although each step of AD food web played crucial roles in actual methane production, the ammonia toxicity on AD process mainly targeted methanogenic process to inhibit methane production.Ammonia inhibition on methanogenic process would result in a shift in methanogenic acetate utilization from direct acetate cleavage toward syntrophic acetate oxidation.<a class="elsevierStyleCrossRefs" href="#bib0200">11,26</a> This was mainly attributed to the greatly decreased abundance of acetoclastic Methanosaeta under high ammonia condition.<a class="elsevierStyleCrossRef" href="#bib0200">11</a> However, whether the expressions of genes involved in acetoclastic methanogenesis were reduced should be revealed. In methanogenic pathway, only the expressions of the genes which encode acetyl-CoA decarbonylase and methyl-coenzyme M reductase were significantly higher in LN (p<0.05), and showed positive correlations with methane production (p<0.05). Acetyl-CoA decarbonylase plays an important role in acetoclastic pathway<a class="elsevierStyleCrossRef" href="#bib0280">27</a> and methyl-coenzyme M reductase is the key enzyme in methanogenesis.<a class="elsevierStyleCrossRef" href="#bib0285">28</a> Thus, the higher expressions of these genes encoding the two enzymes undoubtedly improved methane production. The expressions of genes which encode acetyl-CoA decarbonylase were significantly depressed in HN, indicating that the acetoclastic methanogenesis was inhibited. Based on transcriptional profile, the ammonia toxicity on acetoclastic methanogenesis was further revealed. Additionally, ammonia inhibited methanogens’ activities also probably by depressing the expressions of genes which encode methyl-coenzyme M reductase. Besides methanogenic genes, the genes involved in pyruvate metabolism had significantly higher expressions in HN, which probably improved the production of acetyl-CoA.<a class="elsevierStyleCrossRef" href="#bib0290">29</a> The genes involved in aminoacyl-tRNA biosynthesis and ribosome were significantly higher expressed in HN, indicating that ammonia potentially facilitated translation process.<a class="elsevierStyleCrossRef" href="#bib0210">13</a>Although the expressions of individual key genes could generally explain the ammonia toxicity on AD process, gene co-expressions in response to ammonia probably provided a systemic sight. The inhibition of the co-expressions of the genes involved in methane metabolism, glycerolipid metabolism, pyruvate metabolism and oxidative phosphorylation indicated that these pathways probably performed a cooperation to regulate AD efficiency that was mainly represented by methane production. The coupling relationship between methane metabolism and oxidative phosphorylation has been revealed before.<a class="elsevierStyleCrossRef" href="#bib0150">1</a> The glycerolipid metabolism and pyruvate metabolism probably provided potential substrates<a class="elsevierStyleCrossRef" href="#bib0290">29</a> for methanogenesis. Interestingly, nearly all the genes which encode acetyl-CoA decarbonylase showed inhibition of co-expressions under the high ammonia condition, which further demonstrated that acetoclastic methanogenesis were inhibited by high ammonia. This also showed that these genes compared to other methanogenic genes were unitedly and highly sensitive to NH4+ concentration. These genes could be used as potential indicators for ammonia toxicity on AD process. Additionally, the in inhibition of co-expression of the genes which encode acetyl-CoA decarbonylase and methyl-coenzyme M reductase, indicating the cooperation of the two enzymes in methanogenesis.Consequently, except methanogenesis, most of pathways were not significantly influenced by high ammonia concentration, so that they were probably not the key factors contributing to decreased methane production. Thus, ammonia toxicity on AD process mainly targeted methanogenic process by inhibiting the expressions of genes which encode acetyl-CoA decarbonylase and methyl-coenzyme M reductase to finally decrease methane production. This study revealed mechanisms underlying microbial response to ammonia pressure based on gene expressions, and further discovered ammonia inhibition only targeting on the genes encoding the above two enzymes. However, the adaptions of microbial gene expressions to ammonia pressure during longtime AD also should be considered in the future work.Conflicts of interestAuthors declare that they have no competing interests." "textoCompletoSecciones" => array:1 [ "secciones" => array:9 [ 0 => array:3 [ "identificador" => "xres1091242" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1034364" "titulo" => "Keywords" ] 2 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 3 => array:3 [ "identificador" => "sec0010" "titulo" => "Materials and methods" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Setup of AD system" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Sampling and analysis" ] 2 => array:2 [ "identificador" => "sec0025" "titulo" => "Statistical analysis" ] ] ] 4 => array:3 [ "identificador" => "sec0030" "titulo" => "Results" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0035" "titulo" => "Anaerobic digestion and global expressions of genes" ] 1 => array:2 [ "identificador" => "sec0040" "titulo" => "Differentiated expressions of metabolic pathways" ] 2 => array:2 [ "identificador" => "sec0045" "titulo" => "Gene differentiated expressions" ] ] ] 5 => array:2 [ "identificador" => "sec0050" "titulo" => "Discussion" ] 6 => array:2 [ "identificador" => "sec0055" "titulo" => "Conflicts of interest" ] 7 => array:2 [ "identificador" => "xack370732" "titulo" => "Acknowledgements" ] 8 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2017-09-25" "fechaAceptado" => "2018-04-13" "PalabrasClave" => array:1 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1034364" "palabras" => array:5 [ 0 => "Anaerobic digestion" 1 => "Ammonia" 2 => "Pathway" 3 => "Gene expression" 4 => "Methanogenesis" ] ] ] ] "tieneResumen" => true "resumen" => array:1 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "Anaerobic digestion is important for the management of livestock manure with high ammonia level. Although ammonia effects on anaerobic digestion have been comprehensively studied, the molecular mechanism underlying ammonia inhibition still remains elusive. In this study, based on metatranscriptomic analysis, the transcriptional profile of microbial community in anaerobic digestion under low (1500mgL−1) and high NH4+ (5000mgL−1) concentrations, respectively, were revealed. The results showed that high NH4+ concentrations significantly inhibited methane production but facilitated the accumulations of volatile fatty acids. The expression of methanogenic pathway was significantly inhibited by high NH4+ concentration but most of the other pathways were not significantly affected. Furthermore, the expressions of methanogenic genes which encode acetyl-CoA decarbonylase and methyl-coenzyme M reductase were significantly inhibited by high NH4+ concentration. The inhibition of the co-expressions of the genes which encode acetyl-CoA decarbonylase was observed. Some genes involved in the pathways of aminoacyl-tRNA biosynthesis and ribosome were highly expressed under high NH4+ concentration. Consequently, the ammonia inhibition on anaerobic digestion mainly focused on methanogenic process by suppressing the expressions of genes which encode acetyl-CoA decarbonylase and methyl-coenzyme M reductase. This study improved the accuracy and depth of understanding ammonia inhibition on anaerobic digestion." ] ] "apendice" => array:1 [ 0 => array:1 [ "seccion" => array:1 [ 0 => array:4 [ "apendice" => "The following are the supplementary data to this article:<elsevierMultimedia ident="upi0005"></elsevierMultimedia>" "etiqueta" => "Appendix A" "titulo" => "Supplementary data" "identificador" => "sec0065" ] ] ] ] "multimedia" => array:7 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1085 "Ancho" => 1605 "Tamanyo" => 120837 ] ] "descripcion" => array:1 [ "en" => "Fermentation performance under high (HN) and low (LN) NH4+ concentrations. All the data are presented as means±standard deviations (n=3)." ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Fig. 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 521 "Ancho" => 1578 "Tamanyo" => 41863 ] ] "descripcion" => array:1 [ "en" => "The principal coordinates analysis (PCoA) of global expressions of genes in anaerobic digestions with high NH4+ (HN) and low NH4+ (LN)." ] ] 2 => array:7 [ "identificador" => "fig0015" "etiqueta" => "Fig. 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 2287 "Ancho" => 1584 "Tamanyo" => 216382 ] ] "descripcion" => array:1 [ "en" => "Expression profiles of level 2 at high NH4+ (HN) and low NH4+ (LN). ** significant at p<0.01; * Significant at p<0.05." ] ] 3 => array:7 [ "identificador" => "fig0020" "etiqueta" => "Fig. 4" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr4.jpeg" "Alto" => 993 "Ancho" => 3046 "Tamanyo" => 233538 ] ] "descripcion" => array:1 [ "en" => "Redundancy analysis (RDA) of key pathway (a) and gene (b) expressions where the methanogenic genes mainly encoding acetyl-CoA decarbonylase and methyl-coenzyme M reductase positively contribute to methane production but are omitted to simplify the figure to be clearer." ] ] 4 => array:7 [ "identificador" => "fig0025" "etiqueta" => "Fig. 5" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr5.jpeg" "Alto" => 1818 "Ancho" => 1646 "Tamanyo" => 202808 ] ] "descripcion" => array:1 [ "en" => "Networks of gene expressions negatively (a) and positively (b) responding to ammonia. The taxa with average relative abundance >0.1% and significant differentiated expressions between LN and HN are shown." ] ] 5 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at1" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:3 [ "leyenda" => "Taxa with average relative abundance >1% are shown. The p values represent the significance from the comparison of the relative abundances of pathways under high and low NH4+ concentrations." "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Level 3 \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Low NH4+ \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">High NH4+ \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">p values \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">ABC transporters [PATH:ko02010] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4.66±0.21 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4.76±0.37 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.757 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Alanine, aspartate and glutamate metabolism [PATH:ko00250] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.44±0.2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.7±0.29 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.365 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Aminoacyl-tRNA biosynthesis [PATH:ko00970] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.31±0.11 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.51±0.19 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.270 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Arginine and proline metabolism [PATH:ko00330]<a class="elsevierStyleCrossRef" href="#tblfn0005">a</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.31±0.08 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.21±0.08 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.299 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Bacterial chemotaxis [PATH:ko02030] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.11±0.12 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.26±0.2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.405 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Bacterial secretion system [PATH:ko03070] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.37±0.1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.4±0.13 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.813 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Cell cycle-caulobacter [PATH:ko04112]<a class="elsevierStyleCrossRef" href="#tblfn0005">a</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.45±0.11 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.64±0.01 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.069 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Citrate cycle (TCA cycle) [PATH:ko00020] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.3±0.06 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.39±0.08 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.294 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Cysteine and methionine metabolism [PATH:ko00270] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.16±0.18 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.15±0.07 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.955 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">DNA replication [PATH:ko03030] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.05±0.13 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.21±0.18 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.366 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Flagellar assembly [PATH:ko02040] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">6.65±0.86 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">7.88±1.69 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.414 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Glycine, serine and threonine metabolism [PATH:ko00260] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.27±0.21 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.36±0.26 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.716 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Glycolysis/Gluconeogenesis [PATH:ko00010] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.73±0.09 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.9±0.14 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.208 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">HIF-1 signaling pathway [PATH:ko04066] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.67±0.07 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.17±0.34 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.109 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Histidine metabolism [PATH:ko00340] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.07±0.09 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.95±0.07 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.200 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Methane metabolism [PATH:ko00680]<a class="elsevierStyleCrossRef" href="#tblfn0005">a</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">10.96±0.57 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">6.52±0.83 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.003 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Oxidative phosphorylation [PATH:ko00190] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">6.4±1.28 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4.22±0.67 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.100 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Pentose and glucuronate interconversions [PATH:ko00040] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.04±0.06 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.97±0.12 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.483 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Pentose phosphate pathway [PATH:ko00030] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.15±0.08 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.21±0.09 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.524 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Peroxisome [PATH:ko04146] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.97±0.31 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.54±0.31 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.142 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Plant-pathogen interaction [PATH:ko04626] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.43±0.04 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.46±0.05 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.597 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Purine metabolism [PATH:ko00230] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.42±0.19 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.07±0.3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.062 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Pyruvate metabolism [PATH:ko00620] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.12±0.21 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.69±0.11 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.063 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ribosome [PATH:ko03010] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">8.5±0.26 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">9.6±0.74 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.117 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">RNA degradation [PATH:ko03018] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.64±0.2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4.11±0.18 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.063 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">RNA polymerase [PATH:ko03020]<a class="elsevierStyleCrossRef" href="#tblfn0010">b</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.7±0.02 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.98±0.13 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.038 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Two-component system [PATH:ko02020] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.54±0.1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.61±0.07 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.465 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Valine, leucine and isoleucine degradation [PATH:ko00280] \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.48±0.08 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.7±0.03 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.027 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1865899.png" ] ] ] "notaPie" => array:2 [ 0 => array:3 [ "identificador" => "tblfn0005" "etiqueta" => "a" "nota" => "Indicates significant correlations (p<0.05) between the relative abundances of pathways with daily methane production." ] 1 => array:3 [ "identificador" => "tblfn0010" "etiqueta" => "b" "nota" => "p<0.01." ] ] ] "descripcion" => array:1 [ "en" => "Relative abundances of level 3 pathways under high and low NH4+ concentrations." ] ] 6 => array:5 [ "identificador" => "upi0005" "tipo" => "MULTIMEDIAECOMPONENTE" "mostrarFloat" => false "mostrarDisplay" => true "Ecomponente" => array:2 [ "fichero" => "mmc1.xlsx" "ficheroTamanyo" => 30441 ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:29 [ 0 => array:3 [ "identificador" => "bib0150" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Temperature regulates methane production through the function centralization of microbial community in anaerobic digestion" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:5 [ 0 => "Q. Lin" 1 => "J. De Vrieze" 2 => "G. He" 3 => "X. Li" 4 => "J. Li" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1016/j.biortech.2016.05.046" "Revista" => array:6 [ "tituloSerie" => "Bioresour Technol" "fecha" => "2016" "volumen" => "216" "paginaInicial" => "150" "paginaFinal" => "158" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/27236402" "web" => "Medline" ] ] ] ] ] ] ] ] 1 => array:3 [ "identificador" => "bib0155" "etiqueta" => "2" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Mechanisms and effects of arsanilic acid on antibiotic resistance genes and microbial communities during pig manure digestion" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:6 [ 0 => "W. Sun" 1 => "X. Qian" 2 => "J. Gu" 3 => "X.J. Wang" 4 => "L. Zhang" 5 => "A.Y. Guo" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1016/j.biortech.2017.03.025" "Revista" => array:6 [ "tituloSerie" => "Bioresour Technol" "fecha" => "2017" "volumen" => "234" "paginaInicial" => "217" "paginaFinal" => "223" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/28319770" "web" => "Medline" ] ] ] ] ] ] ] ] 2 => array:3 [ "identificador" => "bib0160" "etiqueta" => "3" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "A critical review on inhibition of anaerobic digestion process by excess ammonia" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 0 => "R. Rajagopal" 1 => "D.I. Masse" 2 => "G. Singh" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1016/j.biortech.2013.06.030" "Revista" => array:6 [ "tituloSerie" => "Bioresour Technol" "fecha" => "2013" "volumen" => "143" "paginaInicial" => "632" "paginaFinal" => "641" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/23835276" "web" => "Medline" ] ] ] ] ] ] ] ] 3 => array:3 [ "identificador" => "bib0165" "etiqueta" => "4" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Stability and inhibition of anaerobic processes caused by insufficiency or excess of ammonia nitrogen" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:4 [ 0 => "J. Prochazka" 1 => "P. Dolejs" 2 => "J. Maca" 3 => "M. Dohanyos" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1007/s00253-011-3625-4" "Revista" => array:6 [ "tituloSerie" => "Appl Microbiol Biotechnol" "fecha" => "2012" "volumen" => "93" "paginaInicial" => "439" "paginaFinal" => "447" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/22002069" "web" => "Medline" ] ] ] ] ] ] ] ] 4 => array:3 [ "identificador" => "bib0170" "etiqueta" => "5" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Inhibition of anaerobic digestion process: a review" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 0 => "Y. Chen" 1 => "J.J. Cheng" 2 => "K.S. Creamer" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1016/j.biortech.2007.01.057" "Revista" => array:6 [ "tituloSerie" => "Bioresour Technol" "fecha" => "2008" "volumen" => "99" "paginaInicial" => "4044" "paginaFinal" => "4064" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/17399981" "web" => "Medline" ] ] ] ] ] ] ] ] 5 => array:3 [ "identificador" => "bib0175" "etiqueta" => "6" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Ammonium inhibition through the decoupling of acidification process and methanogenesis in anaerobic digester revealed by high throughput sequencing" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:5 [ 0 => "M. Zhang" 1 => "Q. Lin" 2 => "J. Rui" 3 => "J. Li" 4 => "X. Li" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:4 [ "tituloSerie" => "Biotechnol Lett" "fecha" => "2016" "paginaInicial" => "1" "paginaFinal" => "6" ] ] ] ] ] ] 6 => array:3 [ "identificador" => "bib0180" "etiqueta" => "7" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Anaerobic digestion of slaughterhouse by-products" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "A. Hejnfelt" 1 => "I. Angelidaki" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:5 [ "tituloSerie" => "Biomass Bioenergy" "fecha" => "2009" "volumen" => "33" "paginaInicial" => "1046" "paginaFinal" => "1054" ] ] ] ] ] ] 7 => array:3 [ "identificador" => "bib0185" "etiqueta" => "8" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Ammonia inhibition in high-solids biogasification: an overview and practical solutions" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:1 [ 0 => "M. Kayhanian" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:5 [ "tituloSerie" => "Environ Technol" "fecha" => "1999" "volumen" => "20" "paginaInicial" => "355" "paginaFinal" => "365" ] ] ] ] ] ] 8 => array:3 [ "identificador" => "bib0190" "etiqueta" => "9" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "The mechanism of ammonia inhibition in the thermophilic digestion of livestock wastes" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "W. Wiegant" 1 => "G. Zeeman" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:5 [ "tituloSerie" => "Agric Wastes" "fecha" => "1986" "volumen" => "16" "paginaInicial" => "243" "paginaFinal" => "253" ] ] ] ] ] ] 9 => array:3 [ "identificador" => "bib0195" "etiqueta" => "10" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Influence of environmental conditions on methanogenic compositions in anaerobic biogas reactors" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 0 => "D. Karakashev" 1 => "D.J. Batstone" 2 => "I. Angelidaki" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:5 [ "tituloSerie" => "Appl Environ Microb" "fecha" => "2005" "volumen" => "71" "paginaInicial" => "331" "paginaFinal" => "338" ] ] ] ] ] ] 10 => array:3 [ "identificador" => "bib0200" "etiqueta" => "11" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Ammonia, a selective agent for methane production by syntrophic acetate oxidation at mesophilic temperature" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "A. Schnurer" 1 => "A. Nordberg" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.2166/wst.2008.097" "Revista" => array:6 [ "tituloSerie" => "Water Sci Technol" "fecha" => "2008" "volumen" => "57" "paginaInicial" => "735" "paginaFinal" => "740" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/18401146" "web" => "Medline" ] ] ] ] ] ] ] ] 11 => array:3 [ "identificador" => "bib0205" "etiqueta" => "12" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Effect of ammonia on the anaerobic degradation of protein by a mesophilic and thermophilic biowaste population" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 0 => "C. Gallert" 1 => "S. Bauer" 2 => "J. Winter" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:6 [ "tituloSerie" => "Appl Microbiol Biotechnol" "fecha" => "1998" "volumen" => "50" "paginaInicial" => "495" "paginaFinal" => "501" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/9830101" "web" => "Medline" ] ] ] ] ] ] ] ] 12 => array:3 [ "identificador" => "bib0210" "etiqueta" => "13" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Aminoacyl-tRNA synthesis" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "M. Ibba" 1 => "D. Soll" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1146/annurev.biochem.69.1.617" "Revista" => array:6 [ "tituloSerie" => "Annu Rev Biochem" "fecha" => "2000" "volumen" => "69" "paginaInicial" => "617" "paginaFinal" => "650" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/10966471" "web" => "Medline" ] ] ] ] ] ] ] ] 13 => array:3 [ "identificador" => "bib0215" "etiqueta" => "14" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Mitigating ammonia inhibition of thermophilic anaerobic treatment of digested piggery wastewater: use of pH reduction, zeolite, biomass and humic acid" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "L. Ho" 1 => "G. Ho" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1016/j.watres.2012.05.016" "Revista" => array:6 [ "tituloSerie" => "Water Res" "fecha" => "2012" "volumen" => "46" "paginaInicial" => "4339" "paginaFinal" => "4350" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/22739499" "web" => "Medline" ] ] ] ] ] ] ] ] 14 => array:3 [ "identificador" => "bib0220" "etiqueta" => "15" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Standard Methods for the Examination of Water and Wastewater" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:1 [ 0 => "APHA" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Libro" => array:3 [ "fecha" => "1998" "editorial" => "American Public Health Association" "editorialLocalizacion" => "Washington, DC" ] ] ] ] ] ] 15 => array:3 [ "identificador" => "bib0225" "etiqueta" => "16" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Nitrogen mineralization, immobilization, and nitrification" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:4 [ 0 => "S.C. Hart" 1 => "J.M. Stark" 2 => "E.A. Davidson" 3 => "M.K. Firestone" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:5 [ "tituloSerie" => "Soil Sci Soc Am J" "fecha" => "1994" "volumen" => "44" "paginaInicial" => "985" "paginaFinal" => "1018" ] ] ] ] ] ] 16 => array:3 [ "identificador" => "bib0230" "etiqueta" => "17" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:3 [ 0 => "F. Meyer" 1 => "D. Paarmann" 2 => "M. D'Souza" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1186/1471-2105-9-1" "Revista" => array:6 [ "tituloSerie" => "BMC Bioinformatics" "fecha" => "2008" "volumen" => "9" "paginaInicial" => "1" "paginaFinal" => "8" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/18173834" "web" => "Medline" ] ] ] ] ] ] ] ] 17 => array:3 [ "identificador" => "bib0235" "etiqueta" => "18" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Metagenomic and metatranscriptomic analysis of microbial community structure and gene expression of activated sludge" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "K. Yu" 1 => "T. Zhang" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1371/journal.pone.0038183" "Revista" => array:5 [ "tituloSerie" => "PLoS ONE" "fecha" => "2012" "volumen" => "7" "paginaInicial" => "e38183" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/22666477" "web" => "Medline" ] ] ] ] ] ] ] ] 18 => array:3 [ "identificador" => "bib0240" "etiqueta" => "19" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Controlling the false discovery rate: a practical and powerful approach to multiple testing" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "Y. Benjamini" 1 => "Y. Hochberg" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:5 [ "tituloSerie" => "J R Stat Soc B" "fecha" => "1995" "volumen" => "57" "paginaInicial" => "289" "paginaFinal" => "300" ] ] ] ] ] ] 19 => array:3 [ "identificador" => "bib0245" "etiqueta" => "20" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Cytoscape: a software environment for integrated models of biomolecular interaction networks" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:3 [ 0 => "P. Shannon" 1 => "A. Markiel" 2 => "O. Ozier" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1101/gr.1239303" "Revista" => array:6 [ "tituloSerie" => "Genome Res" "fecha" => "2003" "volumen" => "13" "paginaInicial" => "2498" "paginaFinal" => "2504" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/14597658" "web" => "Medline" ] ] ] ] ] ] ] ] 20 => array:3 [ "identificador" => "bib0250" "etiqueta" => "21" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Methane yield phenotypes linked to differential gene expression in the sheep rumen microbiome" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:3 [ 0 => "W.B. Shi" 1 => "C.D. Moon" 2 => "S.C. Leahy" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1101/gr.168245.113" "Revista" => array:6 [ "tituloSerie" => "Genome Res" "fecha" => "2014" "volumen" => "24" "paginaInicial" => "1517" "paginaFinal" => "1525" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/24907284" "web" => "Medline" ] ] ] ] ] ] ] ] 21 => array:3 [ "identificador" => "bib0255" "etiqueta" => "22" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Adaptation to pH and role of PacC in the rice blast fungus Magnaporthe oryzae" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:5 [ 0 => "P. Landraud" 1 => "S. Chuzeville" 2 => "G. Billon-Grande" 3 => "N. Poussereau" 4 => "C. Bruel" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:3 [ "tituloSerie" => "PLoS ONE" "fecha" => "2013" "paginaInicial" => "8" ] ] ] ] ] ] 22 => array:3 [ "identificador" => "bib0260" "etiqueta" => "23" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Multiple two-component systems modulate alkali generation in Streptococcus gordonii in response to environmental stresses" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "Y.L. Liu" 1 => "R.A. Burne" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1128/JB.01053-09" "Revista" => array:6 [ "tituloSerie" => "J Bacteriol" "fecha" => "2009" "volumen" => "191" "paginaInicial" => "7353" "paginaFinal" => "7362" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/19783634" "web" => "Medline" ] ] ] ] ] ] ] ] 23 => array:3 [ "identificador" => "bib0265" "etiqueta" => "24" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Weak magnetic field: a powerful strategy to enhance partial nitrification" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:3 [ 0 => "Z.B. Wang" 1 => "X.L. Liu" 2 => "S.Q. Ni" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1016/j.watres.2017.04.058" "Revista" => array:6 [ "tituloSerie" => "Water Res" "fecha" => "2017" "volumen" => "120" "paginaInicial" => "190" "paginaFinal" => "198" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/28486170" "web" => "Medline" ] ] ] ] ] ] ] ] 24 => array:3 [ "identificador" => "bib0270" "etiqueta" => "25" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Ammonia and temperature determine potential clustering in the anaerobic digestion microbiome" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:3 [ 0 => "J. De Vrieze" 1 => "A.M. Saunders" 2 => "Y. He" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1016/j.watres.2015.02.025" "Revista" => array:6 [ "tituloSerie" => "Water Res" "fecha" => "2015" "volumen" => "75" "paginaInicial" => "312" "paginaFinal" => "323" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/25819618" "web" => "Medline" ] ] ] ] ] ] ] ] 25 => array:3 [ "identificador" => "bib0275" "etiqueta" => "26" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Methanogenic population dynamics during startup of a full-scale anaerobic sequencing batch reactor treating swine waste" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 0 => "L.T. Angenent" 1 => "S.W. Sung" 2 => "L. Raskin" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:6 [ "tituloSerie" => "Water Res" "fecha" => "2002" "volumen" => "36" "paginaInicial" => "4648" "paginaFinal" => "4654" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/12418668" "web" => "Medline" ] ] ] ] ] ] ] ] 26 => array:3 [ "identificador" => "bib0280" "etiqueta" => "27" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Structure of the α2¿2 Ni-dependent CO dehydrogenase component of the Methanosarcina barkeri acetyl-CoA decarbonylase/synthase complex" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:3 [ 0 => "W. Gong" 1 => "B. Hao" 2 => "Z. Wei" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1073/pnas.0800415105" "Revista" => array:6 [ "tituloSerie" => "Proc Natl Acad Sci USA" "fecha" => "2008" "volumen" => "105" "paginaInicial" => "9558" "paginaFinal" => "9563" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/18621675" "web" => "Medline" ] ] ] ] ] ] ] ] 27 => array:3 [ "identificador" => "bib0285" "etiqueta" => "28" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Crystal structure of methyl coenzyme M reductase: the key enzyme of biological methane formation" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:5 [ 0 => "U. Ermler" 1 => "W. Grabarse" 2 => "S. Shima" 3 => "M. Goubeaud" 4 => "R.K. Thauer" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:6 [ "tituloSerie" => "Science" "fecha" => "1997" "volumen" => "278" "paginaInicial" => "1457" "paginaFinal" => "1462" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/9367957" "web" => "Medline" ] ] ] ] ] ] ] ] 28 => array:3 [ "identificador" => "bib0290" "etiqueta" => "29" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Synthesis of cell constituents from C2-units by a modified tricarboxylic acid cycle" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "H. Kornberg" 1 => "H. Krebs" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:6 [ "tituloSerie" => "Nature" "fecha" => "1957" "volumen" => "179" "paginaInicial" => "988" "paginaFinal" => "991" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/13430766" "web" => "Medline" ] ] ] ] ] ] ] ] ] ] ] ] "agradecimientos" => array:1 [ 0 => array:4 [ "identificador" => "xack370732" "titulo" => "Acknowledgements" "texto" => "This work was supported by the Key Project of Education Department of Sichuan Province (No. 17ZA0215) and Major Cultivation Project of Education Department of Sichuan Province (No. 17CZ0018)." "vista" => "all" ] ] ] "idiomaDefecto" => "en" "url" => "/15178382/0000004900000004/v1_201810050636/S1517838217309267/v1_201810050636/en/main.assets" "Apartado" => array:4 [ "identificador" => "47987" "tipo" => "SECCION" "en" => array:2 [ "titulo" => "Environmental Microbiology" "idiomaDefecto" => true ] "idiomaDefecto" => "en" ] "PDF" => "https://static.elsevier.es/multimedia/15178382/0000004900000004/v1_201810050636/S1517838217309267/v1_201810050636/en/main.pdf?idApp=UINPBA00004N&text.app=https://www.elsevier.es/" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1517838217309267?idApp=UINPBA00004N"]

Statistics

Environmental Microbiology

Nan Zhanga,b, Huijuan Penga,b, Yong Lia,b, Wenxiu Yanga, Yuneng Zoua, Huiguo Duana,

Corresponding author

duanhuiguo6@163.com

Corresponding author at: No. 705, Dongtong Road, Dongxing District, Neijiang 641100, China.

a Neijiang Normal University, College of Life Sciences, Neijiang, China

b Department of Education, Key Laboratory of Regional Characteristic Agricultural Resources, Neijiang, China

Read

2419

Times
was read the article

760

Total PDF

1659

Total HTML

Share statistics

 array:23 [
  "pii" => "S1517838217309267"
  "issn" => "15178382"
  "doi" => "10.1016/j.bjm.2018.04.008"
  "estado" => "S300"
  "fechaPublicacion" => "2018-10-01"
  "aid" => "405"
  "copyrightAnyo" => "2018"
  "documento" => "article"
  "crossmark" => 1
  "licencia" => "http://creativecommons.org/licenses/by-nc-nd/4.0/"
  "subdocumento" => "fla"
  "cita" => "Braz J Microbiol. 2018;49:770-6"
  "abierto" => array:3 [
    "ES" => true
    "ES2" => true
    "LATM" => true
  ]
  "gratuito" => true
  "lecturas" => array:2 [
    "total" => 468
    "formatos" => array:3 [
      "EPUB" => 81
      "HTML" => 186
      "PDF" => 201
    ]
  ]
  "itemSiguiente" => array:19 [
    "pii" => "S151783821730802X"
    "issn" => "15178382"
    "doi" => "10.1016/j.bjm.2018.01.003"
    "estado" => "S300"
    "fechaPublicacion" => "2018-10-01"
    "aid" => "362"
    "copyright" => "Sociedade Brasileira de Microbiologia"
    "documento" => "article"
    "crossmark" => 1
    "licencia" => "http://creativecommons.org/licenses/by-nc-nd/4.0/"
    "subdocumento" => "fla"
    "cita" => "Braz J Microbiol. 2018;49:777-84"
    "abierto" => array:3 [
      "ES" => true
      "ES2" => true
      "LATM" => true
    ]
    "gratuito" => true
    "lecturas" => array:2 [
      "total" => 565
      "formatos" => array:3 [
        "EPUB" => 98
        "HTML" => 247
        "PDF" => 220
      ]
    ]
    "en" => array:12 [
      "idiomaDefecto" => true
      "cabecera" => "<span class="elsevierStyleTextfn">Veterinary Microbiology</span>"
      "titulo" => "Molecular characterization of feline calicivirus variants from multicat household and public animal shelter in Rio de Janeiro&#44; Brazil"
      "tienePdf" => "en"
      "tieneTextoCompleto" => "en"
      "tieneResumen" => "en"
      "paginas" => array:1 [
        0 => array:2 [
          "paginaInicial" => "777"
          "paginaFinal" => "784"
        ]
      ]
      "contieneResumen" => array:1 [
        "en" => true
      ]
      "contieneTextoCompleto" => array:1 [
        "en" => true
      ]
      "contienePdf" => array:1 [
        "en" => true
      ]
      "resumenGrafico" => array:2 [
        "original" => 0
        "multimedia" => array:7 [
          "identificador" => "fig0005"
          "etiqueta" => "Fig&#46; 1"
          "tipo" => "MULTIMEDIAFIGURA"
          "mostrarFloat" => true
          "mostrarDisplay" => false
          "figura" => array:1 [
            0 => array:4 [
              "imagen" => "gr1.jpeg"
              "Alto" => 3834
              "Ancho" => 3083
              "Tamanyo" => 1376154
            ]
          ]
          "descripcion" => array:1 [
            "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">ML trees of feline calicivirus isolated in this study along with most of the FCV prototypes available so far based on the ORF2 nucleotide sequences&#46; &#40;A&#41; Phylogenetic tree of a 467<span class="elsevierStyleHsp" style=""></span>bp partial fragment of the capsid conserved region A-B&#59; &#40;B&#41; phylogenetic tree of a 529<span class="elsevierStyleHsp" style=""></span>bp partial fragment of the capsid variable region C-F&#46; Isolates from this study are represented with black circles and prototypes from Southern Brazil are represented with&#42;&#46;</p>"
          ]
        ]
      ]
      "autores" => array:1 [
        0 => array:2 [
          "autoresLista" => "Joylson de Jesus Pereira, Natasha Baumworcel, J&#250;lia Monassa Fioretti, Cinthya Fonseca Domingues, La&#237;s Fernandes de Moraes, Robson dos Santos Souza Marinho, Maria Clara Rodrigues Vieira, Ana Maria Viana Pinto, Tatiana Xavier de Castro"
          "autores" => array:9 [
            0 => array:2 [
              "nombre" => "Joylson de Jesus"
              "apellidos" => "Pereira"
            ]
            1 => array:2 [
              "nombre" => "Natasha"
              "apellidos" => "Baumworcel"
            ]
            2 => array:2 [
              "nombre" => "J&#250;lia Monassa"
              "apellidos" => "Fioretti"
            ]
            3 => array:2 [
              "nombre" => "Cinthya Fonseca"
              "apellidos" => "Domingues"
            ]
            4 => array:2 [
              "nombre" => "La&#237;s Fernandes de"
              "apellidos" => "Moraes"
            ]
            5 => array:2 [
              "nombre" => "Robson dos Santos Souza"
              "apellidos" => "Marinho"
            ]
            6 => array:2 [
              "nombre" => "Maria Clara Rodrigues"
              "apellidos" => "Vieira"
            ]
            7 => array:2 [
              "nombre" => "Ana Maria Viana"
              "apellidos" => "Pinto"
            ]
            8 => array:2 [
              "nombre" => "Tatiana Xavier"
              "apellidos" => "de Castro"
            ]
          ]
        ]
      ]
    ]
    "idiomaDefecto" => "en"
    "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S151783821730802X?idApp=UINPBA00004N"
    "url" => "/15178382/0000004900000004/v1_201810050636/S151783821730802X/v1_201810050636/en/main.assets"
  ]
  "itemAnterior" => array:19 [
    "pii" => "S1517838217304616"
    "issn" => "15178382"
    "doi" => "10.1016/j.bjm.2018.02.012"
    "estado" => "S300"
    "fechaPublicacion" => "2018-10-01"
    "aid" => "404"
    "copyright" => "Sociedade Brasileira de Microbiologia"
    "documento" => "article"
    "crossmark" => 1
    "licencia" => "http://creativecommons.org/licenses/by-nc-nd/4.0/"
    "subdocumento" => "fla"
    "cita" => "Braz J Microbiol. 2018;49:757-69"
    "abierto" => array:3 [
      "ES" => true
      "ES2" => true
      "LATM" => true
    ]
    "gratuito" => true
    "lecturas" => array:2 [
      "total" => 748
      "formatos" => array:3 [
        "EPUB" => 58
        "HTML" => 470
        "PDF" => 220
      ]
    ]
    "en" => array:12 [
      "idiomaDefecto" => true
      "cabecera" => "<span class="elsevierStyleTextfn">Environmental Microbiology</span>"
      "titulo" => "Petroleum contamination and bioaugmentation in bacterial rhizosphere communities from <span class="elsevierStyleItalic">Avicennia schaueriana</span>"
      "tienePdf" => "en"
      "tieneTextoCompleto" => "en"
      "tieneResumen" => "en"
      "paginas" => array:1 [
        0 => array:2 [
          "paginaInicial" => "757"
          "paginaFinal" => "769"
        ]
      ]
      "contieneResumen" => array:1 [
        "en" => true
      ]
      "contieneTextoCompleto" => array:1 [
        "en" => true
      ]
      "contienePdf" => array:1 [
        "en" => true
      ]
      "resumenGrafico" => array:2 [
        "original" => 0
        "multimedia" => array:7 [
          "identificador" => "fig0010"
          "etiqueta" => "Fig&#46; 2"
          "tipo" => "MULTIMEDIAFIGURA"
          "mostrarFloat" => true
          "mostrarDisplay" => false
          "figura" => array:1 [
            0 => array:4 [
              "imagen" => "gr2.jpeg"
              "Alto" => 2798
              "Ancho" => 2492
              "Tamanyo" => 394644
            ]
          ]
          "descripcion" => array:1 [
            "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Comparison of the bacterial community structures by DGGE based on bacterial 16S rRNA&#46; S&#58; &#40;S&#41; Standard bacterial 16S rRNA&#59; &#40;1&#41; controls&#44; plants without inoculum and oil&#59; &#40;2&#41; inoculated plants&#59; &#40;3&#41; inoculated plants artificially contaminated with 1<span class="elsevierStyleHsp" style=""></span>mL of emulsified crude oil in 10<span class="elsevierStyleHsp" style=""></span>mL of sea water&#59; &#40;4&#41; plant artificially contaminated with 1<span class="elsevierStyleHsp" style=""></span>mL of emulsified crude oil in 10<span class="elsevierStyleHsp" style=""></span>mL of sea water&#46;</p>"
          ]
        ]
      ]
      "autores" => array:1 [
        0 => array:2 [
          "autoresLista" => "Simone Dealtry, Angela Michelato Ghizelini, Leda C&#46;S&#46; Mendon&#231;a-Hagler, Ricardo Moreira Chaloub, Fernanda Reinert, T&#225;cio M&#46;P&#46; de Campos, Newton C&#46;M&#46; Gomes, Kornelia Smalla"
          "autores" => array:8 [
            0 => array:2 [
              "nombre" => "Simone"
              "apellidos" => "Dealtry"
            ]
            1 => array:2 [
              "nombre" => "Angela Michelato"
              "apellidos" => "Ghizelini"
            ]
            2 => array:2 [
              "nombre" => "Leda C&#46;S&#46;"
              "apellidos" => "Mendon&#231;a-Hagler"
            ]
            3 => array:2 [
              "nombre" => "Ricardo Moreira"
              "apellidos" => "Chaloub"
            ]
            4 => array:2 [
              "nombre" => "Fernanda"
              "apellidos" => "Reinert"
            ]
            5 => array:2 [
              "nombre" => "T&#225;cio M&#46;P&#46; de"
              "apellidos" => "Campos"
            ]
            6 => array:2 [
              "nombre" => "Newton C&#46;M&#46;"
              "apellidos" => "Gomes"
            ]
            7 => array:2 [
              "nombre" => "Kornelia"
              "apellidos" => "Smalla"
            ]
          ]
        ]
      ]
    ]
    "idiomaDefecto" => "en"
    "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1517838217304616?idApp=UINPBA00004N"
    "url" => "/15178382/0000004900000004/v1_201810050636/S1517838217304616/v1_201810050636/en/main.assets"
  ]
  "en" => array:20 [
    "idiomaDefecto" => true
    "cabecera" => "<span class="elsevierStyleTextfn">Environmental Microbiology</span>"
    "titulo" => "Ammonia determines transcriptional profile of microorganisms in anaerobic digestion"
    "tieneTextoCompleto" => true
    "paginas" => array:1 [
      0 => array:2 [
        "paginaInicial" => "770"
        "paginaFinal" => "776"
      ]
    ]
    "autores" => array:1 [
      0 => array:4 [
        "autoresLista" => "Nan Zhang, Huijuan Peng, Yong Li, Wenxiu Yang, Yuneng Zou, Huiguo Duan"
        "autores" => array:6 [
          0 => array:3 [
            "nombre" => "Nan"
            "apellidos" => "Zhang"
            "referencia" => array:2 [
              0 => array:2 [
                "etiqueta" => "<span class="elsevierStyleSup">a</span>"
                "identificador" => "aff0005"
              ]
              1 => array:2 [
                "etiqueta" => "<span class="elsevierStyleSup">b</span>"
                "identificador" => "aff0010"
              ]
            ]
          ]
          1 => array:3 [
            "nombre" => "Huijuan"
            "apellidos" => "Peng"
            "referencia" => array:2 [
              0 => array:2 [
                "etiqueta" => "<span class="elsevierStyleSup">a</span>"
                "identificador" => "aff0005"
              ]
              1 => array:2 [
                "etiqueta" => "<span class="elsevierStyleSup">b</span>"
                "identificador" => "aff0010"
              ]
            ]
          ]
          2 => array:3 [
            "nombre" => "Yong"
            "apellidos" => "Li"
            "referencia" => array:2 [
              0 => array:2 [
                "etiqueta" => "<span class="elsevierStyleSup">a</span>"
                "identificador" => "aff0005"
              ]
              1 => array:2 [
                "etiqueta" => "<span class="elsevierStyleSup">b</span>"
                "identificador" => "aff0010"
              ]
            ]
          ]
          3 => array:3 [
            "nombre" => "Wenxiu"
            "apellidos" => "Yang"
            "referencia" => array:1 [
              0 => array:2 [
                "etiqueta" => "<span class="elsevierStyleSup">a</span>"
                "identificador" => "aff0005"
              ]
            ]
          ]
          4 => array:3 [
            "nombre" => "Yuneng"
            "apellidos" => "Zou"
            "referencia" => array:1 [
              0 => array:2 [
                "etiqueta" => "<span class="elsevierStyleSup">a</span>"
                "identificador" => "aff0005"
              ]
            ]
          ]
          5 => array:4 [
            "nombre" => "Huiguo"
            "apellidos" => "Duan"
            "email" => array:1 [
              0 => "duanhuiguo6&#64;163&#46;com"
            ]
            "referencia" => array:2 [
              0 => array:2 [
                "etiqueta" => "<span class="elsevierStyleSup">a</span>"
                "identificador" => "aff0005"
              ]
              1 => array:2 [
                "etiqueta" => "<span class="elsevierStyleSup">&#42;</span>"
                "identificador" => "cor0005"
              ]
            ]
          ]
        ]
        "afiliaciones" => array:2 [
          0 => array:3 [
            "entidad" => "Neijiang Normal University&#44; College of Life Sciences&#44; Neijiang&#44; China"
            "etiqueta" => "a"
            "identificador" => "aff0005"
          ]
          1 => array:3 [
            "entidad" => "Department of Education&#44; Key Laboratory of Regional Characteristic Agricultural Resources&#44; Neijiang&#44; China"
            "etiqueta" => "b"
            "identificador" => "aff0010"
          ]
        ]
        "correspondencia" => array:1 [
          0 => array:3 [
            "identificador" => "cor0005"
            "etiqueta" => "&#8270;"
            "correspondencia" => "<span class="elsevierStyleItalic">Corresponding author at</span>&#58; No&#46; 705&#44; Dongtong Road&#44; Dongxing District&#44; Neijiang 641100&#44; China&#46;"
          ]
        ]
      ]
    ]
    "resumenGrafico" => array:2 [
      "original" => 0
      "multimedia" => array:7 [
        "identificador" => "fig0005"
        "etiqueta" => "Fig&#46; 1"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr1.jpeg"
            "Alto" => 1085
            "Ancho" => 1605
            "Tamanyo" => 120837
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Fermentation performance under high &#40;HN&#41; and low &#40;LN&#41; NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> concentrations&#46; All the data are presented as means<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>standard deviations &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>3&#41;&#46;</p>"
        ]
      ]
    ]
    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Anaerobic digestion &#40;AD&#41; is a promising technology in the field of waste treatment and renewable energy production&#46; Livestock manure has been processed increasingly by AD to reduce pathogens and to generate bioenergy such as methane&#46;<a class="elsevierStyleCrossRefs" href="#bib0150"><span class="elsevierStyleSup">1&#44;2</span></a> Thus&#44; the improvement of stability and efficiency of AD is crucial for the comprehensive application of this technology&#46; Ammonia concentration is one of crucial factors regulating AD stability&#46;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">3</span></a> Optimal ammonia concentrations provide sufficient buffer capacity and nutrient for microbial growth&#44; which improves the AD stability and efficiency&#46; However&#44; low or excessive ammonia concentrations usually result in the failure of AD&#46; It is reported that low ammonia concentration &#40;&#60;500<span class="elsevierStyleHsp" style=""></span>mg<span class="elsevierStyleHsp" style=""></span>L<span class="elsevierStyleSup">&#8722;1</span>&#41; decreases methane production&#44; biomass and the aceticlastic methanogenic activity&#46;<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">4</span></a> The high ammonia &#40;&#62;4000<span class="elsevierStyleHsp" style=""></span>mg<span class="elsevierStyleHsp" style=""></span>L<span class="elsevierStyleSup">&#8722;1</span>&#41; results in the inhibition of microbial activity and accumulation of volatile fatty acids&#44; which finally causes decreased stability and even failure of AD&#46;<a class="elsevierStyleCrossRefs" href="#bib0160"><span class="elsevierStyleSup">3&#8211;6</span></a> Due to high protein content in manure&#44; there are usually high ammonia concentrations in the AD of manure&#46;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">3</span></a> Thus&#44; AD of livestock manure has to confront the inhibition from high ammonia&#46; It is necessary to reveal the mechanisms underlying ammonia inhibition on the AD process&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">Temperature is considered as a prominent factor regulating ammonia toxicity on AD process&#46;<a class="elsevierStyleCrossRefs" href="#bib0160"><span class="elsevierStyleSup">3&#44;7&#44;8</span></a> The thermophilic temperatures compared to mesophilic temperatures usually cause higher ammonia toxicity&#46;<a class="elsevierStyleCrossRefs" href="#bib0180"><span class="elsevierStyleSup">7&#44;8</span></a> The thermophilic temperatures enhance metabolic activities of microorganisms&#44; which strengthens hydrolysis of substrates including proteins&#46; This process increases ammonia concentration in the slurry&#44; so that ammonia toxicity is undoubtedly strengthened&#46; Thus&#44; under mesophilic temperatures&#44; the ammonia toxicity more depended on the initial ammonia concentration&#44; which facilitates the understanding of the relationship between ammonia concentration and ammonia toxicity&#46; Different methanogens are distinguishably sensitive to ammonia concentrations&#44; which partly determines ammonia toxicity on AD process&#46; Due to spherical <span class="elsevierStyleItalic">Methanosarcina</span> with higher ratio of volume&#47;surface than that of rod-shaped <span class="elsevierStyleItalic">Methanosaeta</span>&#44; the diffusion of ammonia is less into the <span class="elsevierStyleItalic">Methanosarcina</span> than <span class="elsevierStyleItalic">Methanosaeta</span>&#44;<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">9</span></a> which results in their different sensitivities to ammonia concentrations&#46; Thus&#44; high ammonia more probably causes failure of AD where <span class="elsevierStyleItalic">Methanosaeta</span> are dominated in the methanogens than that where <span class="elsevierStyleItalic">Methanosarcina</span> are dominated&#46; The recovery of AD from failure depends on a reconstruction of methanogenic species&#44;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">10</span></a> so that <span class="elsevierStyleItalic">Methanosarcina</span> as dominated methanogens replace <span class="elsevierStyleItalic">Methanosaeta</span>&#46; This process probably causes the decrease of acetoclastic methanogenesis&#46;<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">11</span></a> These studies of ammonia toxicity on AD process mainly focus on methanogens and methanogenic process&#46;<a class="elsevierStyleCrossRefs" href="#bib0160"><span class="elsevierStyleSup">3&#44;5&#44;6&#44;12&#44;13</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">Although the ammonia toxicity on AD process has been comprehensively revealed mainly based on methanogenic microflora&#44;<a class="elsevierStyleCrossRefs" href="#bib0160"><span class="elsevierStyleSup">3&#44;5&#44;12&#8211;14</span></a> the transcriptional profiles of specific pathways and genes in response to ammonia have rarely been discussed&#46; The AD process consists of AD food web &#40;hydrolysis&#44; acidogenesis&#44; acetogenesis and methanogenesis&#41;&#44; so besides methanogenesis&#44; the other three steps of the food web also play important roles in final methane production&#46; Thus&#44; the transcriptional profiles of methanogenesis-related processes are necessary to be revealed based on metatranscriptomic analysis&#44; which can provide a new sight underlying ammonia toxicity on AD process&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">In this study&#44; based on metatranscriptomic analysis&#44; the transcriptional profiles of microbial community in response to low and high NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> concentrations&#44; respectively&#44; were revealed in AD&#46; Specifically&#44; we focused on the expressions of pathways and genes responsible for methane production under different NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> concentrations to further reveal the mechanism underlying ammonia toxicity on AD process&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Materials and methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Setup of AD system</span><p id="par0025" class="elsevierStylePara elsevierViewall">The AD experiment of swine manure was conducted with working volume of 2&#46;5<span class="elsevierStyleHsp" style=""></span>L digestion sludge containing 0&#46;75<span class="elsevierStyleHsp" style=""></span>L initial inoculum&#44; and the total solid content was 7&#37; &#40;Supplement Table S1&#41;&#46; The high ammonia treatment with NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> &#40;5000<span class="elsevierStyleHsp" style=""></span>mg<span class="elsevierStyleHsp" style=""></span>L<span class="elsevierStyleSup">&#8722;1</span>&#41; &#40;HN&#41; and low ammonia treatment with NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> &#40;1500<span class="elsevierStyleHsp" style=""></span>mg<span class="elsevierStyleHsp" style=""></span>L<span class="elsevierStyleSup">&#8722;1</span>&#41; &#40;LN&#41; were determined by adding NH<span class="elsevierStyleInf">4</span>Cl at the beginning of AD&#44; which was mainly based on previous report<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">6</span></a> and pre-experiments&#46; All the treatments were conducted in triplicate at 37<span class="elsevierStyleHsp" style=""></span>&#176;C&#46; Seed slurry was prepared by anaerobic digestion of swine manure &#40;obtained from a pig farm in Neijiang&#44; Sichuan Province&#44; China&#41; at 37<span class="elsevierStyleHsp" style=""></span>&#176;C&#44; for one hydraulic retention time &#40;HRT&#41;&#46; After methane production reached the first peak &#40;6th day&#41; in the reactor&#44; we performed a semi-continuous feeding mode that 500<span class="elsevierStyleHsp" style=""></span>mL of digestate was exchanged every three days with HRT of 15 days and organic loading rate of 4&#46;5<span class="elsevierStyleHsp" style=""></span>g VS &#40;volatile solid&#41; L<span class="elsevierStyleSup">&#8722;1</span><span class="elsevierStyleHsp" style=""></span>day<span class="elsevierStyleSup">&#8722;1</span>&#46; The anaerobic digestion was performed for two HRT&#46; The feeding slurry was adjusted to the corresponding NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> concentration using NH<span class="elsevierStyleInf">4</span>Cl&#46; Details about parameters at the start of fermentation were shown in Supplement Table S1&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Sampling and analysis</span><p id="par0030" class="elsevierStylePara elsevierViewall">At each feeding&#44; methane content in biogas&#44; volatile fatty acids &#40;VFA&#41;&#44; NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> and pH were measured to monitor AD dynamic&#46; The methane content in biogas was measured using an Agilent 6890 gas chromatography system &#40;Agilent Technologies&#44; USA&#41;&#44; equipped with a thermal conductivity detector and carrier gas of argon&#46; The injection port&#44; column oven&#44; and detector were operated at 100&#44; 70&#44; and 150<span class="elsevierStyleHsp" style=""></span>&#176;C&#44; respectively&#46; The daily volume of biogas was detected by water replacement method&#46; The VFA in the slurry was detected using Agilent 1260 Infinity liquid chromatography &#40;Agilent Technologies&#44; USA&#41;&#44; equipped with a differential refraction detector &#40;RID&#41; and mobile phase of H<span class="elsevierStyleInf">2</span>SO<span class="elsevierStyleInf">4</span> &#40;0&#46;005<span class="elsevierStyleHsp" style=""></span>M&#41;&#46; Total solid and volatile solid were measured based on previous report&#46;<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">15</span></a> NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> concentration was quantified with Nessler&#39;s reagent colorimetric method&#46;<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">16</span></a> At the end of the second HRT&#44; the digestate were sampled in triplicate for total RNA extraction with the RNeasy PowerMicrobiome Kit &#40;Cat&#46; No&#46; 26000-50&#59; MO BIO&#44; USA&#41;&#46; The quality of RNA was checked with a NanoDrop 2000 spectrophotometer &#40;Thermo&#44; USA&#41;&#46; Ribosomal RNA was removed from the total RNA with the RiboMinusTM kit &#40;Lot&#46; No&#46; 1539791&#59; Invitrogen&#44; USA&#41;&#46; The metatranscriptomic &#40;mRNA&#41; sequencing was performed using an Illumina Hiseq 2000 &#40;Illumina Inc&#46;&#44; USA&#41;&#46; The sequencing raw data from total 6 samples were uploaded to MG-RAST with assigned MG-RAST ID &#40;mgs589946&#44; mgs589949&#44; mgs589952&#44; mgs589955&#44; mgs589958 and mgs589961&#41; for further analysis&#46;<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">17</span></a> Prior to the analysis&#44; the quality control pipeline in MG-RAST<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">17</span></a> was performed to remove poor quality sequences&#46; The annotation of functional profiles was based on the KEGG Orthologs database including 4 levels&#46; The functional categories was presented as level 2&#46; Level 3 reflected the KEGG pathways&#44; and level 4 &#40;gene expression level&#41; showed expressions of specific genes&#46;<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">18</span></a> During annotation analysis&#44; the pipeline parameters were kept at default settings&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Statistical analysis</span><p id="par0035" class="elsevierStylePara elsevierViewall">The ammonia effect on the general changes of gene expressions was assessed by principal coordinates analysis &#40;PCoA&#41; in R &#40;<a id="intr0005" class="elsevierStyleInterRef" href="http://www.r-project.org/">http&#58;&#47;&#47;www&#46;r-project&#46;org&#47;</a>&#41;&#44; based on the Bray&#8211;Curtis dissimilarity index&#44; using the <span class="elsevierStyleItalic">vegan</span> package&#46; The normality and homoscedasticity of the raw data&#44; and one way analysis of variance &#40;ANOVA&#41; were performed in SPSS 21 software &#40;IBM USA&#41;&#46; Spearman&#39;s correlation analysis&#44; enrichment analysis and redundancy analysis &#40;RDA&#41; were calculated in R with the <span class="elsevierStyleItalic">vegan</span> package&#46; The Spearman&#39;s <span class="elsevierStyleItalic">p</span> value was adjusted using the Benjamini and Hochberg methods&#46;<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">19</span></a> The taxa with average relative abundance &#62;0&#46;1&#37; and significantly different expression &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41; between HN and LN were selected for network analysis to reveal co-response to ammonia&#46; If the correlation <span class="elsevierStyleItalic">p</span> value was &#60;0&#46;05&#44; the correlation between two taxa was considered statistically robust and shown in the network&#46; The network was visualized in Cytoscape software&#46;<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">20</span></a></p></span></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Results</span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Anaerobic digestion and global expressions of genes</span><p id="par0040" class="elsevierStylePara elsevierViewall">There were significant differences of AD performances between LN and HN &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a> and Supplement Table S1&#41;&#46; Methane production and content in the biogas were higher in LN than that in HN &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;01&#41;&#46; The concentrations of acetic acid and propionic acid&#44; and pH were higher in HN&#46; It showed that high NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> concentration inhibited methane production and resulted in some accumulations of VFA&#46; The global expressions of genes showed obvious differences between HN and LN &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#44; which well corresponded with the significant differences of performances of AD&#46; Compared with HN&#44; the replicates in LN clustered more closely &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#44; which implied that high NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> probably caused more randomness of gene expressions in AD&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Differentiated expressions of metabolic pathways</span><p id="par0045" class="elsevierStylePara elsevierViewall">In the comparison between HN and LN based on pathways &#40;level 2&#41;&#44; most expressions of these pathways were higher in HN&#44; but only signal transduction was significantly higher at HN &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46; Surprisingly&#44; only energy metabolism was higher in LN &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;01&#41;&#46; At level 3&#44; most expressions of pathways were not significantly distinguishable between HN and LN &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; The pathway of methane metabolism &#40;ko00680&#41; &#40;usually indicating the methanogenesis in anaerobic digestion&#41; has a higher expression in LN &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;01&#41;&#44; but the pathways of RNA polymerase &#40;ko03020&#41; and Valine&#44; leucine and isoleucine degradation &#40;ko00280&#41; had higher expressions in HN &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41; &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; The relative abundances of arginine and proline metabolism &#40;ko00330&#41; and methane metabolism showed positive correlations with daily methane production &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#44; but those of RNA polymerase and cell cycle-caulobacter &#40;ko04112&#41; showed negative correlations with methane production &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41; &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0050" class="elsevierStylePara elsevierViewall">In redundancy analysis &#40;RDA&#41; of the relationship between the expressions of pathways &#40;level 3&#41; and the environmental variables &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>a&#41;&#44; the expressions of the pathways including methane metabolism&#44; arginine and proline metabolism&#44; pentose phosphate pathway &#40;ko00030&#41;&#44; histidine metabolism &#40;ko00340&#41;&#44; oxidative phosphorylation &#40;ko00190&#41; and pyruvate metabolism &#40;ko00620&#41; positively correlated with methane production&#46; The expressions of RNA degradation &#40;ko030180&#41;&#44; pentose and glucuronate interconversions &#40;ko00040&#41; and Citrate cycle &#40;ko00020&#41; positively correlated with acetic acid and pH&#46; The expressions of DNA replication &#40;ko03030&#41; and peroxisome &#40;ko04146&#41; potentially contributed to propionic acid accumulation&#46;</p><elsevierMultimedia ident="fig0020"></elsevierMultimedia></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Gene differentiated expressions</span><p id="par0055" class="elsevierStylePara elsevierViewall">Besides the overall difference of gene expressions &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#44; the enrichment analysis was applied to further uncover differentiated expressions of individual genes between HN and LN&#46; Probably attributed to significant difference of the expression of methane metabolism &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#44; most of these genes with significant differentiated expressions &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41; were involved in methane metabolism &#40;Supplementary Table S2&#41;&#46; These methanogenic genes mainly encode acetyl-CoA decarbonylase and methyl-coenzyme M reductase&#46; Additionally&#44; most of methanogenic genes showed significant positive correlations with methane production &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41; &#40;Supplementary Table S2&#41;&#46; Besides methanogenic genes&#44; two genes involved in the pathway of pyruvate metabolism showed higher expressions in LN&#44; but three and two genes involved in aminoacyl-tRNA biosynthesis &#40;ko00970&#41; and ribosome &#40;ko03010&#41;&#44; respectively&#44; showed higher expressions in HN &#40;Supplementary Table S2&#41;&#46; In the RDA of the relationship between gene expressions and environmental variables &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>b&#41;&#44; it indicated that besides the methanogenic genes&#44; the genes which encode glycerol kinase&#44; phosphate acetyltransferase&#44; transporting ATPase and pyruvate&#95;orthophosphate dikinase positively contributed to methane production&#46; The genes which encode ribosomal subunits&#44; tRNA&#95;synthetase and phosphoribosylamine&#95;glycine ligase positively contributed to pH and acetic acid&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">Although there were 19 genes &#40;each taxon with average relative abundance<span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>0&#46;1&#37;&#41; significantly distinguishingly expressed between LN and HN &#40;Supplementary Table S2&#41;&#44; the co-expressions of these genes should be further verified&#46; Based on Spearman&#8217; correlations&#44; the co-expressions of these genes to different NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> concentrations were further revealed &#40;<a class="elsevierStyleCrossRef" href="#fig0025">Fig&#46; 5</a> and Supplementary Table S3&#41;&#46; The expressions of the genes involved in methane metabolism&#44; glycerolipid metabolism&#44; pyruvate metabolism and oxidative phosphorylation showed a co-inhibition under the high ammonia condition&#46; The expressions of methanogenic genes especially the genes which encode acetyl-CoA decarbonylase were comprehensively co-inhibited by high ammonia&#46; However&#44; the expressions of the genes involved in ribosome&#44; aminoacyl-tRNA biosynthesis&#44; purine metabolism&#44; cell cycle-caulobacter and RNA degradation showed co-enhancement under the high ammonia condition&#46; The expressions of more genes were co-inhibited under the high ammonia condition&#44; which supported ammonia toxicity on AD process&#46;</p><elsevierMultimedia ident="fig0025"></elsevierMultimedia></span></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Discussion</span><p id="par0065" class="elsevierStylePara elsevierViewall">Although the hydrolysis of substrates would cause variations of ammonia concentrations during AD&#44; in this study the operations of ammonia addition in HN and LN created distinct ammonia pressures to differentiate AD performances and microbial gene expression &#40;<a class="elsevierStyleCrossRefs" href="#fig0005">Figs&#46; 1 and 2</a>&#41;&#46; High ammonia significantly inhibited AD process by decreasing methane production and content in the biogas&#44; and the accumulations of VFA&#46; The decreased methane content in biogas not only resulted in a low methane production but also indicated a mass of byproducts&#46; The accumulations of VFA&#44; especially acetic acid&#44; implied a potential inhibition of acetoclastic methanogenesis&#44; which agreed well with previous reports&#46;<a class="elsevierStyleCrossRefs" href="#bib0160"><span class="elsevierStyleSup">3&#44;5</span></a> Although the accumulations of VFA were observed in HN&#44; such accumulations unlikely caused excessive acidification in AD&#44; which was further supported by the pH value &#40;7&#46;8<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;5&#41;&#46; Additionally&#44; the ammonia inhibition more probably occurred under thermophilic temperatures than mesophilic condition &#40;37<span class="elsevierStyleHsp" style=""></span>&#176;C&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">3</span></a> Thus&#44; in this study&#44; the inhibition of AD process was supposed to be directly attributed to ammonia toxicity on microbial activities&#44; rather than other environmental factors regulated by ammonia&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">The microbial activities were obviously regulated by ammonia&#44; which was supported by the PCoA result &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; In level 2 pathways&#44; the expressions of energy metabolism and signal transduction were significantly influenced &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46; The AD actually is an energy metabolism process during which energy is transferred and transformed through various metabolic pathways especially the methanogenic pathways&#46; The energy metabolism mainly including methane metabolism usually couples to actual methane production&#44;<a class="elsevierStyleCrossRefs" href="#bib0150"><span class="elsevierStyleSup">1&#44;21</span></a> so the inhibited expression of energy metabolism mainly resulted in the low methane production in HN&#46; Signal transduction is usually involved in modulating cell behaviors in response to environmental pressures such as pH and ammonia&#46;<a class="elsevierStyleCrossRefs" href="#bib0255"><span class="elsevierStyleSup">22&#44;23</span></a> Thus&#44; a higher expression of this pathway in HN could be explained&#46; The obviously higher expression of cell motility in HN coupled to that of signal transduction&#44; which agreed with previous report&#46;<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">24</span></a> This further supported microbial response to ammonia by behaviors or movements&#46; Unexpectedly&#44; in HN only the expression of energy metabolism was depressed&#44; but other pathways had higher expressions compared to that in LN &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46; In consideration of that methanogens are not dominant microorganisms compared to bacteria such as Firmicutes&#44; Bacteroidetes and Proteobacteria in AD&#44;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">25</span></a> it is reasonable to deduce that these pathways except energy metabolism were mainly conducted by bacteria&#46; Thus&#44; the higher expressions of these pathways in HN probably indicated high activities of bacteria under high ammonia condition&#46; This was likely because ammonia could improve nutrient of nitrogen for bacterial growth&#46;<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">4</span></a> In level 3&#44; the most significantly differentiated expressions between HN and LN was methane metabolism &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;003&#41; which positively correlated with methane production &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; Most of the other pathways had no significant expression differences&#46; Interestingly&#44; only the expressions of methane metabolism&#44; oxidative phosphorylation and pyruvate metabolism were higher in LN and positively contributed to methane production &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a> and <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#44; but the other pathways had higher expressions in HN&#46; This situation was similar with that of level 2&#46; This further confirmed that high ammonia provided some improvements to substrate metabolisms mainly conducted by bacteria&#44; but inhibited methanogenic activity&#46; Consequently&#44; although each step of AD food web played crucial roles in actual methane production&#44; the ammonia toxicity on AD process mainly targeted methanogenic process to inhibit methane production&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">Ammonia inhibition on methanogenic process would result in a shift in methanogenic acetate utilization from direct acetate cleavage toward syntrophic acetate oxidation&#46;<a class="elsevierStyleCrossRefs" href="#bib0200"><span class="elsevierStyleSup">11&#44;26</span></a> This was mainly attributed to the greatly decreased abundance of acetoclastic <span class="elsevierStyleItalic">Methanosaeta</span> under high ammonia condition&#46;<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">11</span></a> However&#44; whether the expressions of genes involved in acetoclastic methanogenesis were reduced should be revealed&#46; In methanogenic pathway&#44; only the expressions of the genes which encode acetyl-CoA decarbonylase and methyl-coenzyme M reductase were significantly higher in LN &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#44; and showed positive correlations with methane production &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#46; Acetyl-CoA decarbonylase plays an important role in acetoclastic pathway<a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">27</span></a> and methyl-coenzyme M reductase is the key enzyme in methanogenesis&#46;<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">28</span></a> Thus&#44; the higher expressions of these genes encoding the two enzymes undoubtedly improved methane production&#46; The expressions of genes which encode acetyl-CoA decarbonylase were significantly depressed in HN&#44; indicating that the acetoclastic methanogenesis was inhibited&#46; Based on transcriptional profile&#44; the ammonia toxicity on acetoclastic methanogenesis was further revealed&#46; Additionally&#44; ammonia inhibited methanogens&#8217; activities also probably by depressing the expressions of genes which encode methyl-coenzyme M reductase&#46; Besides methanogenic genes&#44; the genes involved in pyruvate metabolism had significantly higher expressions in HN&#44; which probably improved the production of acetyl-CoA&#46;<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">29</span></a> The genes involved in aminoacyl-tRNA biosynthesis and ribosome were significantly higher expressed in HN&#44; indicating that ammonia potentially facilitated translation process&#46;<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">13</span></a></p><p id="par0080" class="elsevierStylePara elsevierViewall">Although the expressions of individual key genes could generally explain the ammonia toxicity on AD process&#44; gene co-expressions in response to ammonia probably provided a systemic sight&#46; The inhibition of the co-expressions of the genes involved in methane metabolism&#44; glycerolipid metabolism&#44; pyruvate metabolism and oxidative phosphorylation indicated that these pathways probably performed a cooperation to regulate AD efficiency that was mainly represented by methane production&#46; The coupling relationship between methane metabolism and oxidative phosphorylation has been revealed before&#46;<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">1</span></a> The glycerolipid metabolism and pyruvate metabolism probably provided potential substrates<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">29</span></a> for methanogenesis&#46; Interestingly&#44; nearly all the genes which encode acetyl-CoA decarbonylase showed inhibition of co-expressions under the high ammonia condition&#44; which further demonstrated that acetoclastic methanogenesis were inhibited by high ammonia&#46; This also showed that these genes compared to other methanogenic genes were unitedly and highly sensitive to NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> concentration&#46; These genes could be used as potential indicators for ammonia toxicity on AD process&#46; Additionally&#44; the in inhibition of co-expression of the genes which encode acetyl-CoA decarbonylase and methyl-coenzyme M reductase&#44; indicating the cooperation of the two enzymes in methanogenesis&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">Consequently&#44; except methanogenesis&#44; most of pathways were not significantly influenced by high ammonia concentration&#44; so that they were probably not the key factors contributing to decreased methane production&#46; Thus&#44; ammonia toxicity on AD process mainly targeted methanogenic process by inhibiting the expressions of genes which encode acetyl-CoA decarbonylase and methyl-coenzyme M reductase to finally decrease methane production&#46; This study revealed mechanisms underlying microbial response to ammonia pressure based on gene expressions&#44; and further discovered ammonia inhibition only targeting on the genes encoding the above two enzymes&#46; However&#44; the adaptions of microbial gene expressions to ammonia pressure during longtime AD also should be considered in the future work&#46;</p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Conflicts of interest</span><p id="par0090" class="elsevierStylePara elsevierViewall">Authors declare that they have no competing interests&#46;</p></span></span>"
    "textoCompletoSecciones" => array:1 [
      "secciones" => array:9 [
        0 => array:3 [
          "identificador" => "xres1091242"
          "titulo" => "Abstract"
          "secciones" => array:1 [
            0 => array:1 [
              "identificador" => "abst0005"
            ]
          ]
        ]
        1 => array:2 [
          "identificador" => "xpalclavsec1034364"
          "titulo" => "Keywords"
        ]
        2 => array:2 [
          "identificador" => "sec0005"
          "titulo" => "Introduction"
        ]
        3 => array:3 [
          "identificador" => "sec0010"
          "titulo" => "Materials and methods"
          "secciones" => array:3 [
            0 => array:2 [
              "identificador" => "sec0015"
              "titulo" => "Setup of AD system"
            ]
            1 => array:2 [
              "identificador" => "sec0020"
              "titulo" => "Sampling and analysis"
            ]
            2 => array:2 [
              "identificador" => "sec0025"
              "titulo" => "Statistical analysis"
            ]
          ]
        ]
        4 => array:3 [
          "identificador" => "sec0030"
          "titulo" => "Results"
          "secciones" => array:3 [
            0 => array:2 [
              "identificador" => "sec0035"
              "titulo" => "Anaerobic digestion and global expressions of genes"
            ]
            1 => array:2 [
              "identificador" => "sec0040"
              "titulo" => "Differentiated expressions of metabolic pathways"
            ]
            2 => array:2 [
              "identificador" => "sec0045"
              "titulo" => "Gene differentiated expressions"
            ]
          ]
        ]
        5 => array:2 [
          "identificador" => "sec0050"
          "titulo" => "Discussion"
        ]
        6 => array:2 [
          "identificador" => "sec0055"
          "titulo" => "Conflicts of interest"
        ]
        7 => array:2 [
          "identificador" => "xack370732"
          "titulo" => "Acknowledgements"
        ]
        8 => array:1 [
          "titulo" => "References"
        ]
      ]
    ]
    "pdfFichero" => "main.pdf"
    "tienePdf" => true
    "fechaRecibido" => "2017-09-25"
    "fechaAceptado" => "2018-04-13"
    "PalabrasClave" => array:1 [
      "en" => array:1 [
        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Keywords"
          "identificador" => "xpalclavsec1034364"
          "palabras" => array:5 [
            0 => "Anaerobic digestion"
            1 => "Ammonia"
            2 => "Pathway"
            3 => "Gene expression"
            4 => "Methanogenesis"
          ]
        ]
      ]
    ]
    "tieneResumen" => true
    "resumen" => array:1 [
      "en" => array:2 [
        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Anaerobic digestion is important for the management of livestock manure with high ammonia level&#46; Although ammonia effects on anaerobic digestion have been comprehensively studied&#44; the molecular mechanism underlying ammonia inhibition still remains elusive&#46; In this study&#44; based on metatranscriptomic analysis&#44; the transcriptional profile of microbial community in anaerobic digestion under low &#40;1500<span class="elsevierStyleHsp" style=""></span>mg<span class="elsevierStyleHsp" style=""></span>L<span class="elsevierStyleSup">&#8722;1</span>&#41; and high NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> &#40;5000<span class="elsevierStyleHsp" style=""></span>mg<span class="elsevierStyleHsp" style=""></span>L<span class="elsevierStyleSup">&#8722;1</span>&#41; concentrations&#44; respectively&#44; were revealed&#46; The results showed that high NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> concentrations significantly inhibited methane production but facilitated the accumulations of volatile fatty acids&#46; The expression of methanogenic pathway was significantly inhibited by high NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> concentration but most of the other pathways were not significantly affected&#46; Furthermore&#44; the expressions of methanogenic genes which encode acetyl-CoA decarbonylase and methyl-coenzyme M reductase were significantly inhibited by high NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> concentration&#46; The inhibition of the co-expressions of the genes which encode acetyl-CoA decarbonylase was observed&#46; Some genes involved in the pathways of aminoacyl-tRNA biosynthesis and ribosome were highly expressed under high NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> concentration&#46; Consequently&#44; the ammonia inhibition on anaerobic digestion mainly focused on methanogenic process by suppressing the expressions of genes which encode acetyl-CoA decarbonylase and methyl-coenzyme M reductase&#46; This study improved the accuracy and depth of understanding ammonia inhibition on anaerobic digestion&#46;</p></span>"
      ]
    ]
    "apendice" => array:1 [
      0 => array:1 [
        "seccion" => array:1 [
          0 => array:4 [
            "apendice" => "<p id="par0105" class="elsevierStylePara elsevierViewall">The following are the supplementary data to this article&#58;<elsevierMultimedia ident="upi0005"></elsevierMultimedia></p>"
            "etiqueta" => "Appendix A"
            "titulo" => "Supplementary data"
            "identificador" => "sec0065"
          ]
        ]
      ]
    ]
    "multimedia" => array:7 [
      0 => array:7 [
        "identificador" => "fig0005"
        "etiqueta" => "Fig&#46; 1"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr1.jpeg"
            "Alto" => 1085
            "Ancho" => 1605
            "Tamanyo" => 120837
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Fermentation performance under high &#40;HN&#41; and low &#40;LN&#41; NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> concentrations&#46; All the data are presented as means<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>standard deviations &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>3&#41;&#46;</p>"
        ]
      ]
      1 => array:7 [
        "identificador" => "fig0010"
        "etiqueta" => "Fig&#46; 2"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr2.jpeg"
            "Alto" => 521
            "Ancho" => 1578
            "Tamanyo" => 41863
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">The principal coordinates analysis &#40;PCoA&#41; of global expressions of genes in anaerobic digestions with high NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> &#40;HN&#41; and low NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> &#40;LN&#41;&#46;</p>"
        ]
      ]
      2 => array:7 [
        "identificador" => "fig0015"
        "etiqueta" => "Fig&#46; 3"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr3.jpeg"
            "Alto" => 2287
            "Ancho" => 1584
            "Tamanyo" => 216382
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Expression profiles of level 2 at high NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> &#40;HN&#41; and low NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> &#40;LN&#41;&#46; &#42;&#42; significant at <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;01&#59; &#42; Significant at <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#46;</p>"
        ]
      ]
      3 => array:7 [
        "identificador" => "fig0020"
        "etiqueta" => "Fig&#46; 4"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr4.jpeg"
            "Alto" => 993
            "Ancho" => 3046
            "Tamanyo" => 233538
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Redundancy analysis &#40;RDA&#41; of key pathway &#40;a&#41; and gene &#40;b&#41; expressions where the methanogenic genes mainly encoding acetyl-CoA decarbonylase and methyl-coenzyme M reductase positively contribute to methane production but are omitted to simplify the figure to be clearer&#46;</p>"
        ]
      ]
      4 => array:7 [
        "identificador" => "fig0025"
        "etiqueta" => "Fig&#46; 5"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr5.jpeg"
            "Alto" => 1818
            "Ancho" => 1646
            "Tamanyo" => 202808
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Networks of gene expressions negatively &#40;a&#41; and positively &#40;b&#41; responding to ammonia&#46; The taxa with average relative abundance &#62;0&#46;1&#37; and significant differentiated expressions between LN and HN are shown&#46;</p>"
        ]
      ]
      5 => array:8 [
        "identificador" => "tbl0005"
        "etiqueta" => "Table 1"
        "tipo" => "MULTIMEDIATABLA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "detalles" => array:1 [
          0 => array:3 [
            "identificador" => "at1"
            "detalle" => "Table "
            "rol" => "short"
          ]
        ]
        "tabla" => array:3 [
          "leyenda" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Taxa with average relative abundance &#62;1&#37; are shown&#46; The <span class="elsevierStyleItalic">p</span> values represent the significance from the comparison of the relative abundances of pathways under high and low NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> concentrations&#46;</p>"
          "tablatextoimagen" => array:1 [
            0 => array:2 [
              "tabla" => array:1 [
                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Level 3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Low NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">High NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">p</span> values&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">ABC transporters &#91;PATH&#58;ko02010&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">4&#46;66<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;21&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">4&#46;76<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;37&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;757&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Alanine&#44; aspartate and glutamate metabolism &#91;PATH&#58;ko00250&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&#46;44<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&#46;7<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;29&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;365&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Aminoacyl-tRNA biosynthesis &#91;PATH&#58;ko00970&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&#46;31<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;11&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&#46;51<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;19&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;270&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Arginine and proline metabolism &#91;PATH&#58;ko00330&#93;<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;31<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;08&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;21<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;08&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;299&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Bacterial chemotaxis &#91;PATH&#58;ko02030&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;11<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;12&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;26<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;405&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Bacterial secretion system &#91;PATH&#58;ko03070&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;37<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;4<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;13&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;813&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Cell cycle-caulobacter &#91;PATH&#58;ko04112&#93;<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;45<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;11&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;64<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;01&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;069&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Citrate cycle &#40;TCA cycle&#41; &#91;PATH&#58;ko00020&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;3<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;06&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;39<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;08&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;294&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Cysteine and methionine metabolism &#91;PATH&#58;ko00270&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;16<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;18&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;15<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;07&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;955&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">DNA replication &#91;PATH&#58;ko03030&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;05<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;13&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;21<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;18&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;366&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Flagellar assembly &#91;PATH&#58;ko02040&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">6&#46;65<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;86&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">7&#46;88<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;69&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;414&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Glycine&#44; serine and threonine metabolism &#91;PATH&#58;ko00260&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&#46;27<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;21&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&#46;36<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;26&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;716&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Glycolysis&#47;Gluconeogenesis &#91;PATH&#58;ko00010&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&#46;73<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;09&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&#46;9<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;14&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;208&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">HIF-1 signaling pathway &#91;PATH&#58;ko04066&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;67<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;07&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&#46;17<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;34&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;109&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Histidine metabolism &#91;PATH&#58;ko00340&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;07<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;09&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;95<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;07&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;200&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Methane metabolism &#91;PATH&#58;ko00680&#93;<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">10&#46;96<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;57&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">6&#46;52<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;83&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;003&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Oxidative phosphorylation &#91;PATH&#58;ko00190&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">6&#46;4<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;28&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">4&#46;22<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;67&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;100&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Pentose and glucuronate interconversions &#91;PATH&#58;ko00040&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;04<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;06&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;97<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;12&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;483&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Pentose phosphate pathway &#91;PATH&#58;ko00030&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;15<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;08&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;21<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;09&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;524&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Peroxisome &#91;PATH&#58;ko04146&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;97<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;31&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&#46;54<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;31&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;142&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Plant-pathogen interaction &#91;PATH&#58;ko04626&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;43<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;04&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;46<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;05&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;597&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Purine metabolism &#91;PATH&#58;ko00230&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&#46;42<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;19&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&#46;07<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;062&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Pyruvate metabolism &#91;PATH&#58;ko00620&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&#46;12<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;21&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;69<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;11&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;063&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ribosome &#91;PATH&#58;ko03010&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">8&#46;5<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;26&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">9&#46;6<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;74&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;117&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">RNA degradation &#91;PATH&#58;ko03018&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&#46;64<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">4&#46;11<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;18&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;063&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">RNA polymerase &#91;PATH&#58;ko03020&#93;<a class="elsevierStyleCrossRef" href="#tblfn0010"><span class="elsevierStyleSup">b</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&#46;7<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;02&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&#46;98<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;13&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;038&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Two-component system &#91;PATH&#58;ko02020&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;54<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;61<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;07&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;465&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Valine&#44; leucine and isoleucine degradation &#91;PATH&#58;ko00280&#93;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;48<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;08&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;7<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;03&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;027&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
              "imagenFichero" => array:1 [
                0 => "xTab1865899.png"
              ]
            ]
          ]
          "notaPie" => array:2 [
            0 => array:3 [
              "identificador" => "tblfn0005"
              "etiqueta" => "a"
              "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Indicates significant correlations &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41; between the relative abundances of pathways with daily methane production&#46;</p>"
            ]
            1 => array:3 [
              "identificador" => "tblfn0010"
              "etiqueta" => "b"
              "nota" => "<p class="elsevierStyleNotepara" id="npar0010"><span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;01&#46;</p>"
            ]
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Relative abundances of level 3 pathways under high and low NH<span class="elsevierStyleInf">4</span><span class="elsevierStyleSup">&#43;</span> concentrations&#46;</p>"
        ]
      ]
      6 => array:5 [
        "identificador" => "upi0005"
        "tipo" => "MULTIMEDIAECOMPONENTE"
        "mostrarFloat" => false
        "mostrarDisplay" => true
        "Ecomponente" => array:2 [
          "fichero" => "mmc1.xlsx"
          "ficheroTamanyo" => 30441
        ]
      ]
    ]
    "bibliografia" => array:2 [
      "titulo" => "References"
      "seccion" => array:1 [
        0 => array:2 [
          "identificador" => "bibs0015"
          "bibliografiaReferencia" => array:29 [
            0 => array:3 [
              "identificador" => "bib0150"
              "etiqueta" => "1"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Temperature regulates methane production through the function centralization of microbial community in anaerobic digestion"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:5 [
                            0 => "Q&#46; Lin"
                            1 => "J&#46; De Vrieze"
                            2 => "G&#46; He"
                            3 => "X&#46; Li"
                            4 => "J&#46; Li"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1016/j.biortech.2016.05.046"
                      "Revista" => array:6 [
                        "tituloSerie" => "Bioresour Technol"
                        "fecha" => "2016"
                        "volumen" => "216"
                        "paginaInicial" => "150"
                        "paginaFinal" => "158"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/27236402"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            1 => array:3 [
              "identificador" => "bib0155"
              "etiqueta" => "2"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Mechanisms and effects of arsanilic acid on antibiotic resistance genes and microbial communities during pig manure digestion"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:6 [
                            0 => "W&#46; Sun"
                            1 => "X&#46; Qian"
                            2 => "J&#46; Gu"
                            3 => "X&#46;J&#46; Wang"
                            4 => "L&#46; Zhang"
                            5 => "A&#46;Y&#46; Guo"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1016/j.biortech.2017.03.025"
                      "Revista" => array:6 [
                        "tituloSerie" => "Bioresour Technol"
                        "fecha" => "2017"
                        "volumen" => "234"
                        "paginaInicial" => "217"
                        "paginaFinal" => "223"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/28319770"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            2 => array:3 [
              "identificador" => "bib0160"
              "etiqueta" => "3"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "A critical review on inhibition of anaerobic digestion process by excess ammonia"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:3 [
                            0 => "R&#46; Rajagopal"
                            1 => "D&#46;I&#46; Masse"
                            2 => "G&#46; Singh"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1016/j.biortech.2013.06.030"
                      "Revista" => array:6 [
                        "tituloSerie" => "Bioresour Technol"
                        "fecha" => "2013"
                        "volumen" => "143"
                        "paginaInicial" => "632"
                        "paginaFinal" => "641"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/23835276"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            3 => array:3 [
              "identificador" => "bib0165"
              "etiqueta" => "4"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Stability and inhibition of anaerobic processes caused by insufficiency or excess of ammonia nitrogen"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:4 [
                            0 => "J&#46; Prochazka"
                            1 => "P&#46; Dolejs"
                            2 => "J&#46; Maca"
                            3 => "M&#46; Dohanyos"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1007/s00253-011-3625-4"
                      "Revista" => array:6 [
                        "tituloSerie" => "Appl Microbiol Biotechnol"
                        "fecha" => "2012"
                        "volumen" => "93"
                        "paginaInicial" => "439"
                        "paginaFinal" => "447"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/22002069"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            4 => array:3 [
              "identificador" => "bib0170"
              "etiqueta" => "5"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Inhibition of anaerobic digestion process&#58; a review"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:3 [
                            0 => "Y&#46; Chen"
                            1 => "J&#46;J&#46; Cheng"
                            2 => "K&#46;S&#46; Creamer"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1016/j.biortech.2007.01.057"
                      "Revista" => array:6 [
                        "tituloSerie" => "Bioresour Technol"
                        "fecha" => "2008"
                        "volumen" => "99"
                        "paginaInicial" => "4044"
                        "paginaFinal" => "4064"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/17399981"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            5 => array:3 [
              "identificador" => "bib0175"
              "etiqueta" => "6"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Ammonium inhibition through the decoupling of acidification process and methanogenesis in anaerobic digester revealed by high throughput sequencing"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:5 [
                            0 => "M&#46; Zhang"
                            1 => "Q&#46; Lin"
                            2 => "J&#46; Rui"
                            3 => "J&#46; Li"
                            4 => "X&#46; Li"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:4 [
                        "tituloSerie" => "Biotechnol Lett"
                        "fecha" => "2016"
                        "paginaInicial" => "1"
                        "paginaFinal" => "6"
                      ]
                    ]
                  ]
                ]
              ]
            ]
            6 => array:3 [
              "identificador" => "bib0180"
              "etiqueta" => "7"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Anaerobic digestion of slaughterhouse by-products"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
                            0 => "A&#46; Hejnfelt"
                            1 => "I&#46; Angelidaki"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:5 [
                        "tituloSerie" => "Biomass Bioenergy"
                        "fecha" => "2009"
                        "volumen" => "33"
                        "paginaInicial" => "1046"
                        "paginaFinal" => "1054"
                      ]
                    ]
                  ]
                ]
              ]
            ]
            7 => array:3 [
              "identificador" => "bib0185"
              "etiqueta" => "8"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Ammonia inhibition in high-solids biogasification&#58; an overview and practical solutions"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:1 [
                            0 => "M&#46; Kayhanian"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:5 [
                        "tituloSerie" => "Environ Technol"
                        "fecha" => "1999"
                        "volumen" => "20"
                        "paginaInicial" => "355"
                        "paginaFinal" => "365"
                      ]
                    ]
                  ]
                ]
              ]
            ]
            8 => array:3 [
              "identificador" => "bib0190"
              "etiqueta" => "9"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "The mechanism of ammonia inhibition in the thermophilic digestion of livestock wastes"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
                            0 => "W&#46; Wiegant"
                            1 => "G&#46; Zeeman"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:5 [
                        "tituloSerie" => "Agric Wastes"
                        "fecha" => "1986"
                        "volumen" => "16"
                        "paginaInicial" => "243"
                        "paginaFinal" => "253"
                      ]
                    ]
                  ]
                ]
              ]
            ]
            9 => array:3 [
              "identificador" => "bib0195"
              "etiqueta" => "10"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Influence of environmental conditions on methanogenic compositions in anaerobic biogas reactors"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:3 [
                            0 => "D&#46; Karakashev"
                            1 => "D&#46;J&#46; Batstone"
                            2 => "I&#46; Angelidaki"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:5 [
                        "tituloSerie" => "Appl Environ Microb"
                        "fecha" => "2005"
                        "volumen" => "71"
                        "paginaInicial" => "331"
                        "paginaFinal" => "338"
                      ]
                    ]
                  ]
                ]
              ]
            ]
            10 => array:3 [
              "identificador" => "bib0200"
              "etiqueta" => "11"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Ammonia&#44; a selective agent for methane production by syntrophic acetate oxidation at mesophilic temperature"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
                            0 => "A&#46; Schnurer"
                            1 => "A&#46; Nordberg"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.2166/wst.2008.097"
                      "Revista" => array:6 [
                        "tituloSerie" => "Water Sci Technol"
                        "fecha" => "2008"
                        "volumen" => "57"
                        "paginaInicial" => "735"
                        "paginaFinal" => "740"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/18401146"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            11 => array:3 [
              "identificador" => "bib0205"
              "etiqueta" => "12"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Effect of ammonia on the anaerobic degradation of protein by a mesophilic and thermophilic biowaste population"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:3 [
                            0 => "C&#46; Gallert"
                            1 => "S&#46; Bauer"
                            2 => "J&#46; Winter"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:6 [
                        "tituloSerie" => "Appl Microbiol Biotechnol"
                        "fecha" => "1998"
                        "volumen" => "50"
                        "paginaInicial" => "495"
                        "paginaFinal" => "501"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/9830101"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            12 => array:3 [
              "identificador" => "bib0210"
              "etiqueta" => "13"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Aminoacyl-tRNA synthesis"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
                            0 => "M&#46; Ibba"
                            1 => "D&#46; Soll"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1146/annurev.biochem.69.1.617"
                      "Revista" => array:6 [
                        "tituloSerie" => "Annu Rev Biochem"
                        "fecha" => "2000"
                        "volumen" => "69"
                        "paginaInicial" => "617"
                        "paginaFinal" => "650"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/10966471"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            13 => array:3 [
              "identificador" => "bib0215"
              "etiqueta" => "14"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Mitigating ammonia inhibition of thermophilic anaerobic treatment of digested piggery wastewater&#58; use of pH reduction&#44; zeolite&#44; biomass and humic acid"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
                            0 => "L&#46; Ho"
                            1 => "G&#46; Ho"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1016/j.watres.2012.05.016"
                      "Revista" => array:6 [
                        "tituloSerie" => "Water Res"
                        "fecha" => "2012"
                        "volumen" => "46"
                        "paginaInicial" => "4339"
                        "paginaFinal" => "4350"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/22739499"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            14 => array:3 [
              "identificador" => "bib0220"
              "etiqueta" => "15"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Standard Methods for the Examination of Water and Wastewater"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:1 [
                            0 => "APHA"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Libro" => array:3 [
                        "fecha" => "1998"
                        "editorial" => "American Public Health Association"
                        "editorialLocalizacion" => "Washington&#44; DC"
                      ]
                    ]
                  ]
                ]
              ]
            ]
            15 => array:3 [
              "identificador" => "bib0225"
              "etiqueta" => "16"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Nitrogen mineralization&#44; immobilization&#44; and nitrification"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:4 [
                            0 => "S&#46;C&#46; Hart"
                            1 => "J&#46;M&#46; Stark"
                            2 => "E&#46;A&#46; Davidson"
                            3 => "M&#46;K&#46; Firestone"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:5 [
                        "tituloSerie" => "Soil Sci Soc Am J"
                        "fecha" => "1994"
                        "volumen" => "44"
                        "paginaInicial" => "985"
                        "paginaFinal" => "1018"
                      ]
                    ]
                  ]
                ]
              ]
            ]
            16 => array:3 [
              "identificador" => "bib0230"
              "etiqueta" => "17"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "The metagenomics RAST server &#8211; a public resource for the automatic phylogenetic and functional analysis of metagenomes"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => true
                          "autores" => array:3 [
                            0 => "F&#46; Meyer"
                            1 => "D&#46; Paarmann"
                            2 => "M&#46; D&#39;Souza"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1186/1471-2105-9-1"
                      "Revista" => array:6 [
                        "tituloSerie" => "BMC Bioinformatics"
                        "fecha" => "2008"
                        "volumen" => "9"
                        "paginaInicial" => "1"
                        "paginaFinal" => "8"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/18173834"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            17 => array:3 [
              "identificador" => "bib0235"
              "etiqueta" => "18"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Metagenomic and metatranscriptomic analysis of microbial community structure and gene expression of activated sludge"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
                            0 => "K&#46; Yu"
                            1 => "T&#46; Zhang"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1371/journal.pone.0038183"
                      "Revista" => array:5 [
                        "tituloSerie" => "PLoS ONE"
                        "fecha" => "2012"
                        "volumen" => "7"
                        "paginaInicial" => "e38183"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/22666477"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            18 => array:3 [
              "identificador" => "bib0240"
              "etiqueta" => "19"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Controlling the false discovery rate&#58; a practical and powerful approach to multiple testing"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
                            0 => "Y&#46; Benjamini"
                            1 => "Y&#46; Hochberg"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:5 [
                        "tituloSerie" => "J R Stat Soc B"
                        "fecha" => "1995"
                        "volumen" => "57"
                        "paginaInicial" => "289"
                        "paginaFinal" => "300"
                      ]
                    ]
                  ]
                ]
              ]
            ]
            19 => array:3 [
              "identificador" => "bib0245"
              "etiqueta" => "20"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Cytoscape&#58; a software environment for integrated models of biomolecular interaction networks"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => true
                          "autores" => array:3 [
                            0 => "P&#46; Shannon"
                            1 => "A&#46; Markiel"
                            2 => "O&#46; Ozier"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1101/gr.1239303"
                      "Revista" => array:6 [
                        "tituloSerie" => "Genome Res"
                        "fecha" => "2003"
                        "volumen" => "13"
                        "paginaInicial" => "2498"
                        "paginaFinal" => "2504"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/14597658"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            20 => array:3 [
              "identificador" => "bib0250"
              "etiqueta" => "21"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Methane yield phenotypes linked to differential gene expression in the sheep rumen microbiome"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => true
                          "autores" => array:3 [
                            0 => "W&#46;B&#46; Shi"
                            1 => "C&#46;D&#46; Moon"
                            2 => "S&#46;C&#46; Leahy"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1101/gr.168245.113"
                      "Revista" => array:6 [
                        "tituloSerie" => "Genome Res"
                        "fecha" => "2014"
                        "volumen" => "24"
                        "paginaInicial" => "1517"
                        "paginaFinal" => "1525"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/24907284"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            21 => array:3 [
              "identificador" => "bib0255"
              "etiqueta" => "22"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Adaptation to pH and role of PacC in the rice blast fungus <span class="elsevierStyleItalic">Magnaporthe oryzae</span>"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:5 [
                            0 => "P&#46; Landraud"
                            1 => "S&#46; Chuzeville"
                            2 => "G&#46; Billon-Grande"
                            3 => "N&#46; Poussereau"
                            4 => "C&#46; Bruel"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:3 [
                        "tituloSerie" => "PLoS ONE"
                        "fecha" => "2013"
                        "paginaInicial" => "8"
                      ]
                    ]
                  ]
                ]
              ]
            ]
            22 => array:3 [
              "identificador" => "bib0260"
              "etiqueta" => "23"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Multiple two-component systems modulate alkali generation in <span class="elsevierStyleItalic">Streptococcus gordonii</span> in response to environmental stresses"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
                            0 => "Y&#46;L&#46; Liu"
                            1 => "R&#46;A&#46; Burne"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1128/JB.01053-09"
                      "Revista" => array:6 [
                        "tituloSerie" => "J Bacteriol"
                        "fecha" => "2009"
                        "volumen" => "191"
                        "paginaInicial" => "7353"
                        "paginaFinal" => "7362"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/19783634"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            23 => array:3 [
              "identificador" => "bib0265"
              "etiqueta" => "24"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Weak magnetic field&#58; a powerful strategy to enhance partial nitrification"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => true
                          "autores" => array:3 [
                            0 => "Z&#46;B&#46; Wang"
                            1 => "X&#46;L&#46; Liu"
                            2 => "S&#46;Q&#46; Ni"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1016/j.watres.2017.04.058"
                      "Revista" => array:6 [
                        "tituloSerie" => "Water Res"
                        "fecha" => "2017"
                        "volumen" => "120"
                        "paginaInicial" => "190"
                        "paginaFinal" => "198"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/28486170"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            24 => array:3 [
              "identificador" => "bib0270"
              "etiqueta" => "25"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Ammonia and temperature determine potential clustering in the anaerobic digestion microbiome"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => true
                          "autores" => array:3 [
                            0 => "J&#46; De Vrieze"
                            1 => "A&#46;M&#46; Saunders"
                            2 => "Y&#46; He"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1016/j.watres.2015.02.025"
                      "Revista" => array:6 [
                        "tituloSerie" => "Water Res"
                        "fecha" => "2015"
                        "volumen" => "75"
                        "paginaInicial" => "312"
                        "paginaFinal" => "323"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/25819618"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            25 => array:3 [
              "identificador" => "bib0275"
              "etiqueta" => "26"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Methanogenic population dynamics during startup of a full-scale anaerobic sequencing batch reactor treating swine waste"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:3 [
                            0 => "L&#46;T&#46; Angenent"
                            1 => "S&#46;W&#46; Sung"
                            2 => "L&#46; Raskin"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:6 [
                        "tituloSerie" => "Water Res"
                        "fecha" => "2002"
                        "volumen" => "36"
                        "paginaInicial" => "4648"
                        "paginaFinal" => "4654"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/12418668"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            26 => array:3 [
              "identificador" => "bib0280"
              "etiqueta" => "27"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Structure of the &#945;2¿2 Ni-dependent CO dehydrogenase component of the Methanosarcina barkeri acetyl-CoA decarbonylase&#47;synthase complex"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => true
                          "autores" => array:3 [
                            0 => "W&#46; Gong"
                            1 => "B&#46; Hao"
                            2 => "Z&#46; Wei"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1073/pnas.0800415105"
                      "Revista" => array:6 [
                        "tituloSerie" => "Proc Natl Acad Sci USA"
                        "fecha" => "2008"
                        "volumen" => "105"
                        "paginaInicial" => "9558"
                        "paginaFinal" => "9563"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/18621675"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            27 => array:3 [
              "identificador" => "bib0285"
              "etiqueta" => "28"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Crystal structure of methyl coenzyme M reductase&#58; the key enzyme of biological methane formation"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:5 [
                            0 => "U&#46; Ermler"
                            1 => "W&#46; Grabarse"
                            2 => "S&#46; Shima"
                            3 => "M&#46; Goubeaud"
                            4 => "R&#46;K&#46; Thauer"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:6 [
                        "tituloSerie" => "Science"
                        "fecha" => "1997"
                        "volumen" => "278"
                        "paginaInicial" => "1457"
                        "paginaFinal" => "1462"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/9367957"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            28 => array:3 [
              "identificador" => "bib0290"
              "etiqueta" => "29"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Synthesis of cell constituents from C2-units by a modified tricarboxylic acid cycle"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
                            0 => "H&#46; Kornberg"
                            1 => "H&#46; Krebs"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:6 [
                        "tituloSerie" => "Nature"
                        "fecha" => "1957"
                        "volumen" => "179"
                        "paginaInicial" => "988"
                        "paginaFinal" => "991"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/13430766"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
          ]
        ]
      ]
    ]
    "agradecimientos" => array:1 [
      0 => array:4 [
        "identificador" => "xack370732"
        "titulo" => "Acknowledgements"
        "texto" => "<p id="par0095" class="elsevierStylePara elsevierViewall">This work was supported by the <span class="elsevierStyleGrantSponsor" id="gs1">Key Project of Education Department of Sichuan Province</span> &#40;No&#46; <span class="elsevierStyleGrantNumber" refid="gs1">17ZA0215</span>&#41; and <span class="elsevierStyleGrantSponsor" id="gs2">Major Cultivation Project of Education Department of Sichuan Province</span> &#40;No&#46; <span class="elsevierStyleGrantNumber" refid="gs2">17CZ0018</span>&#41;&#46;</p>"
        "vista" => "all"
      ]
    ]
  ]
  "idiomaDefecto" => "en"
  "url" => "/15178382/0000004900000004/v1_201810050636/S1517838217309267/v1_201810050636/en/main.assets"
  "Apartado" => array:4 [
    "identificador" => "47987"
    "tipo" => "SECCION"
    "en" => array:2 [
      "titulo" => "Environmental Microbiology"
      "idiomaDefecto" => true
    ]
    "idiomaDefecto" => "en"
  ]
  "PDF" => "https://static.elsevier.es/multimedia/15178382/0000004900000004/v1_201810050636/S1517838217309267/v1_201810050636/en/main.pdf?idApp=UINPBA00004N&text.app=https://www.elsevier.es/"
  "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1517838217309267?idApp=UINPBA00004N"
]

Article information

ISSN: 15178382
Original language: English

DOI:10.1016/j.bjm.2018.04.008

The statistics are updated each day

Year/Month	Html	Pdf	Total

2024 October	8	3	11
2024 September	19	5	24
2024 August	24	5	29
2024 July	14	6	20
2024 June	22	4	26
2024 May	23	2	25
2024 April	21	2	23
2024 March	19	3	22
2024 February	20	5	25
2024 January	36	11	47
2023 December	32	6	38
2023 November	30	14	44
2023 October	68	8	76
2023 September	53	1	54
2023 August	34	8	42
2023 July	19	3	22
2023 June	37	9	46
2023 May	61	10	71
2023 April	48	3	51
2023 March	38	5	43
2023 February	21	4	25
2023 January	18	4	22
2022 December	28	6	34
2022 November	20	14	34
2022 October	50	8	58
2022 September	19	17	36
2022 August	19	9	28
2022 July	20	12	32
2022 June	25	13	38
2022 May	36	15	51
2022 April	23	19	42
2022 March	26	6	32
2022 February	26	10	36
2022 January	35	16	51
2021 December	27	7	34
2021 November	27	21	48
2021 October	37	24	61
2021 September	19	12	31
2021 August	13	11	24
2021 July	17	13	30
2021 June	25	6	31
2021 May	15	15	30
2021 April	58	43	101
2021 March	21	23	44
2021 February	16	14	30
2021 January	21	14	35
2020 December	16	9	25
2020 November	13	2	15
2020 October	15	3	18
2020 September	21	18	39
2020 August	22	12	34
2020 July	24	14	38
2020 June	16	9	25
2020 May	22	6	28
2020 April	17	11	28
2020 March	11	5	16
2020 February	13	3	16
2020 January	11	8	19
2019 December	16	9	25
2019 November	14	7	21
2019 October	20	9	29
2019 September	18	8	26
2019 August	8	3	11
2019 July	8	11	19
2019 June	16	17	33
2019 May	7	11	18
2019 February	1	1	2
2018 November	33	25	58
2018 October	28	25	53
2018 September	0	14	14
2018 August	0	20	20
2018 July	1	23	24
2018 June	0	8	8

Show all

Indexed in:

Follow us:

Statistics

Indexed in:

Follow us:

Statistics

Subscribe to our newsletter