Effect of different polyphenol sources on the efficiency of ellagic acid release by Aspergillus niger

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If all letters next to a bar are different from the letters in another bar, there are significant differences among the treatments, if they have a common letter, they are not significantly different (p<0.05)." ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Amani Lahouar, Sonia Marin, Ana Crespo-Sempere, Salem Saïd, Vicente Sanchis" "autores" => array:5 [ 0 => array:2 [ "nombre" => "Amani" "apellidos" => "Lahouar" ] 1 => array:2 [ "nombre" => "Sonia" "apellidos" => "Marin" ] 2 => array:2 [ "nombre" => "Ana" "apellidos" => "Crespo-Sempere" ] 3 => array:2 [ "nombre" => "Salem" "apellidos" => "Saïd" ] 4 => array:2 [ "nombre" => "Vicente" "apellidos" => "Sanchis" ] ] ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754115001297?idApp=UINPBA00004N" "url" => "/03257541/0000004800000001/v1_201603250025/S0325754115001297/v1_201603250025/en/main.assets" ] "itemAnterior" => array:19 [ "pii" => "S0325754115001674" "issn" => "03257541" "doi" => "10.1016/j.ram.2015.12.002" "estado" => "S300" "fechaPublicacion" => "2016-01-01" "aid" => "82" "copyright" => "Asociación Argentina de Microbiología" "documento" => "article" "crossmark" => 1 "licencia" => "http://creativecommons.org/licenses/by-nc-nd/4.0/" "subdocumento" => "fla" "cita" => "Rev Argent Microbiol. 2016;48:67-70" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:2 [ "total" => 1627 "formatos" => array:3 [ "EPUB" => 63 "HTML" => 952 "PDF" => 612 ] ] "es" => array:12 [ "idiomaDefecto" => true "cabecera" => "INFORME BREVE" "titulo" => "Detección de Brachyspira pilosicoli y otras especies de Brachyspira en granjas avícolas argentinas" "tienePdf" => "es" "tieneTextoCompleto" => "es" "tieneResumen" => array:2 [ 0 => "es" 1 => "en" ] "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "67" "paginaFinal" => "70" ] ] "titulosAlternativos" => array:1 [ "en" => array:1 [ "titulo" => "Detection of Brachyspira pilosicoli and other Brachyspira species in Argentine poultry farms" ] ] "contieneResumen" => array:2 [ "es" => true "en" => true ] "contieneTextoCompleto" => array:1 [ "es" => true ] "contienePdf" => array:1 [ "es" => true ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Natalia V. Illanes, Pablo J. Tamiozzo, Ana Cabral, Judith Bertone, Silvia Romanini, Raúl Yaciuk, Mercedes Vázquez, Bibiana R. Pelliza" "autores" => array:8 [ 0 => array:2 [ "nombre" => "Natalia V." "apellidos" => "Illanes" ] 1 => array:2 [ "nombre" => "Pablo J." "apellidos" => "Tamiozzo" ] 2 => array:2 [ "nombre" => "Ana" "apellidos" => "Cabral" ] 3 => array:2 [ "nombre" => "Judith" "apellidos" => "Bertone" ] 4 => array:2 [ "nombre" => "Silvia" "apellidos" => "Romanini" ] 5 => array:2 [ "nombre" => "Raúl" "apellidos" => "Yaciuk" ] 6 => array:2 [ "nombre" => "Mercedes" "apellidos" => "Vázquez" ] 7 => array:2 [ "nombre" => "Bibiana R." "apellidos" => "Pelliza" ] ] ] ] ] "idiomaDefecto" => "es" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754115001674?idApp=UINPBA00004N" "url" => "/03257541/0000004800000001/v1_201603250025/S0325754115001674/v1_201603250025/es/main.assets" ] "en" => array:20 [ "idiomaDefecto" => true "cabecera" => "Original article" "titulo" => "Effect of different polyphenol sources on the efficiency of ellagic acid release by Aspergillus niger" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "71" "paginaFinal" => "77" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Leonardo Sepúlveda, Reynaldo de la Cruz, José Juan Buenrostro, Juan Alberto Ascacio-Valdés, Antonio Francisco Aguilera-Carbó, Arely Prado, Raúl Rodríguez-Herrera, Cristóbal Noé Aguilar" "autores" => array:8 [ 0 => array:3 [ "nombre" => "Leonardo" "apellidos" => "Sepúlveda" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 1 => array:3 [ "nombre" => "Reynaldo" "apellidos" => "de la Cruz" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 2 => array:3 [ "nombre" => "José Juan" "apellidos" => "Buenrostro" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "c" "identificador" => "aff0015" ] ] ] 3 => array:3 [ "nombre" => "Juan Alberto" "apellidos" => "Ascacio-Valdés" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 4 => array:3 [ "nombre" => "Antonio Francisco" "apellidos" => "Aguilera-Carbó" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 5 => array:3 [ "nombre" => "Arely" "apellidos" => "Prado" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "c" "identificador" => "aff0015" ] ] ] 6 => array:3 [ "nombre" => "Raúl" "apellidos" => "Rodríguez-Herrera" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 7 => array:4 [ "nombre" => "Cristóbal Noé" "apellidos" => "Aguilar" "email" => array:1 [ 0 => "cristobal.aguilar@uadec.edu.mx" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] ] "afiliaciones" => array:3 [ 0 => array:3 [ "entidad" => "Food Research Department, School of Chemistry, Universidad Autónoma de Coahuila, 25280 Saltillo, Coahuila, Mexico" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Animal Nutrition Department, Universidad Autónoma Agraria Antonio Narro, 25315, Buenavista, Saltillo, Coahuila, Mexico" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Department of Biotechnology, Departamento de Biotecnología, Universidad Autónoma Metropolitana, 09340 Iztapalapa, Mexico" "etiqueta" => "c" "identificador" => "aff0015" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Efecto de las diferentes fuentes de polifenoles sobre la eficiencia de liberación de ácido elágico por Aspergillus niger" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 1406 "Ancho" => 1379 "Tamanyo" => 84817 ] ] "descripcion" => array:1 [ "en" => "EA accumulation kinetics using: () CBP-A-GH1; (■) CBP-A-HT4; (▴) CBP-A-PSH in SSC." ] ] ] "textoCompleto" => "IntroductionPolyphenols are a wide range of compounds considered to be secondary metabolites of different plant parts: leaves, stems, flowers, fruits, seeds, and others<a class="elsevierStyleCrossRef" href="#bib0155">2</a>. Polyphenols are divided into three main groups: complex tannins, condensed tannins and hydrolyzable tannins<a class="elsevierStyleCrossRef" href="#bib0230">17</a>. Ellagitannins are a class of hydrolyzable tannins. These compounds are essentially formed by a hexahydroxydiphenic acid (HHDP) group linked by an ester bond to a glucose<a class="elsevierStyleCrossRef" href="#bib0185">8</a>. There are over 500 different structures of ellagitannins reported in the literature<a class="elsevierStyleCrossRef" href="#bib0210">13</a>. Ellagitannins are mainly obtained from the bark and trunks of trees such as oak (Quercus spp.)<a class="elsevierStyleCrossRef" href="#bib0235">18</a> and eucalyptus (Eucalyptus spp.)<a class="elsevierStyleCrossRef" href="#bib0240">19</a>. Ellagitannins are abundant in some red berries<a class="elsevierStyleCrossRef" href="#bib0265">24</a>, plants of the Mexican desert<a class="elsevierStyleCrossRef" href="#bib0175">6</a> and pomegranate fruit<a class="elsevierStyleCrossRef" href="#bib0255">22</a>. Ellagitannins have various beneficial health properties. It has been shown that the ellagitannins present in pomegranate juice can induce apoptosis by activation of the leukemic cell cycle<a class="elsevierStyleCrossRef" href="#bib0200">11</a>. Punicalagin is an ellagitannin from the pomegranate peel, which has been linked to apoptosis in HT-29 colon cancer cells<a class="elsevierStyleCrossRef" href="#bib0260">23</a>. Ellagitannins present in leaf extracts, flower extracts, peel, juice and seeds of pomegranate have beneficial effects on the control of obesity, diabetes, cardiovascular disease, hypertension and hypercholesterolemia<a class="elsevierStyleCrossRef" href="#bib0170">5</a>. Moreover, these polyphenols in pomegranate leaves, obtained by macroporous resin column chromatography have a high antioxidant activity<a class="elsevierStyleCrossRef" href="#bib0290">29</a>. Ellagitannins can be hydrolyzed by chemical or enzymatic methods to release the HHDP group<a class="elsevierStyleCrossRef" href="#bib0220">15</a>; this group undergoes a spontaneous molecular arrangement forming a new molecule called ellagic acid (EA)<a class="elsevierStyleCrossRef" href="#bib0160">3</a>. EA is a secondary metabolite of high industrial interest due to various beneficial effect on human health such as antiviral<a class="elsevierStyleCrossRef" href="#bib0225">16</a>, anticarcinogenic<a class="elsevierStyleCrossRef" href="#bib0245">20</a>, antioxidant<a class="elsevierStyleCrossRef" href="#bib0275">26</a>, and anti-inflammatory activities<a class="elsevierStyleCrossRef" href="#bib0195">10</a>. Industrially, EA is obtained with the use of chemicals, involving high production costs and recovery as well as environmental damage. Therefore, it is necessary to develop methods for the biotechnological production of secondary metabolites. There are few studies about obtaining EA by bioprocessing agroindustrial residues such as pomegranate peel and microorganisms that are capable of degrading the ellagitannin compounds present in the waste by solid-state culture (SSC) to generate EA<a class="elsevierStyleCrossRef" href="#bib0270">25</a>. The aim of this work was to evaluate the effect of different polyphenol sources: cranberry (CP), creosote bush (CBP) and pomegranate (PP) on the hydrolytic efficiency of three different xerophilic Aspergillus niger strains, denominated A-GH1, A-PSH and A-HT4, to obtain EA by SSC.Materials and methodsPolyphenol extraction and purificationCranberries (Vaccinium macrocarpon Ait.) were originally from Wisconsin, USA, and were received in vacuum packed bags (350g) in the month of January of the year 2012. Pomegranates (Punica granatum L. var. Wonderful) were originally from California, USA, and were received in cardboard boxes (25kg), in the same session and year. These fruits were purchased at a supermarket in Saltillo, Coahuila, Mexico. Creosote bush plants (Larrea tridentate Sesse & Mocino ex DC. Coville) were manually collected in Federal Highway 57 along 15km of the Saltillo-Monclova stretch, in Coahuila State, Mexico in the second semester of the year 2011. Pomegranate peel, cranberry and creosote bush leaves were dehydrated at 60°C for 48h, then pulverized in a grinder (PULVEX® Mini 100) to obtain a particle size of 600μm and taken to constant weight<a class="elsevierStyleCrossRef" href="#bib0270">25</a>. Polyphenols were extracted according to the methodology proposed by Ascacio-Valdés et al<a class="elsevierStyleCrossRef" href="#bib0175">6</a>. Substrate was hydrated at 1:5 ratio (100g substrate/500ml distilled water) and incubated at 60°C for 30min. The substrate mass was filtered through muslin cloth and the extract obtained was centrifuged at 3000rpm for 15min. The supernatant was purified by chromatography (Amberlite XAD-resin 16®). The extracts were eluted with distilled water (dH2O) to remove soluble compounds. The polyphenolic compound-rich fraction was eluted with 96% ethanol. Finally, the ethanol was evaporated in a heating oven (NAPCO® Model 322) at 60°C for 24h. The CP CBB and PP were obtained as a fine powder.Support preparationThe use of polyurethane foam (PUF) as inert support for polyphenol biodegradation was assessed. The PUF was cut and ground to a particle size of 0.85mm, then washed (3×) with hot water (80–90°C) for 10min, filtered to eliminate and dried until constant weight<a class="elsevierStyleCrossRef" href="#bib0250">21</a>.Microorganisms and culture mediaA. niger GH1, A. niger PSH and A. niger HT4 strains were supplied by DIA-UAdeC (Departamento de Investigación en Alimentos, Universidad Autónoma de Coahuila). These strains have the ability to degrade substrates rich in polyphenols<a class="elsevierStyleCrossRefs" href="#bib0160">3,12,22</a>. The strains were activated in potato dextrose agar (PDA-Bioxon), and incubated at 30°C for 5 days. Spores were harvested with 0.01% Tween-80 and counted in a Neubauer® chamber. Pontecorvo culture medium having the following composition (g/l): NaNO3 6.0, KH2PO4 1.52, KCl 0.52 MgSO4·7H2O 0.52, ZnSO4 0.001, FeCl 0.85 and 1ml trace metals was used. The trace metal solution contained (mg/l) Na2B4O7·10H2O 10, MnCl2·4H2O 50, Na2MoO4·2H2O 50 and CuSO4·5H2O 250. The carbon source (30g/l) was supplemented with either CP, CBP or PP<a class="elsevierStyleCrossRef" href="#bib0180">7</a> and the initial culture medium pH was adjusted to 6.5 with 1M NaOH. An inoculum size of 2×107 spores per g of culture material was used.SSC conditionsThe SSC was prepared as follows: 0.5g of PUF was homogenized with 1.16ml of culture medium (70% humidity) and packed in columns (0.5cm×5cm) at a packing density of 0.08g/cm3. The solid-state culture was performed for 32h at 30°C, with sampling every 8h (two columns by treatment)<a class="elsevierStyleCrossRef" href="#bib0190">9</a>. The enzymatic extract of the culture was obtained by adding 1.16ml of 50mM citrate buffer (pH 5) within each column, the mass culture was mixed and the extract was obtained by manual pressing. To recover the EA, an ethanol–formic acid (1.16ml of 0.01%) solution was added<a class="elsevierStyleCrossRef" href="#bib0270">25</a> and the extracts obtained were filtered (0.45μm) and frozen until analysis.Ellagitannase activity assayEllagitannase activity was carried out according to the methodology suggested by De la Cruz et al<a class="elsevierStyleCrossRef" href="#bib0205">12</a>. Ellagitannins 1mg/ml in 50mM citrate buffers, pH 5, were used as enzyme substrate. A substrate control (1ml ellagitannins and 50μl of 50mM citrate buffers, pH 5), enzyme control (1ml of 50mM citrate buffers, pH 5 and 50μl of enzymatic extract) and the reaction mixture (1ml of ellagitannins and 50μl of enzymatic extract) were prepared. The reaction was done in a water bath for 10min at 60°C. The reaction was stopped by adding 1050μl of absolute ethanol. Then, samples were sonicated for 25min, filtered through 0.45μm nylon membrane and collected in vials. One ellagitannase enzymatic unit was defined as the enzyme amount needed to release 1μmol of EA per min, under the conditions described.HPLC analysisQuantification of EA was performed on a Varian ProStar model 2301 HPLC. A column Pursuit XRs 5um C18 (150mm×46mm) and, (A) methanol (washing phase), (B) acetonitrile and (C) acetic acid 3% (mobile phase). The flow rate was 1ml/min, at a column temperature of 30°C. Standard curve of EA (≥95%, Sigma–Aldrich®) from 0 to 500μg/ml was prepared<a class="elsevierStyleCrossRef" href="#bib0180">7</a>.Data analysisThe effect of the different polyphenol sources and strains on EA accumulation was assessed under a 3×3 factorial design with two replicates. Data were analyzed by ANOVA using SAS 9.0 and means were compared by Tukey's multiple range procedure (p≤0.05) when needed.ResultsKinetics of EA accumulationCulture kinetics of A-GH1, A-PSH and A-HT4 strains and three culture media enriched with CP, CBP and PP were studied. The kinetic profile when using CP as polyphenolic substrate (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>) showed the highest EA accumulation (74.56mg/g) with the A-PSH strain at 8h of culture followed by the A-HT4 strain (69.55mg/g) at 32h of culture and A-GH1 (64.35mg/g) at 32h of culture. The A-HT4 strain produced 13.69% more EA than the A-GH1 strain; however the former strain also required a 4-fold increase in the culture time required by the A-GH1 strain. Therefore, in terms of process time, A-GH1 resulted in higher EA accumulation than A-HT4. <a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a> shows the EA accumulation profile when using CBP. Total EA accumulation by the different strains was 182.92, 158.54 and 125.97mg/g using A-GH1, A-HT4 and A-PSH strains respectively; however, A-HT4 reached 158.54mg/g in an 8h culture while A-GH1 reached in 32h culture. Once again, a lower EA accumulation value (158.54mg/g) could be observed in one of the strains tested (A-HT4) but a culture time 4 times lower than in strain A-GH1 that showed the highest EA accumulation (182.92mg/g). In contrast, when using PP as substrate, EA accumulation was 163.03, 350.21 and 200.33mg/g for A-GH1 (8h culture), A-HT4 (16h of culture) and A-PSH (16h culture) respectively; the highest EA accumulation occurred at 16h of culture when using A-HT4 and no EA increase was observed at any other time (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>).<elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia><elsevierMultimedia ident="fig0015"></elsevierMultimedia>Ellagitannase activity and productivityEllagitannase activity reached maximum value of 5176.81U/l when using CP as carbon source and A-PSH at 8h of SSC (<a class="elsevierStyleCrossRef" href="#fig0020">Fig. 4</a>). Other strains reached maximum values in the first 8h and then these values were kept constant. <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> shows effect of substrates, strains and interaction on ellagitannase activity and EA productivity. EA productivity was defined as the ratio among the maximum accumulation of EA per culture time. In <a class="elsevierStyleCrossRef" href="#fig0025">Fig. 5</a>, the values of EA productivity are displayed at a time of 16h, which corresponds to the time of maximal EA accumulation obtained. In <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>, the individual effect of each variable, validated by a Tukey test on ellagitannase activity and EA productivity is shown. Then the highest productivity (21.89mg/g/h), was obtained when using the Aspergillus strain coded as A-HT4 and CP as source. It was observed that when A-HT4 and CP were used, a maximum productivity of 21.89mg/g/h was reached.<elsevierMultimedia ident="fig0020"></elsevierMultimedia><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="fig0025"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia>DiscussionThe A-PSH strain has been reported to have the ability to produce EA by hydrolysis of the pomegranate peel by SSC<a class="elsevierStyleCrossRef" href="#bib0255">22</a>. Moreover, this strain also showed the ability to degrade hydrolyzable tannins from extracts of creosote bush (L. tridentata) and tarbush (Flourensia cernua) releasing EA and gallic acid by SSC<a class="elsevierStyleCrossRef" href="#bib0285">28</a>. Furthermore, the A-GH1 strain has been reported for the hydrolysis of polyphenolic compounds from pomegranate peel, reaching 17mg/g of EA at 32h by SSC<a class="elsevierStyleCrossRef" href="#bib0165">4</a>. Vattem and Shetty (2003) reported the use of cranberry pomace and Lentinus edodes strain for EA production reaching a maximum accumulation of 350μg/g of EA by dried cranberry pomace and they attributed the EA accumulation to the β-glucosidase enzyme<a class="elsevierStyleCrossRef" href="#bib0280">27</a>. In this work, when A-HT4 strain and PP are used, a maximum of 350.21mg/g of EA at 16h is reached. It has also been reported that the pomegranate peel is an excellent carbon source for EA production, using an A. niger strain<a class="elsevierStyleCrossRef" href="#bib0150">1</a>. Recent studies mention that there is a possible set of enzymes that are responsible for the release of the HHDP group and formation consequence of EA<a class="elsevierStyleCrossRef" href="#bib0180">7</a>.The values of ellagitannase activity obtained in this study are 166-fold higher than those reported by Aguilera-Carbó et al<a class="elsevierStyleCrossRef" href="#bib0165">4</a>. These authors reported values of 44.5U/l using pomegranate peel as carbon source and A-GH1 at 48h of culture time. Similar studies obtained maximum values of ellagitannase activity (2189.94U/l) at 30h of SSC using PP as carbon source and several fungal strains (A. niger PSH, A. niger GH1, A. niger HT4 and A. niger HC2)<a class="elsevierStyleCrossRef" href="#bib0205">12</a>. Several enzymes responsible for ellagitannin hydrolysis have been reported; however, the authors found that only ellagitannase, clearly associated with EA accumulation on SSC, reached maximum values (200.04U/l) at 12h of SSC using PP and A. niger GH1 strain<a class="elsevierStyleCrossRef" href="#bib0180">7</a>. The authors reported that EA production is higher using partially purified polyphenols, since these molecules have a glucose core, making them more susceptible to attack by microbial enzymes<a class="elsevierStyleCrossRef" href="#bib0215">14</a>. There are a few studies about the use of polyphenols from plants, barks or fruits SSC for obtaining secondary metabolites. The productivity obtained with CP and the A-HT4 strain is higher compared with that in previous reports using valonia tannins as a carbon source, reaching values of 0.92U/l/h<a class="elsevierStyleCrossRef" href="#bib0200">11</a>. The A-GH1 strain has been associated with the release of EA from creosote bush extracts by SSC, reaching a productivity of 1.22U/l/h<a class="elsevierStyleCrossRef" href="#bib0165">4</a>.In conclusion, it was possible to obtain EA from rich substrates in polyphenolic compounds using A. niger strains in SSC. A-HT4 reached a maximum EA value (350.21mg/g of PP at SSC). When CP and the A-PSH strain was used, high values of ellagitannase activity (5176.81U/l) were obtained at 8h of SSC. The EA release mechanism is unknown due to EA complexity; however ellagitannase is one of the enzymes that may be responsible for the hydrolysis of the ester link in the HHDP group to generate EA.Conflict of interestThe authors declare that they have no conflicts of interest.Ethical disclosuresProtection of human and animal subjectsThe authors declare that no experiments were performed on humans or animals for this investigation.Confidentiality of dataThe authors declare that no patient data appears in this article.Right to privacy and informed consentThe authors declare that no patient data appears in this article." "textoCompletoSecciones" => array:1 [ "secciones" => array:12 [ 0 => array:3 [ "identificador" => "xres620840" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec635124" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres620841" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec635125" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:3 [ "identificador" => "sec0010" "titulo" => "Materials and methods" "secciones" => array:7 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Polyphenol extraction and purification" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Support preparation" ] 2 => array:2 [ "identificador" => "sec0025" "titulo" => "Microorganisms and culture media" ] 3 => array:2 [ "identificador" => "sec0030" "titulo" => "SSC conditions" ] 4 => array:2 [ "identificador" => "sec0035" "titulo" => "Ellagitannase activity assay" ] 5 => array:2 [ "identificador" => "sec0040" "titulo" => "HPLC analysis" ] 6 => array:2 [ "identificador" => "sec0045" "titulo" => "Data analysis" ] ] ] 6 => array:3 [ "identificador" => "sec0050" "titulo" => "Results" "secciones" => array:2 [ 0 => array:2 [ "identificador" => "sec0055" "titulo" => "Kinetics of EA accumulation" ] 1 => array:2 [ "identificador" => "sec0060" "titulo" => "Ellagitannase activity and productivity" ] ] ] 7 => array:2 [ "identificador" => "sec0065" "titulo" => "Discussion" ] 8 => array:2 [ "identificador" => "sec0070" "titulo" => "Conflict of interest" ] 9 => array:3 [ "identificador" => "sec0075" "titulo" => "Ethical disclosures" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0080" "titulo" => "Protection of human and animal subjects" ] 1 => array:2 [ "identificador" => "sec0085" "titulo" => "Confidentiality of data" ] 2 => array:2 [ "identificador" => "sec0090" "titulo" => "Right to privacy and informed consent" ] ] ] 10 => array:2 [ "identificador" => "xack209308" "titulo" => "Acknowledgements" ] 11 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2014-12-07" "fechaAceptado" => "2015-08-05" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec635124" "palabras" => array:4 [ 0 => "Polyphenols" 1 => "Aspergillus niger" 2 => "Solid-state culture" 3 => "Ellagitannase" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec635125" "palabras" => array:4 [ 0 => "Polifenoles" 1 => "Aspergillus niger" 2 => "Cultivo en estado sólido" 3 => "Elagitanasa" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "Fungal hydrolysis of ellagitannins produces hexahydroxydiphenic acid, which is considered an intermediate molecule in ellagic acid release. Ellagic acid has important and desirable beneficial health properties. The aim of this work was to identify the effect of different sources of ellagitannins on the efficiency of ellagic acid release by Aspergillus niger. Three strains of A. niger (GH1, PSH and HT4) were assessed for ellagic acid release from different polyphenol sources: cranberry, creosote bush, and pomegranate used as substrate. Polyurethane foam was used as support for solid-state culture in column reactors. Ellagitannase activity was measured for each of the treatments. Ellagic acid was quantified by high performance liquid chromatography. When pomegranate polyphenols were used, a maximum value of ellagic acid (350.21mg/g) was reached with A. niger HT4 in solid-state culture. The highest amount of ellagitannase (5176.81U/l) was obtained at 8h of culture when cranberry polyphenols and strain A. niger PSH were used. Results demonstrated the effect of different polyphenol sources and A. niger strains on ellagic acid release. It was observed that the best source for releasing ellagic acid was pomegranate polyphenols and A. niger HT4 strain, which has the ability to degrade these compounds for obtaining a potent bioactive molecule such as ellagic acid." ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "La hidrólisis fúngica de los elagitaninos produce ácido hexahidroxidifénico, considerado como una molécula intermedia en la liberación de ácido elágico. El ácido elágico tiene importantes y deseables propiedades benéficas para la salud humana. El objetivo de este trabajo fue identificar el efecto de la fuente de elagitaninos sobre la eficiente liberación de ácido elágico por Aspergillus niger. La liberación de ácido elágico se realizó con tres cepas de A. niger (GH1, PSH y HT4) en presencia de diferentes fuentes de polifenoles (arándano, gobernadora y granada), usadas como sustrato. Se empleó espuma de poliuretano como soporte para el cultivo en estado sólido en reactores en columna. Se midió la actividad elagitanasa a cada uno de los tratamientos. El ácido elágico liberado se cuantificó por cromatografía líquida de alta resolución. Cuando se utilizaron los polifenoles de granada, se alcanzó un valor máximo de 350,21mg/g de ácido elágico con A. niger HT4 en cultivo en estado sólido. La mayor actividad elagitanasa (5176.81 U/l) se obtuvo a 8 h de cultivo cuando se usaron los polifenoles de arándano como sustrato y A. niger PSH. Los resultados demostraron el efecto que tiene la fuente de polifenoles y la cepa de A. niger en la liberación de ácido elágico. Se observó que la mejor fuente para la liberación de ácido elágico fueron los polifenoles de granada y que la cepa A. niger HT4 posee la habilidad de degradar estos compuestos para la obtención de potentes moléculas bioactivas, como el ácido elágico." ] ] "multimedia" => array:10 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1488 "Ancho" => 1388 "Tamanyo" => 84545 ] ] "descripcion" => array:1 [ "en" => "EA accumulation kinetics using: () CP-A-GH1; (■) CP-A-HT4; (▴) CP-A-PSH in SSC." ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 1406 "Ancho" => 1379 "Tamanyo" => 84817 ] ] "descripcion" => array:1 [ "en" => "EA accumulation kinetics using: () CBP-A-GH1; (■) CBP-A-HT4; (▴) CBP-A-PSH in SSC." ] ] 2 => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 1431 "Ancho" => 1528 "Tamanyo" => 86588 ] ] "descripcion" => array:1 [ "en" => "EA accumulation kinetics using: () PP-A-GH1; (■) PP-A-HT4; (▴) PP-A-PSH in SSC." ] ] 3 => array:7 [ "identificador" => "fig0020" "etiqueta" => "Figure 4" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr4.jpeg" "Alto" => 1592 "Ancho" => 1508 "Tamanyo" => 139391 ] ] "descripcion" => array:1 [ "en" => "Values of ellagitannase activity, () CP-A-GH1; (■) CP-A-HT4; (▴) CP-A-PSH; (X) CBP-A-GH1; (*) CBP-A-HT4; (●) CBP-A-PSH; (|) PP-A-GH1: (--) PP-A-HT4; (– -) PP-A-PSH." ] ] 4 => array:7 [ "identificador" => "fig0025" "etiqueta" => "Figure 5" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr5.jpeg" "Alto" => 1407 "Ancho" => 1651 "Tamanyo" => 91407 ] ] "descripcion" => array:1 [ "en" => "EA productivity, (<elsevierMultimedia ident="201603250029258521"></elsevierMultimedia>) CP-A-GH1; CP-A-HT4; CP-A-PSH; (<elsevierMultimedia ident="201603250029258522"></elsevierMultimedia>) CBP-A-GH1; CBP-A-HT4; CBP-A-PSH; (<elsevierMultimedia ident="201603250029258523"></elsevierMultimedia>) PP-A-GH1; PP-A-HT4; PP-A-PSH." ] ] 5 => array:7 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:3 [ "leyenda" => "S*X=combined effect of substrate and strains." "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">Responses \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Source of variation \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">df<a class="elsevierStyleCrossRef" href="#tblfn0005">a</a> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">MS<a class="elsevierStyleCrossRef" href="#tblfn0010">b</a> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">p-Value \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">F-test \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">EA productivity \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Replicate \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.00 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.98 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.00 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">S<a class="elsevierStyleCrossRef" href="#tblfn0015">c</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1252.51 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top"><.0001 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">858.68 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">X<a class="elsevierStyleCrossRef" href="#tblfn0020">d</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">487.89 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top"><.0001 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">334.43 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">S*X \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">382.99 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top"><.0001 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">262.52 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="6" align="left" valign="top">R2=0.997</td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="6" align="left" valign="top"></td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ellagitannase activity \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Replicate \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">17034.93 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.26 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.50 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">S<a class="elsevierStyleCrossRef" href="#tblfn0015">c</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">43399.04 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.07 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.82 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">X<a class="elsevierStyleCrossRef" href="#tblfn0020">d</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">230928.25 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top"><.0001 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">20.32 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">S*X \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">112108.11 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top"><.0001 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">9.86 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="6" align="left" valign="top">R2=0.917</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1017942.png" ] ] ] "notaPie" => array:4 [ 0 => array:3 [ "identificador" => "tblfn0005" "etiqueta" => "a" "nota" => "Degree of freedom." ] 1 => array:3 [ "identificador" => "tblfn0010" "etiqueta" => "b" "nota" => "Mean square." ] 2 => array:3 [ "identificador" => "tblfn0015" "etiqueta" => "c" "nota" => "Substrate (polyphenols)." ] 3 => array:3 [ "identificador" => "tblfn0020" "etiqueta" => "d" "nota" => "Strains (A. niger)." ] ] ] "descripcion" => array:1 [ "en" => "Analysis of variance for EA productivity and ellagitannase activity" ] ] 6 => array:7 [ "identificador" => "tbl0010" "etiqueta" => "Table 2" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:2 [ "leyenda" => "Means with the same letter, in the same column, are not significantly different according to the Tukey's multiple range test (p<0.05)." "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">Substrate \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">EA productivity (mg/g/h) \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Ellagitannase activity (U/l) \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">PP \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">40.59 a \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2721.38 a \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">PCB \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">22.06 b \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2671.36 a \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">PC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">12.13 c \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2837.17 a \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="3" align="left" valign="top"></td></tr><tr title="table-row"><td class="td" title="table-entry " colspan="3" align="left" valign="top">Strains</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">A-HT4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">35.11 a \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2733.28 b \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">A-PSH \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">21.76 b \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2944.31 a \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">A-GH1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">17.92 c \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2552.33 c \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1017941.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Substrate and strain effect on EA productivity and ellagitannase activity" ] ] 7 => array:5 [ "identificador" => "201603250029258521" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => false "mostrarDisplay" => true "figura" => array:1 [ 0 => array:4 [ "imagen" => "fx1.jpeg" "Alto" => 42 "Ancho" => 54 "Tamanyo" => 10911 ] ] ] 8 => array:5 [ "identificador" => "201603250029258522" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => false "mostrarDisplay" => true "figura" => array:1 [ 0 => array:4 [ "imagen" => "fx2.jpeg" "Alto" => 42 "Ancho" => 55 "Tamanyo" => 8054 ] ] ] 9 => array:5 [ "identificador" => "201603250029258523" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => false "mostrarDisplay" => true "figura" => array:1 [ 0 => array:4 [ "imagen" => "fx3.jpeg" "Alto" => 42 "Ancho" => 53 "Tamanyo" => 10964 ] ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:29 [ 0 => array:3 [ "identificador" => "bib0150" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Production of antioxidant nutraceuticals by solid-state cultures of pomegranate (Punica granatum) peel and creosote bush (Larrea tridentata) leaves" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:8 [ 0 => "C.N. 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"vista" => "all" ] ] ] "idiomaDefecto" => "en" "url" => "/03257541/0000004800000001/v1_201603250025/S0325754115001285/v1_201603250025/en/main.assets" "Apartado" => array:4 [ "identificador" => "37862" "tipo" => "SECCION" "en" => array:2 [ "titulo" => "Microbiología agrícola, ambiental e industrial" "idiomaDefecto" => true ] "idiomaDefecto" => "en" ] "PDF" => "https://static.elsevier.es/multimedia/03257541/0000004800000001/v1_201603250025/S0325754115001285/v1_201603250025/en/main.pdf?idApp=UINPBA00004N&text.app=https://www.elsevier.es/" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754115001285?idApp=UINPBA00004N"]

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Efecto de las diferentes fuentes de polifenoles sobre la eficiencia de liberación de ácido elágico por Aspergillus niger

Leonardo Sepúlvedaa, Reynaldo de la Cruza, José Juan Buenrostroc, Juan Alberto Ascacio-Valdésa, Antonio Francisco Aguilera-Carbób, Arely Pradoc, Raúl Rodríguez-Herreraa, Cristóbal Noé Aguilara,

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cristobal.aguilar@uadec.edu.mx

Corresponding author.

a Food Research Department, School of Chemistry, Universidad Autónoma de Coahuila, 25280 Saltillo, Coahuila, Mexico

b Animal Nutrition Department, Universidad Autónoma Agraria Antonio Narro, 25315, Buenavista, Saltillo, Coahuila, Mexico

c Department of Biotechnology, Departamento de Biotecnología, Universidad Autónoma Metropolitana, 09340 Iztapalapa, Mexico

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          "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">EA accumulation kinetics using&#58; &#40;<span class="elsevierStyleGlyphlozf"></span>&#41; CBP-A-GH1&#59; &#40;&#9632;&#41; CBP-A-HT4&#59; &#40;&#9652;&#41; CBP-A-PSH in SSC&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Polyphenols are a wide range of compounds considered to be secondary metabolites of different plant parts&#58; leaves&#44; stems&#44; flowers&#44; fruits&#44; seeds&#44; and others<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">2</span></a>&#46; Polyphenols are divided into three main groups&#58; complex tannins&#44; condensed tannins and hydrolyzable tannins<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">17</span></a>&#46; Ellagitannins are a class of hydrolyzable tannins&#46; These compounds are essentially formed by a hexahydroxydiphenic acid &#40;HHDP&#41; group linked by an ester bond to a glucose<a class="elsevierStyleCrossRef" href="#bib0185"><span class="elsevierStyleSup">8</span></a>&#46; There are over 500 different structures of ellagitannins reported in the literature<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">13</span></a>&#46; Ellagitannins are mainly obtained from the bark and trunks of trees such as oak &#40;<span class="elsevierStyleItalic">Quercus</span> spp&#46;&#41;<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">18</span></a> and eucalyptus &#40;<span class="elsevierStyleItalic">Eucalyptus</span> spp&#46;&#41;<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">19</span></a>&#46; Ellagitannins are abundant in some red berries<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">24</span></a>&#44; plants of the Mexican desert<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">6</span></a> and pomegranate fruit<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">22</span></a>&#46; Ellagitannins have various beneficial health properties&#46; It has been shown that the ellagitannins present in pomegranate juice can induce apoptosis by activation of the leukemic cell cycle<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">11</span></a>&#46; Punicalagin is an ellagitannin from the pomegranate peel&#44; which has been linked to apoptosis in HT-29 colon cancer cells<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">23</span></a>&#46; Ellagitannins present in leaf extracts&#44; flower extracts&#44; peel&#44; juice and seeds of pomegranate have beneficial effects on the control of obesity&#44; diabetes&#44; cardiovascular disease&#44; hypertension and hypercholesterolemia<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">5</span></a>&#46; Moreover&#44; these polyphenols in pomegranate leaves&#44; obtained by macroporous resin column chromatography have a high antioxidant activity<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">29</span></a>&#46; Ellagitannins can be hydrolyzed by chemical or enzymatic methods to release the HHDP group<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">15</span></a>&#59; this group undergoes a spontaneous molecular arrangement forming a new molecule called ellagic acid &#40;EA&#41;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">3</span></a>&#46; EA is a secondary metabolite of high industrial interest due to various beneficial effect on human health such as antiviral<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">16</span></a>&#44; anticarcinogenic<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">20</span></a>&#44; antioxidant<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">26</span></a>&#44; and anti-inflammatory activities<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">10</span></a>&#46; Industrially&#44; EA is obtained with the use of chemicals&#44; involving high production costs and recovery as well as environmental damage&#46; Therefore&#44; it is necessary to develop methods for the biotechnological production of secondary metabolites&#46; There are few studies about obtaining EA by bioprocessing agroindustrial residues such as pomegranate peel and microorganisms that are capable of degrading the ellagitannin compounds present in the waste by solid-state culture &#40;SSC&#41; to generate EA<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">25</span></a>&#46; The aim of this work was to evaluate the effect of different polyphenol sources&#58; cranberry &#40;CP&#41;&#44; creosote bush &#40;CBP&#41; and pomegranate &#40;PP&#41; on the hydrolytic efficiency of three different xerophilic <span class="elsevierStyleItalic">Aspergillus niger</span> strains&#44; denominated A-GH1&#44; A-PSH and A-HT4&#44; to obtain EA by SSC&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Materials and methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Polyphenol extraction and purification</span><p id="par0010" class="elsevierStylePara elsevierViewall">Cranberries &#40;<span class="elsevierStyleItalic">Vaccinium macrocarpon</span> Ait&#46;&#41; were originally from Wisconsin&#44; USA&#44; and were received in vacuum packed bags &#40;350<span class="elsevierStyleHsp" style=""></span>g&#41; in the month of January of the year 2012&#46; Pomegranates &#40;<span class="elsevierStyleItalic">Punica granatum</span> L&#46; var&#46; Wonderful&#41; were originally from California&#44; USA&#44; and were received in cardboard boxes &#40;25<span class="elsevierStyleHsp" style=""></span>kg&#41;&#44; in the same session and year&#46; These fruits were purchased at a supermarket in Saltillo&#44; Coahuila&#44; Mexico&#46; Creosote bush plants &#40;<span class="elsevierStyleItalic">Larrea tridentate</span> Sesse &#38; Mocino ex DC&#46; Coville&#41; were manually collected in Federal Highway 57 along 15<span class="elsevierStyleHsp" style=""></span>km of the Saltillo-Monclova stretch&#44; in Coahuila State&#44; Mexico in the second semester of the year 2011&#46; Pomegranate peel&#44; cranberry and creosote bush leaves were dehydrated at 60<span class="elsevierStyleHsp" style=""></span>&#176;C for 48<span class="elsevierStyleHsp" style=""></span>h&#44; then pulverized in a grinder &#40;PULVEX<span class="elsevierStyleSup">&#174;</span> Mini 100&#41; to obtain a particle size of 600<span class="elsevierStyleHsp" style=""></span>&#956;m and taken to constant weight<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">25</span></a>&#46; Polyphenols were extracted according to the methodology proposed by Ascacio-Vald&#233;s et al<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">6</span></a><span class="elsevierStyleItalic">&#46;</span> Substrate was hydrated at 1&#58;5 ratio &#40;100<span class="elsevierStyleHsp" style=""></span>g substrate&#47;500<span class="elsevierStyleHsp" style=""></span>ml distilled water&#41; and incubated at 60<span class="elsevierStyleHsp" style=""></span>&#176;C for 30<span class="elsevierStyleHsp" style=""></span>min&#46; The substrate mass was filtered through muslin cloth and the extract obtained was centrifuged at 3000<span class="elsevierStyleHsp" style=""></span>rpm for 15<span class="elsevierStyleHsp" style=""></span>min&#46; The supernatant was purified by chromatography &#40;Amberlite XAD-resin 16<span class="elsevierStyleSup">&#174;</span>&#41;&#46; The extracts were eluted with distilled water &#40;dH<span class="elsevierStyleInf">2</span>O&#41; to remove soluble compounds&#46; The polyphenolic compound-rich fraction was eluted with 96<span class="elsevierStyleHsp" style=""></span>&#37; ethanol&#46; Finally&#44; the ethanol was evaporated in a heating oven &#40;NAPCO<span class="elsevierStyleSup">&#174;</span> Model 322&#41; at 60<span class="elsevierStyleHsp" style=""></span>&#176;C for 24<span class="elsevierStyleHsp" style=""></span>h&#46; The CP CBB and PP were obtained as a fine powder&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Support preparation</span><p id="par0015" class="elsevierStylePara elsevierViewall">The use of polyurethane foam &#40;PUF&#41; as inert support for polyphenol biodegradation was assessed&#46; The PUF was cut and ground to a particle size of 0&#46;85<span class="elsevierStyleHsp" style=""></span>mm&#44; then washed &#40;3&#215;&#41; with hot water &#40;80&#8211;90<span class="elsevierStyleHsp" style=""></span>&#176;C&#41; for 10<span class="elsevierStyleHsp" style=""></span>min&#44; filtered to eliminate and dried until constant weight<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">21</span></a>&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Microorganisms and culture media</span><p id="par0020" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">A&#46; niger</span> GH1&#44; <span class="elsevierStyleItalic">A&#46; niger</span> PSH and <span class="elsevierStyleItalic">A&#46; niger</span> HT4 strains were supplied by DIA-UAdeC &#40;Departamento de Investigaci&#243;n en Alimentos&#44; Universidad Aut&#243;noma de Coahuila&#41;&#46; These strains have the ability to degrade substrates rich in polyphenols<a class="elsevierStyleCrossRefs" href="#bib0160"><span class="elsevierStyleSup">3&#44;12&#44;22</span></a>&#46; The strains were activated in potato dextrose agar &#40;PDA-Bioxon&#41;&#44; and incubated at 30<span class="elsevierStyleHsp" style=""></span>&#176;C for 5 days&#46; Spores were harvested with 0&#46;01<span class="elsevierStyleHsp" style=""></span>&#37; Tween-80 and counted in a Neubauer<span class="elsevierStyleSup">&#174;</span> chamber&#46; Pontecorvo culture medium having the following composition &#40;g&#47;l&#41;&#58; NaNO<span class="elsevierStyleInf">3</span> 6&#46;0&#44; KH<span class="elsevierStyleInf">2</span>PO<span class="elsevierStyleInf">4</span> 1&#46;52&#44; KCl 0&#46;52 MgSO<span class="elsevierStyleInf">4</span>&#183;7H<span class="elsevierStyleInf">2</span>O 0&#46;52&#44; ZnSO<span class="elsevierStyleInf">4</span> 0&#46;001&#44; FeCl 0&#46;85 and 1<span class="elsevierStyleHsp" style=""></span>ml trace metals was used&#46; The trace metal solution contained &#40;mg&#47;l&#41; Na<span class="elsevierStyleInf">2</span>B<span class="elsevierStyleInf">4</span>O<span class="elsevierStyleInf">7</span>&#183;10H<span class="elsevierStyleInf">2</span>O 10&#44; MnCl<span class="elsevierStyleInf">2</span>&#183;4H<span class="elsevierStyleInf">2</span>O 50&#44; Na<span class="elsevierStyleInf">2</span>MoO<span class="elsevierStyleInf">4</span>&#183;2H<span class="elsevierStyleInf">2</span>O 50 and CuSO<span class="elsevierStyleInf">4</span>&#183;5H<span class="elsevierStyleInf">2</span>O 250&#46; The carbon source &#40;30<span class="elsevierStyleHsp" style=""></span>g&#47;l&#41; was supplemented with either CP&#44; CBP or PP<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">7</span></a> and the initial culture medium pH was adjusted to 6&#46;5 with 1<span class="elsevierStyleHsp" style=""></span>M NaOH&#46; An inoculum size of 2<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">7</span> spores per g of culture material was used&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">SSC conditions</span><p id="par0025" class="elsevierStylePara elsevierViewall">The SSC was prepared as follows&#58; 0&#46;5<span class="elsevierStyleHsp" style=""></span>g of PUF was homogenized with 1&#46;16<span class="elsevierStyleHsp" style=""></span>ml of culture medium &#40;70<span class="elsevierStyleHsp" style=""></span>&#37; humidity&#41; and packed in columns &#40;0&#46;5<span class="elsevierStyleHsp" style=""></span>cm<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>5<span class="elsevierStyleHsp" style=""></span>cm&#41; at a packing density of 0&#46;08<span class="elsevierStyleHsp" style=""></span>g&#47;cm<span class="elsevierStyleSup">3</span>&#46; The solid-state culture was performed for 32<span class="elsevierStyleHsp" style=""></span>h at 30<span class="elsevierStyleHsp" style=""></span>&#176;C&#44; with sampling every 8<span class="elsevierStyleHsp" style=""></span>h &#40;two columns by treatment&#41;<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">9</span></a>&#46; The enzymatic extract of the culture was obtained by adding 1&#46;16<span class="elsevierStyleHsp" style=""></span>ml of 50<span class="elsevierStyleHsp" style=""></span>mM citrate buffer &#40;pH 5&#41; within each column&#44; the mass culture was mixed and the extract was obtained by manual pressing&#46; To recover the EA&#44; an ethanol&#8211;formic acid &#40;1&#46;16<span class="elsevierStyleHsp" style=""></span>ml of 0&#46;01<span class="elsevierStyleHsp" style=""></span>&#37;&#41; solution was added<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">25</span></a> and the extracts obtained were filtered &#40;0&#46;45<span class="elsevierStyleHsp" style=""></span>&#956;m&#41; and frozen until analysis&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Ellagitannase activity assay</span><p id="par0030" class="elsevierStylePara elsevierViewall">Ellagitannase activity was carried out according to the methodology suggested by De la Cruz et al<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">12</span></a><span class="elsevierStyleItalic">&#46;</span> Ellagitannins 1<span class="elsevierStyleHsp" style=""></span>mg&#47;ml in 50<span class="elsevierStyleHsp" style=""></span>mM citrate buffers&#44; pH 5&#44; were used as enzyme substrate&#46; A substrate control &#40;1<span class="elsevierStyleHsp" style=""></span>ml ellagitannins and 50<span class="elsevierStyleHsp" style=""></span>&#956;l of 50<span class="elsevierStyleHsp" style=""></span>mM citrate buffers&#44; pH 5&#41;&#44; enzyme control &#40;1<span class="elsevierStyleHsp" style=""></span>ml of 50<span class="elsevierStyleHsp" style=""></span>mM citrate buffers&#44; pH 5 and 50<span class="elsevierStyleHsp" style=""></span>&#956;l of enzymatic extract&#41; and the reaction mixture &#40;1<span class="elsevierStyleHsp" style=""></span>ml of ellagitannins and 50<span class="elsevierStyleHsp" style=""></span>&#956;l of enzymatic extract&#41; were prepared&#46; The reaction was done in a water bath for 10<span class="elsevierStyleHsp" style=""></span>min at 60<span class="elsevierStyleHsp" style=""></span>&#176;C&#46; The reaction was stopped by adding 1050<span class="elsevierStyleHsp" style=""></span>&#956;l of absolute ethanol&#46; Then&#44; samples were sonicated for 25<span class="elsevierStyleHsp" style=""></span>min&#44; filtered through 0&#46;45<span class="elsevierStyleHsp" style=""></span>&#956;m nylon membrane and collected in vials&#46; One ellagitannase enzymatic unit was defined as the enzyme amount needed to release 1<span class="elsevierStyleHsp" style=""></span>&#956;mol of EA per min&#44; under the conditions described&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">HPLC analysis</span><p id="par0035" class="elsevierStylePara elsevierViewall">Quantification of EA was performed on a Varian ProStar model 2301 HPLC&#46; A column Pursuit XRs 5um C18 &#40;150<span class="elsevierStyleHsp" style=""></span>mm<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>46<span class="elsevierStyleHsp" style=""></span>mm&#41; and&#44; &#40;A&#41; methanol &#40;washing phase&#41;&#44; &#40;B&#41; acetonitrile and &#40;C&#41; acetic acid 3<span class="elsevierStyleHsp" style=""></span>&#37; &#40;mobile phase&#41;&#46; The flow rate was 1<span class="elsevierStyleHsp" style=""></span>ml&#47;min&#44; at a column temperature of 30<span class="elsevierStyleHsp" style=""></span>&#176;C&#46; Standard curve of EA &#40;&#8805;95<span class="elsevierStyleHsp" style=""></span>&#37;&#44; Sigma&#8211;Aldrich<span class="elsevierStyleSup">&#174;</span>&#41; from 0 to 500<span class="elsevierStyleHsp" style=""></span>&#956;g&#47;ml was prepared<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">7</span></a>&#46;</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Data analysis</span><p id="par0040" class="elsevierStylePara elsevierViewall">The effect of the different polyphenol sources and strains on EA accumulation was assessed under a 3<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>3 factorial design with two replicates&#46; Data were analyzed by ANOVA using SAS 9&#46;0 and means were compared by Tukey&#39;s multiple range procedure &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#8804;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41; when needed&#46;</p></span></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Results</span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Kinetics of EA accumulation</span><p id="par0045" class="elsevierStylePara elsevierViewall">Culture kinetics of A-GH1&#44; A-PSH and A-HT4 strains and three culture media enriched with CP&#44; CBP and PP were studied&#46; The kinetic profile when using CP as polyphenolic substrate &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41; showed the highest EA accumulation &#40;74&#46;56<span class="elsevierStyleHsp" style=""></span>mg&#47;g&#41; with the A-PSH strain at 8<span class="elsevierStyleHsp" style=""></span>h of culture followed by the A-HT4 strain &#40;69&#46;55<span class="elsevierStyleHsp" style=""></span>mg&#47;g&#41; at 32<span class="elsevierStyleHsp" style=""></span>h of culture and A-GH1 &#40;64&#46;35<span class="elsevierStyleHsp" style=""></span>mg&#47;g&#41; at 32<span class="elsevierStyleHsp" style=""></span>h of culture&#46; The A-HT4 strain produced 13&#46;69<span class="elsevierStyleHsp" style=""></span>&#37; more EA than the A-GH1 strain&#59; however the former strain also required a 4-fold increase in the culture time required by the A-GH1 strain&#46; Therefore&#44; in terms of process time&#44; A-GH1 resulted in higher EA accumulation than A-HT4&#46; <a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a> shows the EA accumulation profile when using CBP&#46; Total EA accumulation by the different strains was 182&#46;92&#44; 158&#46;54 and 125&#46;97<span class="elsevierStyleHsp" style=""></span>mg&#47;g using A-GH1&#44; A-HT4 and A-PSH strains respectively&#59; however&#44; A-HT4 reached 158&#46;54<span class="elsevierStyleHsp" style=""></span>mg&#47;g in an 8<span class="elsevierStyleHsp" style=""></span>h culture while A-GH1 reached in 32<span class="elsevierStyleHsp" style=""></span>h culture&#46; Once again&#44; a lower EA accumulation value &#40;158&#46;54<span class="elsevierStyleHsp" style=""></span>mg&#47;g&#41; could be observed in one of the strains tested &#40;A-HT4&#41; but a culture time 4 times lower than in strain A-GH1 that showed the highest EA accumulation &#40;182&#46;92<span class="elsevierStyleHsp" style=""></span>mg&#47;g&#41;&#46; In contrast&#44; when using PP as substrate&#44; EA accumulation was 163&#46;03&#44; 350&#46;21 and 200&#46;33<span class="elsevierStyleHsp" style=""></span>mg&#47;g for A-GH1 &#40;8<span class="elsevierStyleHsp" style=""></span>h culture&#41;&#44; A-HT4 &#40;16<span class="elsevierStyleHsp" style=""></span>h of culture&#41; and A-PSH &#40;16<span class="elsevierStyleHsp" style=""></span>h culture&#41; respectively&#59; the highest EA accumulation occurred at 16<span class="elsevierStyleHsp" style=""></span>h of culture when using A-HT4 and no EA increase was observed at any other time &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia><elsevierMultimedia ident="fig0015"></elsevierMultimedia></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Ellagitannase activity and productivity</span><p id="par0050" class="elsevierStylePara elsevierViewall">Ellagitannase activity reached maximum value of 5176&#46;81<span class="elsevierStyleHsp" style=""></span>U&#47;l when using CP as carbon source and A-PSH at 8<span class="elsevierStyleHsp" style=""></span>h of SSC &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>&#41;&#46; Other strains reached maximum values in the first 8<span class="elsevierStyleHsp" style=""></span>h and then these values were kept constant&#46; <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> shows effect of substrates&#44; strains and interaction on ellagitannase activity and EA productivity&#46; EA productivity was defined as the ratio among the maximum accumulation of EA per culture time&#46; In <a class="elsevierStyleCrossRef" href="#fig0025">Fig&#46; 5</a>&#44; the values of EA productivity are displayed at a time of 16<span class="elsevierStyleHsp" style=""></span>h&#44; which corresponds to the time of maximal EA accumulation obtained&#46; In <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#44; the individual effect of each variable&#44; validated by a Tukey test on ellagitannase activity and EA productivity is shown&#46; Then the highest productivity &#40;21&#46;89<span class="elsevierStyleHsp" style=""></span>mg&#47;g&#47;h&#41;&#44; was obtained when using the <span class="elsevierStyleItalic">Aspergillus</span> strain coded as A-HT4 and CP as source&#46; It was observed that when A-HT4 and CP were used&#44; a maximum productivity of 21&#46;89<span class="elsevierStyleHsp" style=""></span>mg&#47;g&#47;h was reached&#46;</p><elsevierMultimedia ident="fig0020"></elsevierMultimedia><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="fig0025"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia></span></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Discussion</span><p id="par0055" class="elsevierStylePara elsevierViewall">The A-PSH strain has been reported to have the ability to produce EA by hydrolysis of the pomegranate peel by SSC<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">22</span></a>&#46; Moreover&#44; this strain also showed the ability to degrade hydrolyzable tannins from extracts of creosote bush &#40;<span class="elsevierStyleItalic">L&#46; tridentata</span>&#41; and tarbush &#40;<span class="elsevierStyleItalic">Flourensia cernua</span>&#41; releasing EA and gallic acid by SSC<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">28</span></a>&#46; Furthermore&#44; the A-GH1 strain has been reported for the hydrolysis of polyphenolic compounds from pomegranate peel&#44; reaching 17<span class="elsevierStyleHsp" style=""></span>mg&#47;g of EA at 32<span class="elsevierStyleHsp" style=""></span>h by SSC<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">4</span></a>&#46; Vattem and Shetty &#40;2003&#41; reported the use of cranberry pomace and <span class="elsevierStyleItalic">Lentinus edodes</span> strain for EA production reaching a maximum accumulation of 350<span class="elsevierStyleHsp" style=""></span>&#956;g&#47;g of EA by dried cranberry pomace and they attributed the EA accumulation to the &#946;-glucosidase enzyme<a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">27</span></a>&#46; In this work&#44; when A-HT4 strain and PP are used&#44; a maximum of 350&#46;21<span class="elsevierStyleHsp" style=""></span>mg&#47;g of EA at 16<span class="elsevierStyleHsp" style=""></span>h is reached&#46; It has also been reported that the pomegranate peel is an excellent carbon source for EA production&#44; using an <span class="elsevierStyleItalic">A&#46; niger</span> strain<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">1</span></a>&#46; Recent studies mention that there is a possible set of enzymes that are responsible for the release of the HHDP group and formation consequence of EA<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">7</span></a>&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">The values of ellagitannase activity obtained in this study are 166-fold higher than those reported by Aguilera-Carb&#243; et al<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">4</span></a>&#46; These authors reported values of 44&#46;5<span class="elsevierStyleHsp" style=""></span>U&#47;l using pomegranate peel as carbon source and A-GH1 at 48<span class="elsevierStyleHsp" style=""></span>h of culture time&#46; Similar studies obtained maximum values of ellagitannase activity &#40;2189&#46;94<span class="elsevierStyleHsp" style=""></span>U&#47;l&#41; at 30<span class="elsevierStyleHsp" style=""></span>h of SSC using PP as carbon source and several fungal strains &#40;<span class="elsevierStyleItalic">A&#46; niger</span> PSH&#44; <span class="elsevierStyleItalic">A&#46; niger</span> GH1&#44; <span class="elsevierStyleItalic">A&#46; niger</span> HT4 and <span class="elsevierStyleItalic">A&#46; niger</span> HC2&#41;<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">12</span></a>&#46; Several enzymes responsible for ellagitannin hydrolysis have been reported&#59; however&#44; the authors found that only ellagitannase&#44; clearly associated with EA accumulation on SSC&#44; reached maximum values &#40;200&#46;04<span class="elsevierStyleHsp" style=""></span>U&#47;l&#41; at 12<span class="elsevierStyleHsp" style=""></span>h of SSC using PP and <span class="elsevierStyleItalic">A&#46; niger</span> GH1 strain<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">7</span></a>&#46; The authors reported that EA production is higher using partially purified polyphenols&#44; since these molecules have a glucose core&#44; making them more susceptible to attack by microbial enzymes<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">14</span></a>&#46; There are a few studies about the use of polyphenols from plants&#44; barks or fruits SSC for obtaining secondary metabolites&#46; The productivity obtained with CP and the A-HT4 strain is higher compared with that in previous reports using valonia tannins as a carbon source&#44; reaching values of 0&#46;92<span class="elsevierStyleHsp" style=""></span>U&#47;l&#47;h<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">11</span></a>&#46; The A-GH1 strain has been associated with the release of EA from creosote bush extracts by SSC&#44; reaching a productivity of 1&#46;22<span class="elsevierStyleHsp" style=""></span>U&#47;l&#47;h<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">4</span></a>&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">In conclusion&#44; it was possible to obtain EA from rich substrates in polyphenolic compounds using <span class="elsevierStyleItalic">A&#46; niger</span> strains in SSC&#46; A-HT4 reached a maximum EA value &#40;350&#46;21<span class="elsevierStyleHsp" style=""></span>mg&#47;g of PP at SSC&#41;&#46; When CP and the A-PSH strain was used&#44; high values of ellagitannase activity &#40;5176&#46;81<span class="elsevierStyleHsp" style=""></span>U&#47;l&#41; were obtained at 8<span class="elsevierStyleHsp" style=""></span>h of SSC&#46; The EA release mechanism is unknown due to EA complexity&#59; however ellagitannase is one of the enzymes that may be responsible for the hydrolysis of the ester link in the HHDP group to generate EA&#46;</p></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Conflict of interest</span><p id="par0070" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span><span id="sec0075" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Ethical disclosures</span><span id="sec0080" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Protection of human and animal subjects</span><p id="par0075" class="elsevierStylePara elsevierViewall">The authors declare that no experiments were performed on humans or animals for this investigation&#46;</p></span><span id="sec0085" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Confidentiality of data</span><p id="par0080" class="elsevierStylePara elsevierViewall">The authors declare that no patient data appears in this article&#46;</p></span><span id="sec0090" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Right to privacy and informed consent</span><p id="par0085" class="elsevierStylePara elsevierViewall">The authors declare that no patient data appears in this article&#46;</p></span></span></span>"
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          "titulo" => "Palabras clave"
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          "identificador" => "sec0005"
          "titulo" => "Introduction"
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        5 => array:3 [
          "identificador" => "sec0010"
          "titulo" => "Materials and methods"
          "secciones" => array:7 [
            0 => array:2 [
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              "titulo" => "Polyphenol extraction and purification"
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              "titulo" => "Support preparation"
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              "titulo" => "Microorganisms and culture media"
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              "titulo" => "SSC conditions"
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              "identificador" => "sec0035"
              "titulo" => "Ellagitannase activity assay"
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              "titulo" => "HPLC analysis"
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          "titulo" => "Results"
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              "identificador" => "sec0055"
              "titulo" => "Kinetics of EA accumulation"
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              "titulo" => "Ellagitannase activity and productivity"
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          "titulo" => "Discussion"
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          "titulo" => "Ethical disclosures"
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              "titulo" => "Protection of human and animal subjects"
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              "titulo" => "Confidentiality of data"
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              "titulo" => "Right to privacy and informed consent"
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          "titulo" => "Acknowledgements"
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        11 => array:1 [
          "titulo" => "References"
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    "fechaRecibido" => "2014-12-07"
    "fechaAceptado" => "2015-08-05"
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          "titulo" => "Keywords"
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          "palabras" => array:4 [
            0 => "Polyphenols"
            1 => "<span class="elsevierStyleItalic">Aspergillus niger</span>"
            2 => "Solid-state culture"
            3 => "Ellagitannase"
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          "palabras" => array:4 [
            0 => "Polifenoles"
            1 => "<span class="elsevierStyleItalic">Aspergillus niger</span>"
            2 => "Cultivo en estado s&#243;lido"
            3 => "Elagitanasa"
          ]
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Fungal hydrolysis of ellagitannins produces hexahydroxydiphenic acid&#44; which is considered an intermediate molecule in ellagic acid release&#46; Ellagic acid has important and desirable beneficial health properties&#46; The aim of this work was to identify the effect of different sources of ellagitannins on the efficiency of ellagic acid release by <span class="elsevierStyleItalic">Aspergillus niger</span>&#46; Three strains of <span class="elsevierStyleItalic">A&#46; niger</span> &#40;GH1&#44; PSH and HT4&#41; were assessed for ellagic acid release from different polyphenol sources&#58; cranberry&#44; creosote bush&#44; and pomegranate used as substrate&#46; Polyurethane foam was used as support for solid-state culture in column reactors&#46; Ellagitannase activity was measured for each of the treatments&#46; Ellagic acid was quantified by high performance liquid chromatography&#46; When pomegranate polyphenols were used&#44; a maximum value of ellagic acid &#40;350&#46;21<span class="elsevierStyleHsp" style=""></span>mg&#47;g&#41; was reached with <span class="elsevierStyleItalic">A&#46; niger</span> HT4 in solid-state culture&#46; The highest amount of ellagitannase &#40;5176&#46;81<span class="elsevierStyleHsp" style=""></span>U&#47;l&#41; was obtained at 8<span class="elsevierStyleHsp" style=""></span>h of culture when cranberry polyphenols and strain <span class="elsevierStyleItalic">A&#46; niger</span> PSH were used&#46; Results demonstrated the effect of different polyphenol sources and <span class="elsevierStyleItalic">A&#46; niger</span> strains on ellagic acid release&#46; It was observed that the best source for releasing ellagic acid was pomegranate polyphenols and <span class="elsevierStyleItalic">A&#46; niger</span> HT4 strain&#44; which has the ability to degrade these compounds for obtaining a potent bioactive molecule such as ellagic acid&#46;</p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">La hidr&#243;lisis f&#250;ngica de los elagitaninos produce &#225;cido hexahidroxidif&#233;nico&#44; considerado como una mol&#233;cula intermedia en la liberaci&#243;n de &#225;cido el&#225;gico&#46; El &#225;cido el&#225;gico tiene importantes y deseables propiedades ben&#233;ficas para la salud humana&#46; El objetivo de este trabajo fue identificar el efecto de la fuente de elagitaninos sobre la eficiente liberaci&#243;n de &#225;cido el&#225;gico por <span class="elsevierStyleItalic">Aspergillus niger</span>&#46; La liberaci&#243;n de &#225;cido el&#225;gico se realiz&#243; con tres cepas de <span class="elsevierStyleItalic">A&#46; niger</span> &#40;GH1&#44; PSH y HT4&#41; en presencia de diferentes fuentes de polifenoles &#40;ar&#225;ndano&#44; gobernadora y granada&#41;&#44; usadas como sustrato&#46; Se emple&#243; espuma de poliuretano como soporte para el cultivo en estado s&#243;lido en reactores en columna&#46; Se midi&#243; la actividad elagitanasa a cada uno de los tratamientos&#46; El &#225;cido el&#225;gico liberado se cuantific&#243; por cromatograf&#237;a l&#237;quida de alta resoluci&#243;n&#46; Cuando se utilizaron los polifenoles de granada&#44; se alcanz&#243; un valor m&#225;ximo de 350&#44;21<span class="elsevierStyleHsp" style=""></span>mg&#47;g de &#225;cido el&#225;gico con <span class="elsevierStyleItalic">A&#46; niger</span> HT4 en cultivo en estado s&#243;lido&#46; La mayor actividad elagitanasa &#40;5176&#46;81 U&#47;l&#41; se obtuvo a 8 h de cultivo cuando se usaron los polifenoles de ar&#225;ndano como sustrato y <span class="elsevierStyleItalic">A&#46; niger</span> PSH&#46; Los resultados demostraron el efecto que tiene la fuente de polifenoles y la cepa de <span class="elsevierStyleItalic">A&#46; niger</span> en la liberaci&#243;n de &#225;cido el&#225;gico&#46; Se observ&#243; que la mejor fuente para la liberaci&#243;n de &#225;cido el&#225;gico fueron los polifenoles de granada y que la cepa <span class="elsevierStyleItalic">A&#46; niger</span> HT4 posee la habilidad de degradar estos compuestos para la obtenci&#243;n de potentes mol&#233;culas bioactivas&#44; como el &#225;cido el&#225;gico&#46;</p></span>"
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          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">EA accumulation kinetics using&#58; &#40;<span class="elsevierStyleGlyphlozf"></span>&#41; CP-A-GH1&#59; &#40;&#9632;&#41; CP-A-HT4&#59; &#40;&#9652;&#41; CP-A-PSH in SSC&#46;</p>"
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          "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">EA accumulation kinetics using&#58; &#40;<span class="elsevierStyleGlyphlozf"></span>&#41; PP-A-GH1&#59; &#40;&#9632;&#41; PP-A-HT4&#59; &#40;&#9652;&#41; PP-A-PSH in SSC&#46;</p>"
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          "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Values of ellagitannase activity&#44; &#40;<span class="elsevierStyleGlyphlozf"></span>&#41; CP-A-GH1&#59; &#40;&#9632;&#41; CP-A-HT4&#59; &#40;&#9652;&#41; CP-A-PSH&#59; &#40;X&#41; CBP-A-GH1&#59; &#40;&#42;&#41; CBP-A-HT4&#59; &#40;&#9679;&#41; CBP-A-PSH&#59; &#40;&#124;&#41; PP-A-GH1&#58; &#40;--&#41; PP-A-HT4&#59; &#40;&#8211; -&#41; PP-A-PSH&#46;</p>"
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          "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">EA productivity&#44; &#40;<elsevierMultimedia ident="201603250029258521"></elsevierMultimedia>&#41; CP-A-GH1&#59; CP-A-HT4&#59; CP-A-PSH&#59; &#40;<elsevierMultimedia ident="201603250029258522"></elsevierMultimedia>&#41; CBP-A-GH1&#59; CBP-A-HT4&#59; CBP-A-PSH&#59; &#40;<elsevierMultimedia ident="201603250029258523"></elsevierMultimedia>&#41; PP-A-GH1&#59; PP-A-HT4&#59; PP-A-PSH&#46;</p>"
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          "leyenda" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">S</span><span class="elsevierStyleHsp" style=""></span>&#42;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">X</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>combined effect of substrate and strains&#46;</p>"
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                  <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">Responses&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;98&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;00&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1252&#46;51&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">487&#46;89&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">S</span><span class="elsevierStyleHsp" style=""></span>&#42;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">X</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">382&#46;99&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#60;&#46;0001&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">262&#46;52&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Replicate&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">17<span class="elsevierStyleHsp" style=""></span>034&#46;93&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;26&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;50&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">S</span><a class="elsevierStyleCrossRef" href="#tblfn0015"><span class="elsevierStyleSup">c</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&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">43<span class="elsevierStyleHsp" style=""></span>399&#46;04&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&#46;82&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">X</span><a class="elsevierStyleCrossRef" href="#tblfn0020"><span class="elsevierStyleSup">d</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&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">230<span class="elsevierStyleHsp" style=""></span>928&#46;25&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#60;&#46;0001&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">20&#46;32&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">S</span><span class="elsevierStyleHsp" style=""></span>&#42;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">X</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">112<span class="elsevierStyleHsp" style=""></span>108&#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">&#60;&#46;0001&nbsp;\t\t\t\t\t\t\n
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          "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Analysis of variance for EA productivity and ellagitannase activity</p>"
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          "leyenda" => "<p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Means with the same letter&#44; in the same column&#44; are not significantly different according to the Tukey&#39;s multiple range test &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#46;</p>"
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                  <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">Substrate&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Ellagitannase activity &#40;U&#47;l&#41;&nbsp;\t\t\t\t\t\t\n
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                  """
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Article information

ISSN: 03257541
Original language: English

DOI:10.1016/j.ram.2015.08.008

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Year/Month	Html	Pdf	Total

2024 October	15	2	17
2024 September	28	2	30
2024 August	35	3	38
2024 July	21	3	24
2024 June	19	6	25
2024 May	21	8	29
2024 April	19	4	23
2024 March	18	4	22
2024 February	22	6	28
2024 January	12	7	19
2023 December	13	9	22
2023 November	24	8	32
2023 October	21	8	29
2023 September	20	2	22
2023 August	20	3	23
2023 July	19	5	24
2023 June	23	4	27
2023 May	17	8	25
2023 April	13	0	13
2023 March	12	4	16
2023 February	19	7	26
2023 January	16	8	24
2022 December	22	20	42
2022 November	24	16	40
2022 October	20	8	28
2022 September	28	8	36
2022 August	32	13	45
2022 July	28	14	42
2022 June	32	11	43
2022 May	36	11	47
2022 April	27	9	36
2022 March	37	16	53
2022 February	46	7	53
2022 January	32	3	35
2021 December	46	14	60
2021 November	19	14	33
2021 October	23	8	31
2021 September	24	15	39
2021 August	40	12	52
2021 July	23	14	37
2021 June	29	12	41
2021 May	35	10	45
2021 April	45	17	62
2021 March	41	8	49
2021 February	53	6	59
2021 January	42	13	55
2020 December	46	10	56
2020 November	39	11	50
2020 October	32	7	39
2020 September	26	10	36
2020 August	23	8	31
2020 July	36	8	44
2020 June	33	10	43
2020 May	30	6	36
2020 April	26	5	31
2020 March	45	11	56
2020 February	49	7	56
2020 January	25	7	32
2019 December	24	10	34
2019 November	41	4	45
2019 October	30	5	35
2019 September	49	17	66
2019 August	18	4	22
2019 July	33	11	44
2019 June	29	22	51
2019 May	68	42	110
2019 April	31	16	47
2019 March	17	9	26
2019 February	11	16	27
2019 January	13	6	19
2018 December	20	5	25
2018 November	32	10	42
2018 October	13	6	19
2018 September	21	7	28
2018 August	15	10	25
2018 July	7	0	7
2018 June	7	2	9
2018 May	4	10	14
2018 April	5	0	5
2018 March	5	1	6
2018 February	3	1	4
2018 January	3	1	4
2017 December	9	2	11
2017 November	12	5	17
2017 October	9	2	11
2017 September	11	12	23
2017 August	10	4	14
2017 July	12	20	32
2017 June	27	13	40
2017 May	23	4	27
2017 April	20	9	29
2017 March	18	53	71
2017 February	15	17	32
2017 January	20	7	27
2016 December	32	5	37
2016 November	25	9	34
2016 October	28	11	39
2016 September	27	8	35
2016 August	27	13	40
2016 July	41	6	47
2016 June	58	29	87
2016 May	58	29	87
2016 April	38	26	64
2016 March	2	1	3

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