Streptomyces globosus DK15 and Streptomyces ederensis ST13 as new producers of factumycin and tetrangomycin antibiotics

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Lanes: 1: 1kb DNA ladder; 2–4: Lactobacillus ghanensis profile (2-MspI, 3-HaeIII, 4-HinfI); 5–7: Enterococcus faecium profile (5-MspI, 6-HaeIII, 7-HinfI); 8–10: Weisella cibaria profile (8-MspI, 9-HaeIII, 10-HinfI); 11–13: Lactococcus garvieae profile (11-MspI, 12-HaeIII, 13-HinfI);14–16: Lactobacillus lactis profile (14-MspI, 15-HaeIII, 16-HinfI); 17–19: Leuconostoc mesenteroides profile (17-MspI, 18-HaeIII, 19-HinfI)." ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Fernanda Corrêa Leal Penido, Fernanda Barbosa Piló, Sávio Henrique de Cicco Sandes, Álvaro Cantini Nunes, Gecernir Colen, Evelyn de Souza Oliveira, Carlos Augusto Rosa, Inayara Cristina Alves Lacerda" "autores" => array:8 [ 0 => array:2 [ "nombre" => "Fernanda Corrêa Leal" "apellidos" => "Penido" ] 1 => array:2 [ "nombre" => "Fernanda Barbosa" "apellidos" => "Piló" ] 2 => array:2 [ "nombre" => "Sávio Henrique de Cicco" "apellidos" => "Sandes" ] 3 => array:2 [ "nombre" => "Álvaro Cantini" "apellidos" => "Nunes" ] 4 => array:2 [ "nombre" => "Gecernir" "apellidos" => "Colen" ] 5 => array:2 [ "nombre" => "Evelyn de Souza" "apellidos" => "Oliveira" ] 6 => array:2 [ "nombre" => "Carlos Augusto" "apellidos" => "Rosa" ] 7 => array:2 [ "nombre" => "Inayara Cristina Alves" "apellidos" => "Lacerda" ] ] ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1517838217304859?idApp=UINPBA00004N" "url" => "/15178382/0000004900000004/v1_201810050636/S1517838217304859/v1_201810050636/en/main.assets" ] "itemAnterior" => array:19 [ "pii" => "S1517838217306573" "issn" => "15178382" "doi" => "10.1016/j.bjm.2018.01.002" "estado" => "S300" "fechaPublicacion" => "2018-10-01" "aid" => "359" "copyright" => "Sociedade Brasileira de Microbiologia" "documento" => "article" "crossmark" => 1 "licencia" => "http://creativecommons.org/licenses/by-nc-nd/4.0/" "subdocumento" => "fla" "cita" => "Braz J Microbiol. 2018;49:808-15" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:2 [ "total" => 622 "formatos" => array:3 [ "EPUB" => 94 "HTML" => 299 "PDF" => 229 ] ] "en" => array:12 [ "idiomaDefecto" => true "cabecera" => "Biotechnology and Industrial Microbiology" "titulo" => "Saccharomyces cerevisiae populations and other yeasts associated with indigenous beers (chicha) of Ecuador" "tienePdf" => "en" "tieneTextoCompleto" => "en" "tieneResumen" => "en" "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "808" "paginaFinal" => "815" ] ] "contieneResumen" => array:1 [ "en" => true ] "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1615 "Ancho" => 1667 "Tamanyo" => 315148 ] ] "descripcion" => array:1 [ "en" => "Chicha de jora (A); Morocho (white maize) (B); Chicha de morocho ready to drink (C); seven-grain chicha (D); cassava for chicha de yuca production (E); Chicha de yuca ready to drink after addition of seeds of the Ungurahua palm (F)." ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Fernanda Barbosa Piló, Enrique Javier Carvajal-Barriga, Maria Cristina Guamán-Burneo, Patricia Portero-Barahona, Arthur Matoso Morato Dias, Larissa Falabella Daher de Freitas, Fátima de Cássia Oliveira Gomes, Carlos Augusto Rosa" "autores" => array:8 [ 0 => array:2 [ "nombre" => "Fernanda Barbosa" "apellidos" => "Piló" ] 1 => array:2 [ "nombre" => "Enrique Javier" "apellidos" => "Carvajal-Barriga" ] 2 => array:2 [ "nombre" => "Maria Cristina" "apellidos" => "Guamán-Burneo" ] 3 => array:2 [ "nombre" => "Patricia" "apellidos" => "Portero-Barahona" ] 4 => array:2 [ "nombre" => "Arthur Matoso Morato" "apellidos" => "Dias" ] 5 => array:2 [ "nombre" => "Larissa Falabella Daher de" "apellidos" => "Freitas" ] 6 => array:2 [ "nombre" => "Fátima de Cássia Oliveira" "apellidos" => "Gomes" ] 7 => array:2 [ "nombre" => "Carlos Augusto" "apellidos" => "Rosa" ] ] ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1517838217306573?idApp=UINPBA00004N" "url" => "/15178382/0000004900000004/v1_201810050636/S1517838217306573/v1_201810050636/en/main.assets" ] "en" => array:21 [ "idiomaDefecto" => true "cabecera" => "Biotechnology and Industrial Microbiology" "titulo" => "Streptomyces globosus DK15 and Streptomyces ederensis ST13 as new producers of factumycin and tetrangomycin antibiotics" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "816" "paginaFinal" => "822" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Ivana Charousová, Juraj Medo, Lukáš Hleba, Soňa Javoreková" "autores" => array:4 [ 0 => array:4 [ "nombre" => "Ivana" "apellidos" => "Charousová" "email" => array:1 [ 0 => "ivanacharousova@gmail.com" ] "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] 1 => array:2 [ "nombre" => "Juraj" "apellidos" => "Medo" ] 2 => array:2 [ "nombre" => "Lukáš" "apellidos" => "Hleba" ] 3 => array:2 [ "nombre" => "Soňa" "apellidos" => "Javoreková" ] ] "afiliaciones" => array:1 [ 0 => array:2 [ "entidad" => "Slovak University of Agriculture in Nitra, Faculty of Biotechnology and Food Sciences, Department of Microbiology, Tr. A. Hlinku 2, 949 76, Nitra, Slovak Republic" "identificador" => "aff0005" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author. Tel.: +421 91702930812." ] ] ] ] "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" => 2173 "Ancho" => 3004 "Tamanyo" => 309351 ] ] "descripcion" => array:1 [ "en" => "Fractionation RP-HPLC chromatogram of factumycin, UV spectrum of factumycin with the max. at 364nm, and ESI-HRMS spectrum, showing the prominent ion clusters for [M+H]+ at m/z 743.4268." ] ] ] "presentadoPor" => "Presented by Dr. Solange I. Mussatto" "textoCompleto" => "IntroductionSince people started suffering from diseases caused by infectious microorganisms, the quest for their remedies led to the discovery of a large number of antibiotics from microorganisms.<a class="elsevierStyleCrossRef" href="#bib0185">1</a> Most of the research was dedicated to study the polyketide bioactive compounds.<a class="elsevierStyleCrossRef" href="#bib0190">2</a> One of the most important and well acknowledged group of the prolific producers of polyketide antibiotics are the actinomycetes, mainly terrestrial representatives of the genus Streptomyces.<a class="elsevierStyleCrossRef" href="#bib0195">3</a> Polyketides have played an important role in the antibiotic drug discovery with most antibacterial drugs being derived from a natural product or natural product lead.<a class="elsevierStyleCrossRef" href="#bib0200">4</a> Examples of natural products with the polyketide structure include the tetrangomycin and factumycin. Tetrangomycins belong to the group of polyketide angucyclinones, naturally occurring benzaanthraquinones that had been isolated from Streptomyces rimosus and Streptomyces griseus.<a class="elsevierStyleCrossRefs" href="#bib0205">5–8</a> Angucyclinones, benz[a]anthraquinone derivatives isolated from Streptomyces spp. have attracted much attention due to their broad and strong biological activities, mainly antiviral, antifungal, and antitumor.<a class="elsevierStyleCrossRefs" href="#bib0205">5,9–10</a> Immunosuppressive function of tetrangomycin by reducing the transcription of cytokine genes and the inhibitory activity of tetrangomycin against methicilin resistant Staphylococus aureus (MRSA) was described by Özakin et al.<a class="elsevierStyleCrossRef" href="#bib0235">11</a> Factumycin is a linear polyketide elfamycin compound and had been isolated from Streptomyces lavendulae and Streptomyces griseus.<a class="elsevierStyleCrossRefs" href="#bib0240">12–14</a> According to Thaker et al.<a class="elsevierStyleCrossRef" href="#bib0255">15</a> a screen of factumycin in combination with known antibiotics revealed unexpected synergy with tetracyclines, offering a possible new application of factumycin as a lead in Gram-negative targeted antibiotic combination therapy. Identification of factumycin antibiotic has high importance, because Gram - negative pathogens are becoming increasingly antibiotic resistant and consequently a serious clinical challenge.<a class="elsevierStyleCrossRef" href="#bib0255">15</a>Therefore, an attempt has been made to isolate the antibiotic-producing actinomycetes with emphasis on the selection and the detailed identification of Streptomyces polyketide-producers.Material and methodsSoil samples and isolation of actinomycetesActinomycetes were isolated by the dilution agar plating method from the forest soils located in Vietnam, Phu Quoc National Park (10°09¿33.49“S 103°59¿07.02”V) and in Sardinia, Foresta di Monte Pisanu (40°25′30.24“S 8°58′34.72″V). An aliquot of 0.1ml of solution was taken and spread over the surface of starch-casein medium.<a class="elsevierStyleCrossRef" href="#bib0260">16</a> Plates were incubated at 30°C and monitored after 7 days. The selected strains were maintained by cultivation on the ISP2 medium<a class="elsevierStyleCrossRef" href="#bib0265">17</a>, incubated at 30°C for 10 days and stored at – 20°C in the presence of glycerol (30% v/v). For all acquired actinomycete isolates, 16S rRNA sequences as well as microscopic (shape of spore chains) and macroscopic morphology (colors of aerial and substrate mycelium, soluble pigments and melanin) were studied in accordance with the guidelines established by the International Streptomycete Project.<a class="elsevierStyleCrossRef" href="#bib0265">17</a>Screening for antimicrobial activityThe morphologically different actinomycete isolates were screened against four Gram - positive bacteria [Bacillus subtilis (DSM 10), Micrococcus luteus (DSM1790), Staphylococcus aureus (Newman), Mycobacterium smegmatis (ATCC 700084)], four Gram - negative bacteria [Escherichia coli (DSM 1116), Escherichia coli (TolC), Pseudomonas aeruginosa (PA14), Chromobacterium violaceum (DSM 30191)], two yeasts [Candida albicans (DSM 1665), Pichia anomala (DSM 6766)] and one filamentous microscopic fungus Mucor hiemalis (DSM 2656) obtained from DSMZ (German Collection of Microorganisms and Cell Cultures), Braunschweig, Germany and ATCC (American Type Culture Collection), Manassas, VA 20110, USA. Raw extracts were prepared from 20ml of 5 day old liquid culture using ethyl acetate (Sigma-Aldrich, USA) according to Wink (2014). Ethylacetate was evaporated and extract was dissolved in 1ml of ethylacetate: acetone: methanol (1:1:1) solution. Detection of biological activity was carried out by preparing 4 - 6h cultures of indicator bacteria followed by dilution with Mueller- Hinton (MH) broth (Merck, Germany) and yeast and fungi by dilution with Mycosel broth<a class="elsevierStyleCrossRef" href="#bib0270">18</a> to obtain 0.01 McFarland turbidity. The antimicrobial activity of streptomycetes was performed by using the broth micro - dilution method <a class="elsevierStyleCrossRef" href="#bib0275">19</a> in 96 - well microplates (BRAND, Germany). The dose in well A corresponds to the extract made from 1.33ml Streptomyces liquid culture per 1ml of the inoculated broth. Concentration decreased 2 fold in wells B-H. The readings were made after 24h of incubation through visual observation of the growth.HPLC and LC/MS analysis of selected crude extractsThe most active raw extracts were selected for the fractionation by liquid - chromatography (Agilent 1100) equipment. The wavelength monitoring was performed at 210 and 360nm. Sample (5μl) was injected onto a HPLC column (X-Bridge 3.5μm, 2.1x100mm; Waters, Milford, USA). Separation was performed using the buffers A2: 950ml H2O, 50ml acetonitrile + 0.05mM (385mg.l-1) ammonium acetate + 40μl acetic acid; B2: 50ml H2O, 950ml acetonitrile, 0.05mM (385mg.l-1) ammonium acetate + 40μl acetic acid and a DAD detector (200-400nm). Fractions (0.15ml) from the HPLC column were collected in a 96 well plates every 0.5min and dried with heated nitrogen in MiniVap (Porvair Sciences, UK) for 45-60min at 40°C. Afterwards, each well was filled with 150μl of the selected formerly inhibited test microorganisms and incubated at 30°C for 24h. Due to the fact that inhibited wells were visible, the extracts were applied to an LC–MS system [(Agilent 1200 series with DAD detector (200–600nm) in connection with a maXis UHR–TOF mass spectrometer (Bruker Daltonics, USA)] for peak–activity correlation. Samples were analyzed using a Waters ACQUITY UPLC BEH C18 Column, 2.1 x 50mm, 1.7μm. The mobile phase consisted of H2O with 0.1% formic acid as solvent A and CH3CN with 0.1% formic acid as solvent B at a flow rate of 0.6ml.min-1. The gradient was as follows: 0.5min 5% B, 19.5min 95% B and 10min 95% B. Equilibration time between samples was 5min. The column temperature was maintained at 40°C. The main software for processing of results was Data Analysis included in the Compass-software from Bruker (USA).Genomic DNA isolation, PCR conditions and phylogenetic analysis of the most active isolatesFor the taxonomic identification, the 16S rRNA gene of the selected streptomycetes was sequenced. The isolation of genomic DNA was done by the method described by Sambrook et al. <a class="elsevierStyleCrossRef" href="#bib0280">20</a> and amplified by PCR using primers F27 and R1492 according to Cook and Meyers.<a class="elsevierStyleCrossRef" href="#bib0285">21</a> The reaction mixture was made in a total volume of 50μl (5μl of 10 × DreamTaq Green PCR buffer, 5μl of 2 mmol.dm -3 dNTP, 2μl of each 10μmol.dm-3 primer, 0,3μl Taq DNA polymerase and 0,5μl of template DNA (approximately 20 ng)). The PCR reaction ran in the thermo cycler Biometra T Personal (Germany) under the following conditions: 95°C for 3min, 40 cycles of 95°C for 30sec, 56°C for 30sec, 72°C for 90sec and final extension at 72°C for 10min. The PCR products were purified with Exonuclease I and Thermosensitive Alkaline Phosphatase (Sigma-Aldrich, USA).For a rough classification, the 16S rRNA genes were sequenced in MacroGen Company, South Korea. The obtained 16S rRNA sequences were checked for quality and assembled using the program SeqMan II. The similarity and homology of the 16S rRNA gene sequences were analyzed with the similar existing sequences available in the data bank of NCBI using BLAST search (<a id="intr0005" class="elsevierStyleInterRef" href="http://www.ncbi.nlm.nih.gov/BLAST">http://www.ncbi.nlm.nih.gov/BLAST</a>). The phylogenetic tree was constructed with the Maximum - Likelihood method<a class="elsevierStyleCrossRef" href="#bib0290">22</a> using PhyML<a class="elsevierStyleCrossRef" href="#bib0295">23</a>, with bootstrap values based on 1000 replications.Cultural and biochemical characteristicsFor the taxonomic identification, additional to the 16S rRNA gene sequences and morphological traits, physiological and biochemical features of the isolates DK15 and ST13 were determined. Physiological criteria such as a sodium chloride resistance was tested on ISP9 medium supplemented with 2.5, 5, 7.5 and 10% of NaCl, utilization of different carbon sources (glucose, mannitol, arabinose, inositol, mannose, fructose, galactose, rhamnose, sucrose, xylose) was tested on ISP9 medium with the final concentration of carbon sources adjusted to 1%, pH (levels of 2-9) and temperature (4, 25, 28, 30, 37 and 42°C) tolerance was tested on the ISP2 medium. Commercially available test kits such as an ApiZym® and ApiCoryne® (bioMérieux, France) were used for the biochemical characterisation. The Api stripes were inoculated following by manufacturer's manual. The observed characteristics were compared with the phylogenetically related type cultures obtained from German Collection of Microorganisms and Cell Cultures (DSMZ), Braunschweig, Germany.MALDI-TOF MS identificationFor the MALDI–TOF MS analysis, cellular proteins were extracted according to Loucif et al. <a class="elsevierStyleCrossRef" href="#bib0300">24</a>. For both strains, four extractions were performed, and 1μl of each suspension was deposited on the MALDI–TOF steel target plate (Bruker Daltonics, Germany) in three replicates. The plate was allowed to dry at room temperature and then overlaid with 1μl of matrix solution containing α–cyano–hydroxycinnamic acid (SigmaAldrich, USA) saturated with acetonitrile (50%), trifluoroacetic acid (2.5%), and ultrapure water. This mixture was allowed to co–crystallize with the samples. Analysis of protein spectra was performed with the Microflex LT MALDI–TOF MS spectrometer. The measurements were taken in the linear positive ion mode with voltage of 20kV over a mass range of 2–20 kDA. The resulting spectra were analyzed using MALDI Biotyper, and flexAnalysis (Bruker Daltonics). The obtained spectra were compared with our own created database from type Streptomyces cultures obtained from DSMZ, Braunschweig, Germany, which included all the most phylogenetically related species. For the clustering of the Streptomyces species, a mean spectra projection (MSP) dendrogram was constructed with MALDI Biotyper 3.1.ResultsAntimicrobial activity of the crude extracts and identification of the antibacterial compounds by LC/MS analysisTo establish effective bacteria for the control of human pathogens, a total of 57 actinomycetes were isolated from the forest soil samples. 28 isolates representing 10 species were acquired from Vietnam soil while 29 isolates of 8 species were found in Sardinia soil. Out of all 57 isolates, 8 did not show any antimicrobial activity, 13 low activity (A-B dilution of crude extract), 34 high (C-F), and 2 very high (G-H) based on the results from a classical approach of assessing microplates for the growth inhibition. Two of the most active strains were designed as ST13 and DK15. As shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>, the crude extracts exhibited high antimicrobial activities against Gram - positive bacteria and against Gram-negative bacterium Chromobacterium violaceum DSM30191, but weak activity against Escherichia coli DSM1116 and Pseudomonas aeruginosa PA14.<elsevierMultimedia ident="tbl0005"></elsevierMultimedia>Although the nature and type of the active antibacterial compounds were not clear, the prominent antibacterial activities of isolates highlight them as candidates for further investigation. Therefore both ethylacetate extracts were subjected to HPLC fractionation followed by LC/MS analysis of the active compounds. The range of inhibited wells for selected strains revealed that the tested extracts exhibited the strongest antimicrobial activity against Gram-positive bacterium Staphylococcus aureus (inhibited wells until H, strain ST-13) and Gram-negative bacterium Chromobacterium violaceum (inhibited wells until G, strain DK-15).The peak-activity-correlation test (<a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a>) of ST-13 extract revealed that the active fractions after HPLC fractionation were located at retention times 13.0-13.5min. The dominant peak in HPLC chromatogram appearing at this retention time exhibited UV-VIS maxima at 268nm and ESI-HRMS spectrum showing the prominent ion clusters for [M+H]+ at m/z 339.0861. These data correlated to tetrangomycin.<elsevierMultimedia ident="fig0005"></elsevierMultimedia>The second peak-activity-correlation test (<a class="elsevierStyleCrossRef" href="#fig0010">Figure 2</a>) of DK-15 extract revealed that the active fractions were located between retention times 16.0-16.5min. The peak appearing at this retention times exhibit UV-VIS maxima at 364nm and ESI-HRMS spectrum showing the prominent ion clusters for [M +H]+at m/z 743.4268. These data correlated to factumycin.<elsevierMultimedia ident="fig0010"></elsevierMultimedia>Characterization and identification of antibiotic-producing isolates ST13 and DK15Both strains were observed to be Gram-positive, aerobic, non-motile and with abundant substrate and aerial mycelium typical for the genus Streptomyces. In the present study, isolates DK15 and ST13 were subjected to the molecular, protein and polyphasic identification. The 16S rRNA genes were sequenced and compared with the 16S rRNA sequences of previously described the most related type cultures. A comparison of the sequences using Genbank database showed the highest similarity of ST13 with Streptomyces ederensis DSM-40741T (99%, 1450 of 1460 bases were identical, 2 gaps) and Streptomyces phaeochromogenes DSM-40073T (99%, 1448/1463, 4 gaps). Isolate DK15 showed identical sequences with Streptomyces globosus DSM-40815T and Streptomyces toxytricini DSM-40178T. A maximum likehood phylogenetic analysis confirmed these findings (<a class="elsevierStyleCrossRef" href="#fig0015">Figure 3</a>). The sequences of 16S rRNA gene were deposited under accession numbers KX527570 for DK15 and KX527568 for ST13. The MSP dendrogram showed high concordance with the clustering and topology of the 16S rRNA gene tree, and clustered strain ST-13 with Streptomyces ederensis (DSM-40741T) and strain DK-15 with Streptomyces globosus (DSM-40815T) (<a class="elsevierStyleCrossRef" href="#fig0015">Figure 3</a>). These results were in concordance with cultural and physiological features of the tested strains (<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>) and the most related type strains (data available in Compendium of Actinobacteria).<a class="elsevierStyleCrossRef" href="#bib0305">25</a><elsevierMultimedia ident="fig0015"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia>Activity of the extracellular enzymes was quantified using the Api Zym® and Api Coryne® stripes. A huge enzymatic potential was discovered within the tested streptomycetes. It was found that isolates showed high alkaline phosphatase, esterase, leucinearylamidase, valinearylamidase, glucosidase, N-acetyl-glucoseamidase and urease activity (> 40 nmol).From the available literature we found out, that isolate DK15 identified as Streptomyces globosus DK15 represent a new source of factumycin antibiotic and isolate ST13 idenfied as Streptomyces ederensis ST13 represent a new source of tetrangomycin antibiotic. The results from present study indicated, that during our research streptomycete programme we found out two new producers of polyketide antibacterial compounds.DiscussionUsing crude ethylacetate extracts prepared from ST13 and DK15 cells, the high antimicrobial activities were detected against Gram-positive and Gram-negative bacteria. Chromatographic analysis of crude extract of our strains ST13 and DK15 led to the identification of the antibacterial compounds factumycin and tetrangomycin with polyketide structure.Polyketides constitute an important group of secondary metabolites highly relevant as therapeutics for clinical use as many of them are potent antibiotic, antifungal, antitumor, immunosuppressant, antiviral or antiparasitic agents.<a class="elsevierStyleCrossRefs" href="#bib0310">26,27</a> Many polyketide secondary metabolites are produced by a group of filamentous gram-positive bacteria of the Actinomycetales order.<a class="elsevierStyleCrossRef" href="#bib0320">28</a> Tetrangomycin, one of the first members of angucyclinones, was previously isolated from the culture broth of Streptomyces rimosus, or S. cyanogenus S-136. <a class="elsevierStyleCrossRefs" href="#bib0215">7,29</a> Özakin et al.<a class="elsevierStyleCrossRef" href="#bib0235">11</a> reported high antimicrobial activity of crude extract which contained tetrangomycin from Streptomyces sp. CAH29 against MRSA. Our results also indicate highest activity against S. aureus. Activity of tetrangomycin is probably based on inhibition of the staphyloxanthin production by S. aureus and there is a potential of use this substance in new MRSA drug.Factumycin were previously found in S. collinus, Streptomyces sp. WAC5292, and S. lavendulae.<a class="elsevierStyleCrossRefs" href="#bib0330">30,15,13</a>High antimicrobial activity of the factumycin was reported mainly against Gram negative bacteria.<a class="elsevierStyleCrossRef" href="#bib0255">15</a>In our case, inhibition of gram negative as well as gram positive species (M. smegmatis, B. subtilis) was detected however it depends on testing strains.The search for polyketide antibiotics requires the screening and reliable identification of Streptomyces strains which has always been considered to be very difficult<a class="elsevierStyleCrossRef" href="#bib0335">31</a>. Despite specificity of 16S rRNA region, there exist some drawbacks and inconsistencies in this method of identification.<a class="elsevierStyleCrossRef" href="#bib0340">32</a> In our study, sequences of 16S rRNA gene did not allow us identification of strain DK15. Recently, study of Loucif et al.<a class="elsevierStyleCrossRef" href="#bib0300">24</a> demonstrated that protein analysis using MALDI-TOF-MS can be used for the rapid identification of Streptomyces species. Comparison of protein spectra together with analysis of 16S rRNA gene and detailed morphological, physiological and enzymatic analysis provide very exact results about taxonomic position of streptomycete strains we analyzed. Strain ST13 was identified as S. ederensis and strain DK15 as S. globosus. Tetrangomycin have not been previously reported from S. ederensis (producer of moenomycin, bambermycin, and phaeochromycin)<a class="elsevierStyleCrossRefs" href="#bib0345">33-35</a> and factumycin from S. globosus (producer of actinomycin, and 2-deoxystreptamine aminocyclitol aminoglycoside antibiotic)<a class="elsevierStyleCrossRef" href="#bib0360">36</a>, and therefore we reported a new producers of these high active antibacterial compounds. These strains were isolated from the forest soils in national parks. Such soils can be considered as rich deposits of novel active strains with high antimicrobial activity.Conflict of interestThe authors have not declared any conflict of interest." "textoCompletoSecciones" => array:1 [ "secciones" => array:9 [ 0 => array:3 [ "identificador" => "xres1091264" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1034386" "titulo" => "Keywords" ] 2 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 3 => array:3 [ "identificador" => "sec0010" "titulo" => "Material and methods" "secciones" => array:6 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Soil samples and isolation of actinomycetes" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Screening for antimicrobial activity" ] 2 => array:2 [ "identificador" => "sec0025" "titulo" => "HPLC and LC/MS analysis of selected crude extracts" ] 3 => array:2 [ "identificador" => "sec0030" "titulo" => "Genomic DNA isolation, PCR conditions and phylogenetic analysis of the most active isolates" ] 4 => array:2 [ "identificador" => "sec0035" "titulo" => "Cultural and biochemical characteristics" ] 5 => array:2 [ "identificador" => "sec0040" "titulo" => "MALDI-TOF MS identification" ] ] ] 4 => array:3 [ "identificador" => "sec0045" "titulo" => "Results" "secciones" => array:1 [ 0 => array:2 [ "identificador" => "sec0050" "titulo" => "Characterization and identification of antibiotic-producing isolates ST13 and DK15" ] ] ] 5 => array:2 [ "identificador" => "sec0055" "titulo" => "Discussion" ] 6 => array:2 [ "identificador" => "sec0060" "titulo" => "Conflict of interest" ] 7 => array:2 [ "identificador" => "xack370739" "titulo" => "Acknowledgments" ] 8 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2017-06-12" "fechaAceptado" => "2017-12-13" "PalabrasClave" => array:1 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1034386" "palabras" => array:5 [ 0 => "Streptomyces" 1 => "16S rRNA" 2 => "MALDI-TOF MS" 3 => "Tetrangomycin" 4 => "Factumycin" ] ] ] ] "tieneResumen" => true "resumen" => array:1 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "Fifty seven soil-borne actinomycete strains were assessed for the antibiotic production. Two of the most active isolates, designed as Streptomyces ST-13 and DK-15 exhibited a broad range of antimicrobial activity and therefore they were selected for HPLC fractionation against the most suppressed bacteria Staphylococcus aureus (ST-13) and Chromobacterium violaceum (DK-15). LC/MS analysis of extracts showed the presence of polyketides factumycin (DK15) and tetrangomycin (ST13). The taxonomic position of the antibiotic-producing actinomycetes was determined using a polyphasic approach. Phenotypic characterization and 16S rRNA gene sequence analysis of the isolates matched those described for members of the genus Streptomyces. DK-15 strain exhibited the highest 16S rRNA gene sequence similarity to Streptomyces globosus DSM-40815 (T) and Streptomyces toxytricini DSM-40178 (T) and ST-13 strain to Streptomyces ederensis DSM-40741 (T) and Streptomyces phaeochromogenes DSM-40073 (T). For the proper identification, MALDI-TOF/MS profile of whole-cell proteins led to the identification of S. globosus DK-15 (accession number: KX527570) and S. ederensis ST13 (accession number: KX527568). To our knowledge, there is no report about the production of these antibiotics by S.globosus and S. ederensis, thus isolates DK15 and ST13 identified as S. globosus DK-15 and S.ederensis ST-13 can be considered as new sources of these unique antibacterial metabolites." ] ] "apendice" => array:1 [ 0 => array:1 [ "seccion" => array:1 [ 0 => array:4 [ "apendice" => "<elsevierMultimedia ident="upi0005"></elsevierMultimedia>" "etiqueta" => "Appendix A" "titulo" => "Supplementary data" "identificador" => "sec0070" ] ] ] ] "multimedia" => array:6 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 2183 "Ancho" => 3004 "Tamanyo" => 286283 ] ] "descripcion" => array:1 [ "en" => "Fractionation RP-HPLC chromatogram of tetrangomycin, UV spectrum of tetrangomycin with the max at 268nm, and ESI-HRMS spectrum, showing the prominent ion clusters for [M+H]+ at m/z 339.0861." ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 2173 "Ancho" => 3004 "Tamanyo" => 309351 ] ] "descripcion" => array:1 [ "en" => "Fractionation RP-HPLC chromatogram of factumycin, UV spectrum of factumycin with the max. at 364nm, and ESI-HRMS spectrum, showing the prominent ion clusters for [M+H]+ at m/z 743.4268." ] ] 2 => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 1637 "Ancho" => 2500 "Tamanyo" => 155636 ] ] "descripcion" => array:1 [ "en" => "Comparison between 16S rRNA phylogenetic tree and the MSP dendrogram. A. Mean spectra projection (MSP) dendrogram, B. 16S rRNA based phylogenetic tree of Streptomyces type strains, T1-T11 – DSM type cultures used for grouping of Streptomyces species, T1 - Streptomyces viridis DSM-42078 (T), T2 - S. phaeochromogenes DSM- 40788 (T), T3 - S. ederensis DSM-40741 (T), T4 - S. iakyrus DSM-40482 (T), T5 - S. griseochromogenes DSM-40499 (T), T6 - S. gougerotii DSM-40324 (T), T7 - S. albus DSM-40313 (T), T8 - S. diastaticus DSM-40495 (T), T9 - S. alboflavus DSM-40045 (T), T10 - S. toxytricini DSM-40178 (T), T11 - S. globosus DSM-41122 (T)." ] ] 3 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at1" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "leyenda" => "Dilution stages represented stepwise 2-fold dilution of crude extracts (A – crude extract from 1,33ml of Streptomyces culture in 1ml of inoculated media, B – 0.66ml.ml-1; C – 0.66ml.ml-1; D – 0.33ml.ml-1;E – 0.17ml.ml-1; F – 0.08ml.ml-1; G – 0.04ml.ml-1;and H – 0.02ml.ml-1)" "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-with-role" title="table-head ; entry_with_role_rowhead " align="left" valign="top" scope="col">Indicator microorganisms \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " colspan="2" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Dilution stages (A-H)</th></tr><tr title="table-row"><th class="td" title="table-head " align="" valign="top" scope="col" style="border-bottom: 2px solid black"> \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">ST-13 \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">DK-15 \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">Bacillus subtilis (DSM10) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">G \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">F \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">Chromobacterium violaceum (DSM30191) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">C \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">G \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">Escherichia coli (DSM1116) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">B \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">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">Escherichia coli (TolC) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">C \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">C \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">Micrococcus luteus (DSM1790) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">G \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">D \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">Pseudomonas aeruginosa (PA14) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">- \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">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">Mycobacterium smegmatis (ATCC700084) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">F \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">F \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">Staphylococcus aureus (Newman) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">H \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">E \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">Mucor hiemalis (DSM2656) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">C \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">Pichia anomala (DSM6766) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">D \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">Candida albicans (DSM1665) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">B \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1865938.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Dilution stages of the crude extracts prepared from isolates DK-15 and ST-13." ] ] 4 => array:8 [ "identificador" => "tbl0010" "etiqueta" => "Table 2" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at2" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "leyenda" => "+ positive growth, - negative growth, ISP - International Streptomycete Project" "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-with-role" title="table-head ; entry_with_role_rowhead " align="left" valign="top" scope="col">Test \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " colspan="2" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Labeling of strains</th></tr><tr title="table-row"><th class="td" title="table-head " align="" valign="top" scope="col" style="border-bottom: 2px solid black"> \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">DK15 \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">ST13 \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">Gram staining \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \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">Spore chain \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">RF \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">RF \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">Aerial mycelium \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">ISP2-ISP5 beige red, ISP6-ISP7 no \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">ISP2-ISP5,7 grey, ISP6 none \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">Substrate mycelium \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">ISP2,7 yellow, ISP3-6 ivory \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">ISP2-7 brown \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">Soluble pigment color \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">- \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">ISP6-7 brown \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">Melanin production \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">- \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \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">NaCl tolerance up to: \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">2.5 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">5.0 \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">Utilization of carbon sources</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Glucose \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \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">Raffinose \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">- \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \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">Arabinose \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">- \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \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">Inositol \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">- \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \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">Mannose \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">- \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \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">Fructose \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \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">Rhamnose \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \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">Sucrose \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">- \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">+ \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">Xylose \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">- \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">- \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">Cellulose \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">- \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">- \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">Optimal pH \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">7 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">7 \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">Optimal temperature \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">30°C \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">28°C \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1865937.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Cultural, morphological and physiological characteristics of strains DK-15 and ST-13." ] ] 5 => array:5 [ "identificador" => "upi0005" "tipo" => "MULTIMEDIAECOMPONENTE" "mostrarFloat" => false "mostrarDisplay" => true "Ecomponente" => array:2 [ "fichero" => "mmc1.docx" "ficheroTamanyo" => 12752 ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:36 [ 0 => array:3 [ "identificador" => "bib0185" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Microbial drug discovery: 80 years of progress" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "A.L. 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Biotechnology and Industrial Microbiology

Ivana Charousová

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, Juraj Medo, Lukáš Hleba, Soňa Javoreková

Slovak University of Agriculture in Nitra, Faculty of Biotechnology and Food Sciences, Department of Microbiology, Tr. A. Hlinku 2, 949 76, Nitra, Slovak Republic

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    "titulo" => "Streptomyces globosus DK15 and Streptomyces ederensis ST13 as new producers of factumycin and tetrangomycin antibiotics"
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          "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Fractionation RP-HPLC chromatogram of factumycin&#44; UV spectrum of factumycin with the max&#46; at 364<span class="elsevierStyleHsp" style=""></span>nm&#44; and ESI-HRMS spectrum&#44; showing the prominent ion clusters for &#91;M&#43;H&#93;&#43; at <span class="elsevierStyleItalic">m&#47;z</span> 743&#46;4268&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Since people started suffering from diseases caused by infectious microorganisms&#44; the quest for their remedies led to the discovery of a large number of antibiotics from microorganisms&#46;<a class="elsevierStyleCrossRef" href="#bib0185"><span class="elsevierStyleSup">1</span></a> Most of the research was dedicated to study the polyketide bioactive compounds&#46;<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">2</span></a> One of the most important and well acknowledged group of the prolific producers of polyketide antibiotics are the actinomycetes&#44; mainly terrestrial representatives of the genus <span class="elsevierStyleItalic">Streptomyces</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">3</span></a> Polyketides have played an important role in the antibiotic drug discovery with most antibacterial drugs being derived from a natural product or natural product lead&#46;<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">4</span></a> Examples of natural products with the polyketide structure include the tetrangomycin and factumycin&#46; Tetrangomycins belong to the group of polyketide angucyclinones&#44; naturally occurring benzaanthraquinones that had been isolated from <span class="elsevierStyleItalic">Streptomyces rimosus</span> and <span class="elsevierStyleItalic">Streptomyces griseus&#46;</span><a class="elsevierStyleCrossRefs" href="#bib0205"><span class="elsevierStyleSup">5&#8211;8</span></a> Angucyclinones&#44; benz&#91;a&#93;anthraquinone derivatives isolated from <span class="elsevierStyleItalic">Streptomyces</span> spp&#46; have attracted much attention due to their broad and strong biological activities&#44; mainly antiviral&#44; antifungal&#44; and antitumor&#46;<a class="elsevierStyleCrossRefs" href="#bib0205"><span class="elsevierStyleSup">5&#44;9&#8211;10</span></a> Immunosuppressive function of tetrangomycin by reducing the transcription of cytokine genes and the inhibitory activity of tetrangomycin against methicilin resistant <span class="elsevierStyleItalic">Staphylococus aureus</span> &#40;MRSA&#41; was described by &#214;zakin <span class="elsevierStyleItalic">et al</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">11</span></a> Factumycin is a linear polyketide elfamycin compound and had been isolated from <span class="elsevierStyleItalic">Streptomyces lavendulae</span> and <span class="elsevierStyleItalic">Streptomyces griseus</span>&#46;<a class="elsevierStyleCrossRefs" href="#bib0240"><span class="elsevierStyleSup">12&#8211;14</span></a> According to Thaker <span class="elsevierStyleItalic">et al</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">15</span></a> a screen of factumycin in combination with known antibiotics revealed unexpected synergy with tetracyclines&#44; offering a possible new application of factumycin as a lead in Gram-negative targeted antibiotic combination therapy&#46; Identification of factumycin antibiotic has high importance&#44; because Gram - negative pathogens are becoming increasingly antibiotic resistant and consequently a serious clinical challenge&#46;<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">15</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Therefore&#44; an attempt has been made to isolate the antibiotic-producing actinomycetes with emphasis on the selection and the detailed identification of <span class="elsevierStyleItalic">Streptomyces</span> polyketide-producers&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Material and methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Soil samples and isolation of actinomycetes</span><p id="par0015" class="elsevierStylePara elsevierViewall">Actinomycetes were isolated by the dilution agar plating method from the forest soils located in Vietnam&#44; Phu Quoc National Park &#40;10&#176;09¿33&#46;49&#8220;S 103&#176;59¿07&#46;02&#8221;V&#41; and in Sardinia&#44; Foresta di Monte Pisanu &#40;40&#176;25&#8242;30&#46;24&#8220;S 8&#176;58&#8242;34&#46;72&#8243;V&#41;&#46; An aliquot of 0&#46;1<span class="elsevierStyleHsp" style=""></span>ml of solution was taken and spread over the surface of starch-casein medium&#46;<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">16</span></a> Plates were incubated at 30<span class="elsevierStyleHsp" style=""></span>&#176;C and monitored after 7 days&#46; The selected strains were maintained by cultivation on the ISP2 medium<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">17</span></a>&#44; incubated at 30<span class="elsevierStyleHsp" style=""></span>&#176;C for 10 days and stored at &#8211; 20<span class="elsevierStyleHsp" style=""></span>&#176;C in the presence of glycerol &#40;30&#37; v&#47;v&#41;&#46; For all acquired actinomycete isolates&#44; 16S rRNA sequences as well as microscopic &#40;shape of spore chains&#41; and macroscopic morphology &#40;colors of aerial and substrate mycelium&#44; soluble pigments and melanin&#41; were studied in accordance with the guidelines established by the International Streptomycete Project&#46;<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">17</span></a></p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Screening for antimicrobial activity</span><p id="par0020" class="elsevierStylePara elsevierViewall">The morphologically different actinomycete isolates were screened against four Gram - positive bacteria &#91;<span class="elsevierStyleItalic">Bacillus subtilis</span> &#40;DSM 10&#41;&#44; <span class="elsevierStyleItalic">Micrococcus luteus</span> &#40;DSM1790&#41;&#44; <span class="elsevierStyleItalic">Staphylococcus aureus</span> &#40;Newman&#41;&#44; <span class="elsevierStyleItalic">Mycobacterium smegmatis</span> &#40;ATCC 700084&#41;&#93;&#44; four Gram - negative bacteria &#91;<span class="elsevierStyleItalic">Escherichia coli</span> &#40;DSM 1116&#41;&#44; <span class="elsevierStyleItalic">Escherichia coli</span> &#40;TolC&#41;&#44; <span class="elsevierStyleItalic">Pseudomonas aeruginosa</span> &#40;PA14&#41;&#44; <span class="elsevierStyleItalic">Chromobacterium violaceum</span> &#40;DSM 30191&#41;&#93;&#44; two yeasts &#91;<span class="elsevierStyleItalic">Candida albicans</span> &#40;DSM 1665&#41;&#44; <span class="elsevierStyleItalic">Pichia anomala</span> &#40;DSM 6766&#41;&#93; and one filamentous microscopic fungus <span class="elsevierStyleItalic">Mucor hiemalis</span> &#40;DSM 2656&#41; obtained from DSMZ &#40;German Collection of Microorganisms and Cell Cultures&#41;&#44; Braunschweig&#44; Germany and ATCC &#40;American Type Culture Collection&#41;&#44; Manassas&#44; VA 20110&#44; USA&#46; Raw extracts were prepared from 20<span class="elsevierStyleHsp" style=""></span>ml of 5 day old liquid culture using ethyl acetate &#40;Sigma-Aldrich&#44; USA&#41; according to Wink &#40;2014&#41;&#46; Ethylacetate was evaporated and extract was dissolved in 1<span class="elsevierStyleHsp" style=""></span>ml of ethylacetate&#58; acetone&#58; methanol &#40;1&#58;1&#58;1&#41; solution&#46; Detection of biological activity was carried out by preparing 4 - 6<span class="elsevierStyleHsp" style=""></span>h cultures of indicator bacteria followed by dilution with Mueller- Hinton &#40;MH&#41; broth &#40;Merck&#44; Germany&#41; and yeast and fungi by dilution with Mycosel broth<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">18</span></a> to obtain 0&#46;01 McFarland turbidity&#46; The antimicrobial activity of streptomycetes was performed by using the broth micro - dilution method <a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">19</span></a> in 96 - well microplates &#40;BRAND&#44; Germany&#41;&#46; The dose in well A corresponds to the extract made from 1&#46;33<span class="elsevierStyleHsp" style=""></span>ml <span class="elsevierStyleItalic">Streptomyces</span> liquid culture per 1<span class="elsevierStyleHsp" style=""></span>ml of the inoculated broth&#46; Concentration decreased 2 fold in wells B-H&#46; The readings were made after 24<span class="elsevierStyleHsp" style=""></span>h of incubation through visual observation of the growth&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">HPLC and LC&#47;MS analysis of selected crude extracts</span><p id="par0025" class="elsevierStylePara elsevierViewall">The most active raw extracts were selected for the fractionation by liquid - chromatography &#40;Agilent 1100&#41; equipment&#46; The wavelength monitoring was performed at 210 and 360<span class="elsevierStyleHsp" style=""></span>nm&#46; Sample &#40;5<span class="elsevierStyleHsp" style=""></span>&#956;l&#41; was injected onto a HPLC column &#40;X-Bridge 3&#46;5<span class="elsevierStyleHsp" style=""></span>&#956;m&#44; 2&#46;1x100<span class="elsevierStyleHsp" style=""></span>mm&#59; Waters&#44; Milford&#44; USA&#41;&#46; Separation was performed using the buffers A2&#58; 950<span class="elsevierStyleHsp" style=""></span>ml H<span class="elsevierStyleInf">2</span>O&#44; 50<span class="elsevierStyleHsp" style=""></span>ml acetonitrile &#43; 0&#46;05<span class="elsevierStyleHsp" style=""></span>mM &#40;385<span class="elsevierStyleHsp" style=""></span>mg&#46;l<span class="elsevierStyleSup">-1</span>&#41; ammonium acetate &#43; 40<span class="elsevierStyleHsp" style=""></span>&#956;l acetic acid&#59; B2&#58; 50<span class="elsevierStyleHsp" style=""></span>ml H<span class="elsevierStyleInf">2</span>O&#44; 950<span class="elsevierStyleHsp" style=""></span>ml acetonitrile&#44; 0&#46;05<span class="elsevierStyleHsp" style=""></span>mM &#40;385<span class="elsevierStyleHsp" style=""></span>mg&#46;l<span class="elsevierStyleSup">-1</span>&#41; ammonium acetate &#43; 40<span class="elsevierStyleHsp" style=""></span>&#956;l acetic acid and a DAD detector &#40;200-400<span class="elsevierStyleHsp" style=""></span>nm&#41;&#46; Fractions &#40;0&#46;15<span class="elsevierStyleHsp" style=""></span>ml&#41; from the HPLC column were collected in a 96 well plates every 0&#46;5<span class="elsevierStyleHsp" style=""></span>min and dried with heated nitrogen in MiniVap &#40;Porvair Sciences&#44; UK&#41; for 45-60<span class="elsevierStyleHsp" style=""></span>min at 40<span class="elsevierStyleHsp" style=""></span>&#176;C&#46; Afterwards&#44; each well was filled with 150<span class="elsevierStyleHsp" style=""></span>&#956;l of the selected formerly inhibited test microorganisms and incubated at 30<span class="elsevierStyleHsp" style=""></span>&#176;C for 24<span class="elsevierStyleHsp" style=""></span>h&#46; Due to the fact that inhibited wells were visible&#44; the extracts were applied to an LC&#8211;MS system &#91;&#40;Agilent 1200 series with DAD detector &#40;200&#8211;600<span class="elsevierStyleHsp" style=""></span>nm&#41; in connection with a maXis UHR&#8211;TOF mass spectrometer &#40;Bruker Daltonics&#44; USA&#41;&#93; for peak&#8211;activity correlation&#46; Samples were analyzed using a Waters ACQUITY UPLC BEH C18 Column&#44; 2&#46;1 x 50<span class="elsevierStyleHsp" style=""></span>mm&#44; 1&#46;7<span class="elsevierStyleHsp" style=""></span>&#956;m&#46; The mobile phase consisted of H<span class="elsevierStyleInf">2</span>O with 0&#46;1&#37; formic acid as solvent A and CH<span class="elsevierStyleInf">3</span>CN with 0&#46;1&#37; formic acid as solvent B at a flow rate of 0&#46;6<span class="elsevierStyleHsp" style=""></span>ml&#46;min<span class="elsevierStyleSup">-1</span>&#46; The gradient was as follows&#58; 0&#46;5<span class="elsevierStyleHsp" style=""></span>min 5&#37; B&#44; 19&#46;5<span class="elsevierStyleHsp" style=""></span>min 95&#37; B and 10<span class="elsevierStyleHsp" style=""></span>min 95&#37; B&#46; Equilibration time between samples was 5<span class="elsevierStyleHsp" style=""></span>min&#46; The column temperature was maintained at 40<span class="elsevierStyleHsp" style=""></span>&#176;C&#46; The main software for processing of results was Data Analysis included in the Compass-software from Bruker &#40;USA&#41;&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Genomic DNA isolation&#44; PCR conditions and phylogenetic analysis of the most active isolates</span><p id="par0030" class="elsevierStylePara elsevierViewall">For the taxonomic identification&#44; the 16S rRNA gene of the selected streptomycetes was sequenced&#46; The isolation of genomic DNA was done by the method described by Sambrook <span class="elsevierStyleItalic">et al</span>&#46; <a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">20</span></a> and amplified by PCR using primers F27 and R1492 according to Cook and Meyers&#46;<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">21</span></a> The reaction mixture was made in a total volume of 50<span class="elsevierStyleHsp" style=""></span>&#956;l &#40;5<span class="elsevierStyleHsp" style=""></span>&#956;l of 10 &#215; DreamTaq Green PCR buffer&#44; 5<span class="elsevierStyleHsp" style=""></span>&#956;l of 2 mmol&#46;dm <span class="elsevierStyleSup">-3</span> dNTP&#44; 2<span class="elsevierStyleHsp" style=""></span>&#956;l of each 10<span class="elsevierStyleHsp" style=""></span>&#956;mol&#46;dm<span class="elsevierStyleSup">-3</span> primer&#44; 0&#44;3<span class="elsevierStyleHsp" style=""></span>&#956;l Taq DNA polymerase and 0&#44;5<span class="elsevierStyleHsp" style=""></span>&#956;l of template DNA &#40;approximately 20 ng&#41;&#41;&#46; The PCR reaction ran in the thermo cycler Biometra T Personal &#40;Germany&#41; under the following conditions&#58; 95<span class="elsevierStyleHsp" style=""></span>&#176;C for 3<span class="elsevierStyleHsp" style=""></span>min&#44; 40 cycles of 95<span class="elsevierStyleHsp" style=""></span>&#176;C for 30<span class="elsevierStyleHsp" style=""></span>sec&#44; 56<span class="elsevierStyleHsp" style=""></span>&#176;C for 30<span class="elsevierStyleHsp" style=""></span>sec&#44; 72<span class="elsevierStyleHsp" style=""></span>&#176;C for 90<span class="elsevierStyleHsp" style=""></span>sec and final extension at 72<span class="elsevierStyleHsp" style=""></span>&#176;C for 10<span class="elsevierStyleHsp" style=""></span>min&#46; The PCR products were purified with Exonuclease I and Thermosensitive Alkaline Phosphatase &#40;Sigma-Aldrich&#44; USA&#41;&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">For a rough classification&#44; the 16S rRNA genes were sequenced in MacroGen Company&#44; South Korea&#46; The obtained 16S rRNA sequences were checked for quality and assembled using the program SeqMan II&#46; The similarity and homology of the 16S rRNA gene sequences were analyzed with the similar existing sequences available in the data bank of NCBI using BLAST search &#40;<a id="intr0005" class="elsevierStyleInterRef" href="http://www.ncbi.nlm.nih.gov/BLAST">http&#58;&#47;&#47;www&#46;ncbi&#46;nlm&#46;nih&#46;gov&#47;BLAST</a>&#41;&#46; The phylogenetic tree was constructed with the Maximum - Likelihood method<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">22</span></a> using PhyML<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">23</span></a>&#44; with bootstrap values based on 1000 replications&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Cultural and biochemical characteristics</span><p id="par0040" class="elsevierStylePara elsevierViewall">For the taxonomic identification&#44; additional to the 16S rRNA gene sequences and morphological traits&#44; physiological and biochemical features of the isolates DK15 and ST13 were determined&#46; Physiological criteria such as a sodium chloride resistance was tested on ISP9 medium supplemented with 2&#46;5&#44; 5&#44; 7&#46;5 and 10&#37; of NaCl&#44; utilization of different carbon sources &#40;glucose&#44; mannitol&#44; arabinose&#44; inositol&#44; mannose&#44; fructose&#44; galactose&#44; rhamnose&#44; sucrose&#44; xylose&#41; was tested on ISP9 medium with the final concentration of carbon sources adjusted to 1&#37;&#44; pH &#40;levels of 2-9&#41; and temperature &#40;4&#44; 25&#44; 28&#44; 30&#44; 37 and 42<span class="elsevierStyleHsp" style=""></span>&#176;C&#41; tolerance was tested on the ISP2 medium&#46; Commercially available test kits such as an ApiZym&#174; and ApiCoryne&#174; &#40;bioM&#233;rieux&#44; France&#41; were used for the biochemical characterisation&#46; The Api stripes were inoculated following by manufacturer&#39;s manual&#46; The observed characteristics were compared with the phylogenetically related type cultures obtained from German Collection of Microorganisms and Cell Cultures &#40;DSMZ&#41;&#44; Braunschweig&#44; Germany&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">MALDI-TOF MS identification</span><p id="par0045" class="elsevierStylePara elsevierViewall">For the MALDI&#8211;TOF MS analysis&#44; cellular proteins were extracted according to Loucif <span class="elsevierStyleItalic">et al</span>&#46; <a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">24</span></a>&#46; For both strains&#44; four extractions were performed&#44; and 1<span class="elsevierStyleHsp" style=""></span>&#956;l of each suspension was deposited on the MALDI&#8211;TOF steel target plate &#40;Bruker Daltonics&#44; Germany&#41; in three replicates&#46; The plate was allowed to dry at room temperature and then overlaid with 1<span class="elsevierStyleHsp" style=""></span>&#956;l of matrix solution containing &#945;&#8211;cyano&#8211;hydroxycinnamic acid &#40;SigmaAldrich&#44; USA&#41; saturated with acetonitrile &#40;50&#37;&#41;&#44; trifluoroacetic acid &#40;2&#46;5&#37;&#41;&#44; and ultrapure water&#46; This mixture was allowed to co&#8211;crystallize with the samples&#46; Analysis of protein spectra was performed with the Microflex LT MALDI&#8211;TOF MS spectrometer&#46; The measurements were taken in the linear positive ion mode with voltage of 20<span class="elsevierStyleHsp" style=""></span>kV over a mass range of 2&#8211;20 kDA&#46; The resulting spectra were analyzed using MALDI Biotyper&#44; and flexAnalysis &#40;Bruker Daltonics&#41;&#46; The obtained spectra were compared with our own created database from type <span class="elsevierStyleItalic">Streptomyces cultures</span> obtained from DSMZ&#44; Braunschweig&#44; Germany&#44; which included all the most phylogenetically related species&#46; For the clustering of the <span class="elsevierStyleItalic">Streptomyces</span> species&#44; a mean spectra projection &#40;MSP&#41; dendrogram was constructed with MALDI Biotyper 3&#46;1&#46;</p></span></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Results</span><p id="par0050" class="elsevierStylePara elsevierViewall">Antimicrobial activity of the crude extracts and identification of the antibacterial compounds by LC&#47;MS analysis</p><p id="par0055" class="elsevierStylePara elsevierViewall">To establish effective bacteria for the control of human pathogens&#44; a total of 57 actinomycetes were isolated from the forest soil samples&#46; 28 isolates representing 10 species were acquired from Vietnam soil while 29 isolates of 8 species were found in Sardinia soil&#46; Out of all 57 isolates&#44; 8 did not show any antimicrobial activity&#44; 13 low activity &#40;A-B dilution of crude extract&#41;&#44; 34 high &#40;C-F&#41;&#44; and 2 very high &#40;G-H&#41; based on the results from a classical approach of assessing microplates for the growth inhibition&#46; Two of the most active strains were designed as ST13 and DK15&#46; As shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#44; the crude extracts exhibited high antimicrobial activities against Gram - positive bacteria and against Gram-negative bacterium <span class="elsevierStyleItalic">Chromobacterium violaceum</span> DSM30191&#44; but weak activity against <span class="elsevierStyleItalic">Escherichia coli</span> DSM1116 and <span class="elsevierStyleItalic">Pseudomonas aeruginosa</span> PA14&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0060" class="elsevierStylePara elsevierViewall">Although the nature and type of the active antibacterial compounds were not clear&#44; the prominent antibacterial activities of isolates highlight them as candidates for further investigation&#46; Therefore both ethylacetate extracts were subjected to HPLC fractionation followed by LC&#47;MS analysis of the active compounds&#46; The range of inhibited wells for selected strains revealed that the tested extracts exhibited the strongest antimicrobial activity against Gram-positive bacterium <span class="elsevierStyleItalic">Staphylococcus aureus</span> &#40;inhibited wells until H&#44; strain ST-13&#41; and Gram-negative bacterium <span class="elsevierStyleItalic">Chromobacterium violaceum</span> &#40;inhibited wells until G&#44; strain DK-15&#41;&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">The peak-activity-correlation test &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a>&#41; of ST-13 extract revealed that the active fractions after HPLC fractionation were located at retention times 13&#46;0-13&#46;5<span class="elsevierStyleHsp" style=""></span>min&#46; The dominant peak in HPLC chromatogram appearing at this retention time exhibited UV-VIS maxima at 268<span class="elsevierStyleHsp" style=""></span>nm and ESI-HRMS spectrum showing the prominent ion clusters for &#91;M&#43;H&#93;&#43; at <span class="elsevierStyleItalic">m&#47;z</span> 339&#46;0861&#46; These data correlated to <span class="elsevierStyleBold">tetrangomycin</span>&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0070" class="elsevierStylePara elsevierViewall">The second peak-activity-correlation test &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Figure 2</a>&#41; of DK-15 extract revealed that the active fractions were located between retention times 16&#46;0-16&#46;5<span class="elsevierStyleHsp" style=""></span>min&#46; The peak appearing at this retention times exhibit UV-VIS maxima at 364<span class="elsevierStyleHsp" style=""></span>nm and ESI-HRMS spectrum showing the prominent ion clusters for &#91;M <span class="elsevierStyleSup">&#43;</span>H&#93;<span class="elsevierStyleSup">&#43;</span>at <span class="elsevierStyleItalic">m&#47;z</span> 743&#46;4268&#46; These data correlated to <span class="elsevierStyleBold">factumycin</span>&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Characterization and identification of antibiotic-producing isolates ST13 and DK15</span><p id="par0075" class="elsevierStylePara elsevierViewall">Both strains were observed to be Gram-positive&#44; aerobic&#44; non-motile and with abundant substrate and aerial mycelium typical for the genus <span class="elsevierStyleItalic">Streptomyces</span>&#46; In the present study&#44; isolates DK15 and ST13 were subjected to the molecular&#44; protein and polyphasic identification&#46; The 16S rRNA genes were sequenced and compared with the 16S rRNA sequences of previously described the most related type cultures&#46; A comparison of the sequences using Genbank database showed the highest similarity of ST13 with <span class="elsevierStyleItalic">Streptomyces ederensis</span> DSM-40741T &#40;99&#37;&#44; 1450 of 1460 bases were identical&#44; 2 gaps&#41; and <span class="elsevierStyleItalic">Streptomyces phaeochromogenes</span> DSM-40073T &#40;99&#37;&#44; 1448&#47;1463&#44; 4 gaps&#41;&#46; Isolate DK15 showed identical sequences with <span class="elsevierStyleItalic">Streptomyces globosus</span> DSM-40815T and <span class="elsevierStyleItalic">Streptomyces toxytricini</span> DSM-40178T&#46; A maximum likehood phylogenetic analysis confirmed these findings &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Figure 3</a>&#41;&#46; The sequences of 16S rRNA gene were deposited under accession numbers KX527570 for DK15 and KX527568 for ST13&#46; The MSP dendrogram showed high concordance with the clustering and topology of the 16S rRNA gene tree&#44; and clustered strain ST-13 with <span class="elsevierStyleItalic">Streptomyces ederensis</span> &#40;DSM-40741T&#41; and strain DK-15 with <span class="elsevierStyleItalic">Streptomyces globosus</span> &#40;DSM-40815T&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Figure 3</a>&#41;&#46; These results were in concordance with cultural and physiological features of the tested strains &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41; and the most related type strains &#40;data available in Compendium of Actinobacteria&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">25</span></a></p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0080" class="elsevierStylePara elsevierViewall">Activity of the extracellular enzymes was quantified using the Api Zym&#174; and Api Coryne&#174; stripes&#46; A huge enzymatic potential was discovered within the tested streptomycetes&#46; It was found that isolates showed high alkaline phosphatase&#44; esterase&#44; leucinearylamidase&#44; valinearylamidase&#44; glucosidase&#44; N-acetyl-glucoseamidase and urease activity &#40;&#62; 40 nmol&#41;&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">From the available literature we found out&#44; that isolate DK15 identified as <span class="elsevierStyleItalic">Streptomyces globosus</span> DK15 represent a new source of factumycin antibiotic and isolate ST13 idenfied as <span class="elsevierStyleItalic">Streptomyces ederensis</span> ST13 represent a new source of tetrangomycin antibiotic&#46; The results from present study indicated&#44; that during our research streptomycete programme we found out two new producers of polyketide antibacterial compounds&#46;</p></span></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Discussion</span><p id="par0090" class="elsevierStylePara elsevierViewall">Using crude ethylacetate extracts prepared from ST13 and DK15 cells&#44; the high antimicrobial activities were detected against Gram-positive and Gram-negative bacteria&#46; Chromatographic analysis of crude extract of our strains ST13 and DK15 led to the identification of the antibacterial compounds factumycin and tetrangomycin with polyketide structure&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">Polyketides constitute an important group of secondary metabolites highly relevant as therapeutics for clinical use as many of them are potent antibiotic&#44; antifungal&#44; antitumor&#44; immunosuppressant&#44; antiviral or antiparasitic agents&#46;<a class="elsevierStyleCrossRefs" href="#bib0310"><span class="elsevierStyleSup">26&#44;27</span></a> Many polyketide secondary metabolites are produced by a group of filamentous gram-positive bacteria of the <span class="elsevierStyleItalic">Actinomycetales</span> order&#46;<a class="elsevierStyleCrossRef" href="#bib0320"><span class="elsevierStyleSup">28</span></a> Tetrangomycin&#44; one of the first members of angucyclinones&#44; was previously isolated from the culture broth of <span class="elsevierStyleItalic">Streptomyces rimosus</span>&#44; or <span class="elsevierStyleItalic">S&#46; cyanogenus</span> S-136&#46; <a class="elsevierStyleCrossRefs" href="#bib0215"><span class="elsevierStyleSup">7&#44;29</span></a> &#214;zakin <span class="elsevierStyleItalic">et al</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">11</span></a> reported high antimicrobial activity of crude extract which contained tetrangomycin from <span class="elsevierStyleItalic">Streptomyces</span> sp&#46; CAH29 against MRSA&#46; Our results also indicate highest activity against <span class="elsevierStyleItalic">S&#46; aureus</span>&#46; Activity of tetrangomycin is probably based on inhibition of the staphyloxanthin production by <span class="elsevierStyleItalic">S&#46; aureus</span> and there is a potential of use this substance in new MRSA drug&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">Factumycin were previously found in S&#46; collinus&#44; Streptomyces sp&#46; WAC5292&#44; and S&#46; lavendulae&#46;<a class="elsevierStyleCrossRefs" href="#bib0330"><span class="elsevierStyleSup">30&#44;15&#44;13</span></a><span class="elsevierStyleItalic">High antimicrobial activity of the factumycin was reported mainly against Gram negative bacteria&#46;</span><a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">15</span></a><span class="elsevierStyleItalic">In our case&#44; inhibition of gram negative as well as gram positive species &#40;M&#46; smegmatis&#44; B&#46; subtilis&#41; was detected however it depends on testing strains&#46;</span></p><p id="par0105" class="elsevierStylePara elsevierViewall">The search for polyketide antibiotics requires the screening and reliable identification of <span class="elsevierStyleItalic">Streptomyces</span> strains which has always been considered to be very difficult<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">31</span></a>&#46; Despite specificity of 16S rRNA region&#44; there exist some drawbacks and inconsistencies in this method of identification&#46;<a class="elsevierStyleCrossRef" href="#bib0340"><span class="elsevierStyleSup">32</span></a> In our study&#44; sequences of 16S rRNA gene did not allow us identification of strain DK15&#46; Recently&#44; study of Loucif <span class="elsevierStyleItalic">et al</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">24</span></a> demonstrated that protein analysis using MALDI-TOF-MS can be used for the rapid identification of <span class="elsevierStyleItalic">Streptomyces</span> species&#46; Comparison of protein spectra together with analysis of 16S rRNA gene and detailed morphological&#44; physiological and enzymatic analysis provide very exact results about taxonomic position of streptomycete strains we analyzed&#46; Strain ST13 was identified as <span class="elsevierStyleItalic">S&#46; ederensis</span> and strain DK15 as <span class="elsevierStyleItalic">S&#46; globosus</span>&#46; Tetrangomycin have not been previously reported from <span class="elsevierStyleItalic">S&#46; ederensis</span> &#40;producer of moenomycin&#44; bambermycin&#44; and phaeochromycin&#41;<a class="elsevierStyleCrossRefs" href="#bib0345"><span class="elsevierStyleSup">33-35</span></a> and factumycin from <span class="elsevierStyleItalic">S&#46; globosus</span> &#40;producer of actinomycin&#44; and 2-deoxystreptamine aminocyclitol aminoglycoside antibiotic&#41;<a class="elsevierStyleCrossRef" href="#bib0360"><span class="elsevierStyleSup">36</span></a>&#44; and therefore we reported a new producers of these high active antibacterial compounds&#46; These strains were isolated from the forest soils in national parks&#46; Such soils can be considered as rich deposits of novel active strains with high antimicrobial activity&#46;</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Conflict of interest</span><p id="par0110" class="elsevierStylePara elsevierViewall">The authors have not declared any conflict of interest&#46;</p></span></span>"
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          "titulo" => "Introduction"
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          "titulo" => "Material and methods"
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              "titulo" => "Soil samples and isolation of actinomycetes"
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            1 => array:2 [
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              "titulo" => "Screening for antimicrobial activity"
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              "titulo" => "HPLC and LC&#47;MS analysis of selected crude extracts"
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            3 => array:2 [
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              "titulo" => "Genomic DNA isolation&#44; PCR conditions and phylogenetic analysis of the most active isolates"
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              "titulo" => "Cultural and biochemical characteristics"
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          "titulo" => "Results"
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              "titulo" => "Characterization and identification of antibiotic-producing isolates ST13 and DK15"
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          "titulo" => "Discussion"
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          "identificador" => "xack370739"
          "titulo" => "Acknowledgments"
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          "titulo" => "References"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Fifty seven soil-borne actinomycete strains were assessed for the antibiotic production&#46; Two of the most active isolates&#44; designed as <span class="elsevierStyleItalic">Streptomyces</span> ST-13 and DK-15 exhibited a broad range of antimicrobial activity and therefore they were selected for HPLC fractionation against the most suppressed bacteria <span class="elsevierStyleItalic">Staphylococcus aureus</span> &#40;ST-13&#41; and <span class="elsevierStyleItalic">Chromobacterium violaceum</span> &#40;DK-15&#41;&#46; LC&#47;MS analysis of extracts showed the presence of polyketides factumycin &#40;DK15&#41; and tetrangomycin &#40;ST13&#41;&#46; The taxonomic position of the antibiotic-producing actinomycetes was determined using a polyphasic approach&#46; Phenotypic characterization and 16S rRNA gene sequence analysis of the isolates matched those described for members of the genus <span class="elsevierStyleItalic">Streptomyces</span>&#46; DK-15 strain exhibited the highest 16S rRNA gene sequence similarity to <span class="elsevierStyleItalic">Streptomyces globosus</span> DSM-40815 &#40;T&#41; and <span class="elsevierStyleItalic">Streptomyces toxytricini</span> DSM-40178 &#40;T&#41; and ST-13 strain to <span class="elsevierStyleItalic">Streptomyces ederensis</span> DSM-40741 &#40;T&#41; and <span class="elsevierStyleItalic">Streptomyces phaeochromogenes</span> DSM-40073 &#40;T&#41;&#46; For the proper identification&#44; MALDI-TOF&#47;MS profile of whole-cell proteins led to the identification of <span class="elsevierStyleItalic">S&#46; globosus</span> DK-15 &#40;accession number&#58; KX527570&#41; and <span class="elsevierStyleItalic">S&#46; ederensis</span> ST13 &#40;accession number&#58; KX527568&#41;&#46; To our knowledge&#44; there is no report about the production of these antibiotics by <span class="elsevierStyleItalic">S&#46;globosus</span> and <span class="elsevierStyleItalic">S&#46; ederensis</span>&#44; thus isolates DK15 and ST13 identified as <span class="elsevierStyleItalic">S&#46; globosus</span> DK-15 and <span class="elsevierStyleItalic">S&#46;ederensis</span> ST-13 can be considered as new sources of these unique antibacterial metabolites&#46;</p></span>"
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          "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Comparison between 16S rRNA phylogenetic tree and the MSP dendrogram&#46; <span class="elsevierStyleBold">A&#46;</span> Mean spectra projection &#40;MSP&#41; dendrogram&#44; <span class="elsevierStyleBold">B&#46;</span> 16S rRNA based phylogenetic tree of <span class="elsevierStyleItalic">Streptomyces</span> type strains&#44; <span class="elsevierStyleBold">T1-T11</span> &#8211; DSM type cultures used for grouping of <span class="elsevierStyleItalic">Streptomyces</span> species&#44; T1 - <span class="elsevierStyleItalic">Streptomyces viridis</span> DSM-42078 &#40;T&#41;&#44; T2 - <span class="elsevierStyleItalic">S&#46; phaeochromogenes</span> DSM- 40788 &#40;T&#41;&#44; T3 - <span class="elsevierStyleItalic">S&#46; ederensis</span> DSM-40741 &#40;T&#41;&#44; T4 - <span class="elsevierStyleItalic">S&#46; iakyrus</span> DSM-40482 &#40;T&#41;&#44; T5 - <span class="elsevierStyleItalic">S&#46; griseochromogenes</span> DSM-40499 &#40;T&#41;&#44; T6 - <span class="elsevierStyleItalic">S&#46; gougerotii</span> DSM-40324 &#40;T&#41;&#44; T7 - <span class="elsevierStyleItalic">S&#46; albus</span> DSM-40313 &#40;T&#41;&#44; T8 - <span class="elsevierStyleItalic">S&#46; diastaticus</span> DSM-40495 &#40;T&#41;&#44; T9 - <span class="elsevierStyleItalic">S&#46; alboflavus</span> DSM-40045 &#40;T&#41;&#44; T10 - <span class="elsevierStyleItalic">S&#46; toxytricini</span> DSM-40178 &#40;T&#41;&#44; T11 - <span class="elsevierStyleItalic">S&#46; globosus</span> DSM-41122 &#40;T&#41;&#46;</p>"
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          "leyenda" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Dilution stages represented stepwise 2-fold dilution of crude extracts &#40;A &#8211; crude extract from 1&#44;33<span class="elsevierStyleHsp" style=""></span>ml of <span class="elsevierStyleItalic">Streptomyces</span> culture in 1<span class="elsevierStyleHsp" style=""></span>ml of inoculated media&#44; B &#8211; 0&#46;66<span class="elsevierStyleHsp" style=""></span>ml&#46;ml<span class="elsevierStyleSup">-1</span>&#59; C &#8211; 0&#46;66<span class="elsevierStyleHsp" style=""></span>ml&#46;ml<span class="elsevierStyleSup">-1</span>&#59; D &#8211; 0&#46;33<span class="elsevierStyleHsp" style=""></span>ml&#46;ml<span class="elsevierStyleSup">-1</span>&#59;E &#8211; 0&#46;17<span class="elsevierStyleHsp" style=""></span>ml&#46;ml<span class="elsevierStyleSup">-1</span>&#59; F &#8211; 0&#46;08<span class="elsevierStyleHsp" style=""></span>ml&#46;ml<span class="elsevierStyleSup">-1</span>&#59; G &#8211; 0&#46;04<span class="elsevierStyleHsp" style=""></span>ml&#46;ml<span class="elsevierStyleSup">-1</span>&#59;and H &#8211; 0&#46;02<span class="elsevierStyleHsp" style=""></span>ml&#46;ml<span class="elsevierStyleSup">-1</span>&#41;</p>"
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                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td-with-role" title="table-head ; entry_with_role_rowhead " align="left" valign="top" scope="col">Indicator microorganisms&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " colspan="2" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Dilution stages &#40;A-H&#41;</th></tr><tr title="table-row"><th class="td" title="table-head  " align="" valign="top" scope="col" style="border-bottom: 2px solid black">&nbsp;\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">ST-13&nbsp;\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">DK-15&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Bacillus subtilis</span> &#40;DSM10&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">G&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">F&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Chromobacterium violaceum</span> &#40;DSM30191&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">C&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">G&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Escherichia coli</span> &#40;DSM1116&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">B&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">B&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Escherichia coli</span> &#40;TolC&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">C&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">C&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Micrococcus luteus</span> &#40;DSM1790&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">G&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">D&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Pseudomonas aeruginosa</span> &#40;PA14&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" 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">A&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Mycobacterium smegmatis</span> &#40;ATCC700084&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">F&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">F&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Staphylococcus aureus</span> &#40;Newman&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">H&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">E&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Mucor hiemalis</span> &#40;DSM2656&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">A&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">C&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Pichia anomala</span> &#40;DSM6766&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">A&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">D&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Candida albicans</span> &#40;DSM1665&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">A&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">B&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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                  \t\t\t\t\tvoid\n
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                  \t\t\t\t</th><th class="td" title="table-head  " colspan="2" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Labeling of strains</th></tr><tr title="table-row"><th class="td" title="table-head  " align="" valign="top" scope="col" style="border-bottom: 2px solid black">&nbsp;\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">DK15&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">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#43;&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">RF&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">RF&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Aerial mycelium</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">ISP2-ISP5 beige red&#44; ISP6-ISP7 no&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">ISP2-ISP5&#44;7 grey&#44; ISP6 none&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">ISP2&#44;7 yellow&#44; ISP3-6 ivory&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">ISP2-7 brown&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">Soluble pigment color</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" 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">ISP6-7 brown&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">-&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">NaCl tolerance up to&#58;</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">2&#46;5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">5&#46;0&nbsp;\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"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td" title="table-entry  " colspan="3" align="left" valign="top"><span class="elsevierStyleItalic">Utilization of carbon sources</span></td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Glucose&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Raffinose&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">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Arabinose&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">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Inositol&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" 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">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Mannose&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" 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">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Fructose&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Rhamnose&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Sucrose&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" 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">&#43;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Xylose&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">-&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Cellulose&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" 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">-&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Optimal pH&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Optimal temperature&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">30<span class="elsevierStyleHsp" style=""></span>&#176;C&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">28<span class="elsevierStyleHsp" style=""></span>&#176;C&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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                0 => array:2 [
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                    0 => array:2 [
                      "titulo" => "Microbial drug discovery&#58; 80 years of progress"
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                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
                            0 => "A&#46;L&#46; Demain"
                            1 => "S&#46; Sanchez"
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                    0 => array:2 [
                      "doi" => "10.1038/ja.2008.16"
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                        "tituloSerie" => "J Antibiot&#46;"
                        "fecha" => "2009"
                        "volumen" => "62"
                        "numero" => "1"
                        "paginaInicial" => "5"
                        "paginaFinal" => "16"
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                      "titulo" => "Molecular insights on the biosynthesis of antitumour compounds by actinomycetes"
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                          "autores" => array:3 [
                            0 => "C&#46; Olano"
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                            2 => "J&#46;A&#46; Salas"
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                    0 => array:2 [
                      "doi" => "10.1111/j.1751-7915.2010.00231.x"
                      "Revista" => array:7 [
                        "tituloSerie" => "Microb Biotechnol&#46;"
                        "fecha" => "2011"
                        "volumen" => "4"
                        "numero" => "2"
                        "paginaInicial" => "144"
                        "paginaFinal" => "164"
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        "texto" => "<p id="par0115" class="elsevierStylePara elsevierViewall">The authors are grateful to the Helmholtz Centre for Infection Research &#40;Microbial Strain Collection Group&#41;&#44; Braunschweig&#44; Germany for the scholarship and support of the results&#46; This study was also supported by the Scientific Grant Agency of the Ministry of Education of the Slovak Republic and of the Slovak Academy of Sciences grant no&#46; VEGA 1&#47;0305&#47;17&#46; The authors are grateful to Ms&#46; Martina Drexlerova for the editing and English corrections&#46;</p>"
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Article information

ISSN: 15178382
Original language: English

DOI:10.1016/j.bjm.2017.12.007

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Year/Month	Html	Pdf	Total

2024 November	9	1	10
2024 October	39	12	51
2024 September	56	29	85
2024 August	48	27	75
2024 July	38	24	62
2024 June	49	6	55
2024 May	48	19	67
2024 April	60	11	71
2024 March	81	8	89
2024 February	51	10	61
2024 January	79	9	88
2023 December	64	19	83
2023 November	94	22	116
2023 October	108	14	122
2023 September	60	9	69
2023 August	59	16	75
2023 July	52	9	61
2023 June	76	22	98
2023 May	76	18	94
2023 April	87	12	99
2023 March	79	15	94
2023 February	63	15	78
2023 January	47	11	58
2022 December	57	10	67
2022 November	66	25	91
2022 October	42	20	62
2022 September	56	376	432
2022 August	39	19	58
2022 July	40	10	50
2022 June	46	24	70
2022 May	61	26	87
2022 April	82	23	105
2022 March	137	17	154
2022 February	140	11	151
2022 January	132	12	144
2021 December	73	13	86
2021 November	75	12	87
2021 October	64	31	95
2021 September	57	21	78
2021 August	84	16	100
2021 July	50	17	67
2021 June	50	17	67
2021 May	38	7	45
2021 April	94	17	111
2021 March	35	28	63
2021 February	30	21	51
2021 January	37	13	50
2020 December	31	17	48
2020 November	15	9	24
2020 October	16	5	21
2020 September	21	14	35
2020 August	28	13	41
2020 July	40	21	61
2020 June	32	21	53
2020 May	26	13	39
2020 April	19	11	30
2020 March	26	8	34
2020 February	35	15	50
2020 January	22	11	33
2019 December	22	9	31
2019 November	16	9	25
2019 October	18	12	30
2019 September	17	10	27
2019 August	10	6	16
2019 July	14	12	26
2019 June	16	19	35
2019 May	7	10	17
2019 February	1	1	2
2018 November	34	32	66
2018 October	29	21	50
2018 September	0	11	11
2018 August	0	15	15
2018 July	0	16	16
2018 June	0	11	11
2018 May	0	6	6
2018 April	0	2	2

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