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Original article
Antagonist activities and phylogenetic relationships of actinomycetes isolated from an Artemisia habitat
Actividades antagónicas y relaciones filogenéticas de actinomicetos aislados de un hábitat de Artemisia
Ana Cecilia Gonzalez-Francoa,1, Loreto Robles-Hernándezb,1,
Corresponding author
lrobles@uach.mx

Corresponding author.
a Department of Microbiology, Molecular Biology and Biochemistry, University of Idaho, Moscow, ID 83844-3052, USA
b Department of Entomology, Plant Pathology and Nematology, University of Idaho, Moscow, ID 83844-2339, USA
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Introduction</span><p id="par0020" class="elsevierStylePara elsevierViewall">Actinomycetes comprise an extensive and diverse group of gram-positive&#44; aerobic&#44; mycelial bacteria that play an important physiological and ecological role in soil&#46;<a class="elsevierStyleCrossRefs" href="#bib0310"><span class="elsevierStyleSup">29&#44;31</span></a> They can degrade a wide diversity of recalcitrant compounds such as lignocelluloses and many other polymers occurring in soil and litter&#44; as well as a range of xenobiotic compounds&#46;<a class="elsevierStyleCrossRefs" href="#bib0185"><span class="elsevierStyleSup">4&#44;7&#44;19</span></a> Because of their metabolic diversity&#44; actinomycetes are a great source of lytic enzymes&#44; antibiotics and a great deal of other bioactive metabolites&#46;<a class="elsevierStyleCrossRefs" href="#bib0190"><span class="elsevierStyleSup">5&#44;10&#44;28</span></a> This group of organisms produce more than half of the naturally occurring antibiotics discovered to date and continue to be screened for useful compounds&#46;<a class="elsevierStyleCrossRefs" href="#bib0190"><span class="elsevierStyleSup">5&#44;8</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">Because actinomycetes are largely spread in nature&#44; they have been isolated from many environments including soils&#44; composts&#44; plant materials and waters&#46;<a class="elsevierStyleCrossRefs" href="#bib0190"><span class="elsevierStyleSup">5&#44;10&#44;23&#44;26</span></a> Actinomycetes&#44; especially <span class="elsevierStyleItalic">Streptomyces</span> spp&#46; isolated from rhizosphere soils&#44; sometimes represent novel species&#46;<a class="elsevierStyleCrossRefs" href="#bib0245"><span class="elsevierStyleSup">16&#44;20</span></a> They are great root colonizers&#44; where they protect the plants against phytopathogens and promote plant growth&#46;<a class="elsevierStyleCrossRefs" href="#bib0170"><span class="elsevierStyleSup">1&#44;11&#44;24&#44;33</span></a></p><p id="par0030" class="elsevierStylePara elsevierViewall">Desert plants such as <span class="elsevierStyleItalic">Artemisia</span> spp&#46; are known to produce a great diversity of phenols and terpenoids with antimicrobial activities&#46;<a class="elsevierStyleCrossRef" href="#bib0315"><span class="elsevierStyleSup">30</span></a> Thus&#44; rhizosphere actinomycetes from <span class="elsevierStyleItalic">Artemisia</span>&#44; which can endure unfavorable growth conditions&#44; are worthy of examination for antimicrobial activities&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">The present study involved the screening for antimicrobial activities of actinomycetes from rhizosphere soils of <span class="elsevierStyleItalic">Artemisia tridentata</span> and their counterpart bulk soils&#46; Their antagonistic activity was characterized based on <span class="elsevierStyleItalic">in vitro</span> bioassays against a broad panel of bacteria and fungal plant pathogens&#46; A select group of the actinomycetes strongly antagonistic to all filamentous fungi tested was further characterized for antagonism toward two drug-resistant strains of <span class="elsevierStyleItalic">Candida albicans</span>&#58; ATCC MY-204276 &#40;fluconazole-resistant&#41; and ATCC 44373 &#40;5-fluorocytosine-resistant&#41;&#46; In addition&#44; a selection of three strongly antifungal groups of isolates were further characterized by partial 16s rRNA gene amplification&#44; and phylogenetic trees were constructed to determine if there was a relationship between antimicrobial activity and genetic relatedness&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Material and methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Source of actinomycetes</span><p id="par0040" class="elsevierStylePara elsevierViewall">Two hundred and two actinomycete strains were previously isolated from two sagebrush rhizosphere soils &#91;one from a young plant &#40;RSYP&#41; and one from an old growth plant &#40;RSOP&#41;&#93;&#44; and two non-rhizosphere bulk soils near the sagebrush &#40;B1Y and B1O&#44; for the young and old plant system&#44; respectively&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">9</span></a></p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Evaluation of antimicrobial activities</span><p id="par0045" class="elsevierStylePara elsevierViewall">Antimicrobial susceptibility tests were performed <span class="elsevierStyleItalic">in vitro</span> by using a panel of plant pathogen strains including&#58; <span class="elsevierStyleItalic">Fusarium oxysporum</span> ATCC 070233 as well as <span class="elsevierStyleItalic">Rhizoctonia solani</span> and <span class="elsevierStyleItalic">Pythium ultimum</span>&#59; two gram-positive bacteria &#40;<span class="elsevierStyleItalic">Bacillus subtilis</span> and <span class="elsevierStyleItalic">Rathayibacter tritici</span>&#41; and two gram-negative bacteria &#40;<span class="elsevierStyleItalic">Xanthomonas campestris</span> pv&#46; <span class="elsevierStyleItalic">campestris</span> and <span class="elsevierStyleItalic">Burkholderia cepacea</span>&#41;&#46; All fungal strains were from Dr&#46; Don Crawford&#39;s laboratory stock&#44; Department of Microbiology&#44; Molecular Biology and Biochemistry&#44; while the bacterial strains were from the Bacteriology laboratory&#44; Department of Entomology&#44; Plant Pathology and Nematology&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">The antimicrobial susceptibility for filamentous fungi were assessed following the <span class="elsevierStyleItalic">in vitro</span> plate bioassay&#46; Actinomycete isolates were streak-inoculated to one side of PDA and YDA plates and incubated at 30<span class="elsevierStyleHsp" style=""></span>&#176;C for eight days to allow the production and diffusion of metabolites and extracellular hydrolytic enzymes&#46; An agar plug containing actively growing fungus was then placed onto the opposite side of the inoculated plates and incubated at 30<span class="elsevierStyleHsp" style=""></span>&#176;C&#46; Fungal mycelial plugs were placed on noninoculated plates as controls&#46; Growth inhibition was recorded at different time intervals&#44; depending on the fungus&#44; for 7 days&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">The antimicrobial bioassay plates for bacteria were performed by streak-inoculation of the actinomycete to one side of multiple PDA plates and incubated at 30<span class="elsevierStyleHsp" style=""></span>&#176;C for 10 days to allow the production and diffusion of metabolites and extracellular hydrolytic enzymes&#46; Forty-eight-hour bacterial growth from NBY &#40;ATCC Medium 763&#41; plates was then inoculated as lines perpendicular to the actinomycete growth and incubated at 30<span class="elsevierStyleHsp" style=""></span>&#176;C&#46; Bacteria were also streaked on non-inoculated plates to serve as controls&#46;<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">2</span></a> Bacterial growth inhibition was recorded at different time intervals for 5 days&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">A selected group of actinomycetes strongly antagonistic to all filamentous fungi tested were further characterized for antagonism toward two drug-resistant strains of <span class="elsevierStyleItalic">Candida albicans</span>&#58; ATCC MY-204276 &#40;fluconazole resistant&#41; and ATCC 44373 &#40;5-fluorocytosine-resistant&#41;&#46; Anti-<span class="elsevierStyleItalic">Candida</span> activity was tested as described for bacteria except for PDA and YDA were used instead&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">PCR amplification of partial 16s rRNA gene sequences</span><p id="par0065" class="elsevierStylePara elsevierViewall">Genomic DNA from the isolates with potent antifungal activity were extracted using the UltraClean&#8482; Microbial DNA Isolation Kit &#40;Mo Bio Laboratories&#44; Inc&#46;&#44; Solana Beach&#44; CA&#41; according to the manufacturer&#39;s instructions&#46; 16S rDNA partial sequences of cultured isolates were amplified using the primers 27F &#40;5&#8242;-AGAGTTTGATCMTGGCTCAG-3&#8242;&#41; and 907R &#40;5&#697;-CCGTCAATTCMTTTRAGTT-3&#697;&#41;&#46; Each PCR mixture contained 20<span class="elsevierStyleHsp" style=""></span>&#956;mol&#47;l &#40;each&#41; primer&#44; 0&#46;2<span class="elsevierStyleHsp" style=""></span>mmol&#47;l &#40;each&#41; dNTPs&#44; 25<span class="elsevierStyleHsp" style=""></span>mmol&#47;l MgCl<span class="elsevierStyleInf">2</span>&#44; 5<span class="elsevierStyleHsp" style=""></span>&#956;l of 10x PCR universal buffer &#40;Invitrogen TECH-LINE&#8482;&#44; USA&#41; 1<span class="elsevierStyleHsp" style=""></span>&#956;l of the DNA template&#44; and 1&#46;25<span class="elsevierStyleHsp" style=""></span>U of Taq DNA polymerase &#40;Invitrogen TECH-LINE&#8482;&#44; USA&#41; to a final volume of 50<span class="elsevierStyleHsp" style=""></span>&#956;l&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">Thermocycling conditions were as follows&#58; one cycle at 95<span class="elsevierStyleHsp" style=""></span>&#176;C for 5<span class="elsevierStyleHsp" style=""></span>min&#59; followed by 30 cycles &#40;each&#41; at 95<span class="elsevierStyleHsp" style=""></span>&#176;C for 1<span class="elsevierStyleHsp" style=""></span>min&#44; 55<span class="elsevierStyleHsp" style=""></span>&#176;C for 1<span class="elsevierStyleHsp" style=""></span>min&#44; and 72<span class="elsevierStyleHsp" style=""></span>&#176;C for 2<span class="elsevierStyleHsp" style=""></span>min&#59; and finally&#44; one cycle at 72<span class="elsevierStyleHsp" style=""></span>&#176;C for 7<span class="elsevierStyleHsp" style=""></span>min in a Gene Amp PCR System 2400 thermocycler &#40;Applied Biosystems&#41;&#46; The positive control consisted of reaction mixtures containing 8<span class="elsevierStyleHsp" style=""></span>&#956;g of DNA of <span class="elsevierStyleItalic">Streptomyces lydicus</span> WYEC-108&#46; The negative control lacked the DNA template but contained all other reactants&#46; A 1-kb plus ladder &#40;GIBCO BRL Life Technologies&#41; was used as a DNA size marker&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">The purified PCR amplicons were sequenced by the Laboratory of Biotechnology and Bioanalysis at Washington State University &#40;Pullman&#44; WA&#41;&#46; Sequences were compared against known sequences using the NCBI BLAST database&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Phylogenetic analysis</span><p id="par0080" class="elsevierStylePara elsevierViewall">The BioEdit program was used as an editing tool to facilitate sequence analysis&#46; Multiple alignments were obtained using the Clustal W program&#46; Phylogenetic trees were inferred by three algorithms&#44; the maximum-parsimony&#44; neighbor-joining&#44; and maximum-likelihood methods using the PAUP&#42; package&#46; In addition&#44; the 16S rDNA sequence of <span class="elsevierStyleItalic">Haemophilus paragallinarum</span> was added to the analysis as an out-group&#46; Bootstrap analyses for the neighbor-joining and the maximum-likelihood results were generated based on 200 re-samplings&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">Evolutionary distance matrices for the neighbor-joining method were generated&#46; The TreeView &#40;WIN 32&#41; program was used for viewing the trees generated by the three algorithms&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Statistical analysis</span><p id="par0090" class="elsevierStylePara elsevierViewall">The generalized linear model was used&#44; assuming a binomial distribution to test for significant activity effect across soils&#46; Pair-wise comparisons among soils were done using contrasts and chi-square tests&#46; All computations were carried out using SAS 8&#46;2 Copyright &#40;c&#41; 1999&#8211;2001 by SAS Institute Inc&#46;&#44; Cary&#44; NC&#44; USA&#46;</p></span></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Results</span><p id="par0095" class="elsevierStylePara elsevierViewall">Two hundred and two actinomycetes were isolated from the four mentioned soils and their antifungal activities showed that isolates from both rhizosphere soils&#44; RSYP and RSOP&#44; had the highest activity against <span class="elsevierStyleItalic">F&#46; oxysporum</span>&#59; however&#44; they were not significantly different from those of their bulk soils &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; The highest antagonistic activities against <span class="elsevierStyleItalic">R&#46; solani</span> were detected in RSOP&#59; this was significantly different from the rest of the soils&#44; followed by the activities of bulk soils B1Y and B1O&#46; The highest anti-<span class="elsevierStyleItalic">Pythium</span> activities were detected in organisms found in three soil samples&#58; bulk soil B1Y and rhizosphere soils&#44; RSOP and RSYP&#46; Bulk soil B1O activity was significantly lower than that in the other three soils &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46;The antibacterial activities of isolates from bulk soils B1Y and B1O had higher activities against Gram-negative bacteria&#44; <span class="elsevierStyleItalic">X&#46; campestris</span> pv&#46; <span class="elsevierStyleItalic">campestris</span> and <span class="elsevierStyleItalic">B&#46; cepacea</span> than their counterparts RSYP and RSOP&#59; however&#44; no statistical differences were detected among soils &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41;&#46; On the other hand&#44; the highest activities against Gram-positive bacteria&#44; such as <span class="elsevierStyleItalic">B&#46; subtilis</span>&#44; were detected in the isolates of bulk soil B1Y and rhizosphere soil RSOP&#44; with no statistical difference between the two&#44; followed by the antagonistic activity of bulk soil B1O &#40;<a class="elsevierStyleCrossRef" href="#tbl0015">Table 3</a>&#41;&#46; Finally&#44; isolates from soil B1Y showed the highest antagonistic activity against <span class="elsevierStyleItalic">Rathayibacter</span>&#44; followed by both rhizosphere soils&#44; RSYP and RSOP&#59; isolates from bulk soil B1O had the lowest activity against <span class="elsevierStyleItalic">Rathayibacter</span> &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><elsevierMultimedia ident="tbl0015"></elsevierMultimedia><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Selected isolates</span><p id="par0100" class="elsevierStylePara elsevierViewall">Forty-two isolates out of two hundred and two actinomycetes were selected for their strong antifungal activity&#46; They were divided into three groups&#58; Group 1 was comprised of antagonistic isolates with broad-spectrum antifungal activity against lower &#40;<span class="elsevierStyleItalic">P&#46; ultimum</span>&#41; and higher filamentous fungi &#40;<span class="elsevierStyleItalic">F&#46; oxysporum</span> and <span class="elsevierStyleItalic">R&#46; solani</span>&#41;&#59; Group 2 contained isolates with only anti-<span class="elsevierStyleItalic">Pythium</span> activity&#44; and Group 3 was comprised of those isolates with both anti-<span class="elsevierStyleItalic">Rhizoctonia</span> and anti-<span class="elsevierStyleItalic">Fusarium</span> activities &#40;<a class="elsevierStyleCrossRef" href="#tbl0015">Table 3</a>&#41;&#46; Of the selected strains&#44; 17 were from RSOP &#40;overall 29&#46;3&#37; of isolates with strong antifungal activity&#41;&#59; bulk soil B1O accounted for six isolates &#40;overall 13&#46;95&#37; of isolates with strong antifungal activity&#41;&#59; none of the isolates of this soil showed strong inhibition against <span class="elsevierStyleItalic">P&#46; ultimum</span>&#46; On the other hand&#44; only four isolates &#40;overall 14&#46;8&#37; of isolates with strong antifungal activity&#41; from RSYP were selected&#59; none of the isolates were classified into Group 3&#46; Its counterpart bulk soil BYO accounted for 15 strong antifungal isolates &#40;20&#46;3&#37; of isolates with strong antifungal activity&#41;&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Anti-<span class="elsevierStyleItalic">Candida</span> activities</span><p id="par0105" class="elsevierStylePara elsevierViewall">Twelve isolates that showed antagonism against all three phytopathogenic filamentous fungi tested were also screened for anti-<span class="elsevierStyleItalic">Candida</span> activities &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; Antagonistic activity was detected toward both strains of <span class="elsevierStyleItalic">C&#46; albicans</span> &#40;ATCC MY-204276&#44; fluconazole-resistant and ATCC 44373&#44; 5-fluorocytosine-resistant&#41; in both media &#40;PDA and YDA&#41;&#44; with different levels of activities observed between both media&#46; <span class="elsevierStyleItalic">C&#46; albicans</span> ATCC 44373 was inhibited to the greatest extent on PDA by strain R1O41&#44; followed by B1O9&#44; R1Y9 and R1Y10 while isolates R1O44 and B1O10 only showed antagonistic activity on YDA&#44; but to a great extent&#44; after R1O41&#46; Isolates R1O7-2&#44; R1O3-2&#44; R1O4-2 and B1Y54&#44; all showed lesser antagonistic activity in both media &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>A&#41;&#46; Inhibition toward <span class="elsevierStyleItalic">C&#46; albicans</span> ATCC MY-204276 was higher on PDA in most isolates &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; On PDA&#44; strain R1O41 was the best inhibitor&#44; followed by B1Y14&#44; B1Y54 and R1O7-2 while isolates R1O41&#44; B1Y14 and R1O7-2 showed the highest activity on YDA&#59; isolate R1Y9 only showed antagonism on PDA&#46; The comparison of anti-Candida activity on PDA and YDA by strain is shown in <a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a>&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">16S rDNA sequence analysis</span><p id="par0110" class="elsevierStylePara elsevierViewall">Analysis of the partial 16S rRNA gene sequences of 42 selected strong antifungal isolates by BLAST revealed that 31 belonged to the genus <span class="elsevierStyleItalic">Streptomyces</span> while the remaining 11 strains were only identified as actinobacteria &#40;<a class="elsevierStyleCrossRef" href="#tbl0015">Table 3</a>&#41;&#46; Analysis of the 16S rRNA gene of the isolates B1Y37 and R1O49 showed 100&#37; sequence identity with <span class="elsevierStyleItalic">Streptomyces ciscaucasicus</span> strain DSM 40275 &#40;accession AY508512&#41;&#44; and <span class="elsevierStyleItalic">Streptomyces</span><span class="elsevierStyleItalic">africanus</span> &#40;accession AY208912&#41;&#44; respectively&#46; Isolates B1Y3&#44; R1054 and R1O59 had 100&#37; sequence identity with the undefined <span class="elsevierStyleItalic">actinobacterium</span> 17a-5 &#40;accession AY561563&#41;&#46; Isolates B1Y54&#44; R2O4&#44; R1Y25&#44; B1Y64&#44; and R1O31 had 98&#37; sequence identity to <span class="elsevierStyleItalic">S&#46; violaceusniger</span> &#40;accession AJ391823&#41;&#44; <span class="elsevierStyleItalic">Streptomyces</span> sp&#46; LK4-2 &#40;AY277376&#41;&#44; <span class="elsevierStyleItalic">S&#46; griseocarneus</span> &#40;X99943&#41;&#44; <span class="elsevierStyleItalic">Streptomyces</span> sp&#46; &#40;accession AY167807&#44; AJ621613 and AJ621604&#41;&#44; and <span class="elsevierStyleItalic">Streptomyces</span> sp&#46; &#40;Y15499&#41;&#44; respectively&#46; The remaining isolates had 99&#37; sequence identity with the best match&#40;es&#41; in the blast search &#40;<a class="elsevierStyleCrossRef" href="#tbl0015">Table 3</a>&#41;&#46;</p><p id="par0115" class="elsevierStylePara elsevierViewall">Fragment 27F-907R of the forty-two selected isolates was also used to construct a multiple alignment and a phylogenetic tree&#44; which is shown in <a class="elsevierStyleCrossRef" href="#fig0010">Figure 2</a>&#46; Bootstrap analysis of the tree revealed that all of the phylogenetic relationships were not resolved by using only partial 16S rDNA sequences&#46; Additional studies will be needed to resolve all the intraspecies relationships among various <span class="elsevierStyleItalic">Streptomyces</span> strains&#59; however&#44; very defined branches and some clades were generated with the three different algorithms used&#46; One of the defined branches grouped all the isolates identified in the blast search as actinobacteria&#44; while those isolates with 98&#37; identity to <span class="elsevierStyleItalic">Streptomyces</span> sp&#46; were in one of the major clusters of the neighbor-joining tree &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; All the antagonists against filamentous fungi of group one that also showed anti-yeast activity were located on one major cluster by the analysis&#46; Those isolates within group two &#40;strong anti-<span class="elsevierStyleItalic">Pythium</span> activity&#41; and group three &#40;strong anti-<span class="elsevierStyleItalic">Rhizoctonia</span> and Anti-<span class="elsevierStyleItalic">Fusarium</span> activity&#41;&#44; were found all over the tree&#44; and did not fall into a specific branch or clade on the tree &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia></span></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Discussion</span><p id="par0120" class="elsevierStylePara elsevierViewall">Within the rhizosphere&#44; plant roots have a direct effect on composition and density of the soil microbial populations&#46; Root exudates selectively influence the growth of bacterial and fungal populations by altering the presence of substrates in soil in the vicinity of roots&#46;<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">27</span></a> The varieties of organic compounds released by plants have been postulated to be a key factor influencing the diversity of microorganisms in the rhizosphere of different plant species&#46;<a class="elsevierStyleCrossRefs" href="#bib0180"><span class="elsevierStyleSup">3&#44;32</span></a> Sagebrush roots are known for their wide production of phenols&#44; and other aromatic compounds as well as terpenoids with antimicrobial activities&#46;<a class="elsevierStyleCrossRefs" href="#bib0230"><span class="elsevierStyleSup">13&#44;17&#44;30</span></a> Those antimicrobial compounds can be used as a carbon source by some microorganisms&#44; including actinomycetes&#46;<a class="elsevierStyleCrossRefs" href="#bib0225"><span class="elsevierStyleSup">12&#44;19</span></a> Therefore&#44; it is not surprising that actinomycetes actively grow and colonize root systems like those of desert sagebrush plants&#46;<a class="elsevierStyleCrossRefs" href="#bib0210"><span class="elsevierStyleSup">9&#44;15</span></a></p><p id="par0125" class="elsevierStylePara elsevierViewall">In the present work&#44; the sagebrush rhizosphere soil of the old plant &#40;RSOP&#41; appears to be enriched in highly active antifungal and antibacterial Gram-positive compound-producing actinomycetes&#59; while the rhizosphere soil of the young plant &#40;RSYP&#41; enriched for anti-<span class="elsevierStyleItalic">Fusarium</span> actinomycetes with lower antibacterial actinomycetes compared to its counterpart bulk soil showing a lower rhizosphere effect than that in the old plant&#46; These differences can be explained by the rhizosphere effect&#44; and by the qualitative and quantitative differences in root exudates due to the different plant ages&#46;<a class="elsevierStyleCrossRefs" href="#bib0270"><span class="elsevierStyleSup">21&#44;27</span></a> In this context&#44; it was demonstrated that the roots of <span class="elsevierStyleItalic">Artemisia tridentata</span> produce different types of antimicrobial and phytotoxic secondary metabolites depending on the age of the plant&#46;<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">13</span></a> On the other hand&#44; in our study&#44; the antimicrobial activities of each rhizosphere soil were compared to its counterpart bulk soil to avoid soil effect&#46; It is well known that the soil type qualitatively and quantitatively affects microbial communities in the rhizosphere&#46;<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">3</span></a></p><p id="par0130" class="elsevierStylePara elsevierViewall">Forty-two actinomycetes &#40;21&#37; of the total number of isolates&#41; were selected for their strong antifungal properties and classified into three groups based on their activities toward <span class="elsevierStyleItalic">F&#46; oxysporium</span> and <span class="elsevierStyleItalic">R&#46; solani</span> &#40;higher fungi rich in chitin in their cell wall&#41;&#44; and <span class="elsevierStyleItalic">P&#46; ultimum</span> &#40;a lower fungus rich in cellulose in its cell wall&#41;&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">Isolates from the four soils were present in each of the three antifungal groups&#44; except for isolates from RSYP and B1O&#46; RSYP isolates showed strong antagonism against <span class="elsevierStyleItalic">R&#46; solani</span> or <span class="elsevierStyleItalic">F&#46; oxysporum</span>&#44; but none of them showed antagonism against both fungi while B1O isolates did not show strong antagonism&#44; only against <span class="elsevierStyleItalic">P&#46; ultimum</span>&#46;</p><p id="par0140" class="elsevierStylePara elsevierViewall">In our study of anti-yeast activity&#44; diverse results were observed&#46; Isolate R1O41 showed the strongest antagonism in both media compared to the remaining antagonistic isolates evidencing the potent broad-spectrum antifungal activities and their complex strategies to control the two antifungal drug-resistant <span class="elsevierStyleItalic">Candida albicans</span> strains&#46; A significant difference &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41; in anti-yeast activities between media within the same antagonist was observed in some of them&#44; which may be influenced by diverse factors that involved the synthesis of antibiotics and other secondary metabolites in culture media&#46; Data previously published showed that medium composition and their concentrations are strongly related to antibiotic production&#46;<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">22</span></a> Simply metabolizable carbon sources such as glucose generally repress production of many antibiotics&#44; particularly when they are used as the sole carbon source&#46;<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">25</span></a> Studies on fermentation media show that polysaccharides are generally the best carbon sources for antibiotic production as they support a slow growth rate which is desirable for antibiotic production&#46;<a class="elsevierStyleCrossRefs" href="#bib0195"><span class="elsevierStyleSup">6&#44;22&#44;25</span></a> Moreover&#44; there are also cases where glucose is an excellent carbon source for antibiotic production&#46; It has been reported that dextrose was a great carbon source for the antibiotic production of <span class="elsevierStyleItalic">Streptomyces kanamyceticus</span> M27&#46;<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">18</span></a></p><p id="par0145" class="elsevierStylePara elsevierViewall">Nitrogen is another component strongly related to antibiotic synthesis&#46; As with the carbon component&#44; simply metabolizable nitrogen sources usually decrease antibiotic production while complex nitrogen sources such as yeast extract&#44; malt extract and soybean meal can increase the production of antibiotics produced by streptomycetes&#44; which can be attributed to the slow decomposition of these compounds in the medium&#46;<a class="elsevierStyleCrossRefs" href="#bib0255"><span class="elsevierStyleSup">18&#44;22</span></a></p><p id="par0150" class="elsevierStylePara elsevierViewall">In addition to nutrients&#44; microbial interactions can regulate the production of antibiotics and other secondary metabolites&#46; In such interactions&#44; production of secondary metabolites can facilitate communication&#44; but can also act as defensive molecules which help microorganisms to defend themselves against competitors&#46;<a class="elsevierStyleCrossRef" href="#bib0320"><span class="elsevierStyleSup">31</span></a> In our study of the anti-yeast bioassay&#44; the signaling between the yeast and each antagonist must be unique in each case and may be reflected in some antifungal activities or the lack of them&#59; for example&#44; B1Y14 showed antifungal activity against <span class="elsevierStyleItalic">C&#46; albicans</span> ATCC MY-204276 in both media&#59; however&#44; no activity was detected against <span class="elsevierStyleItalic">C&#46; albicans</span> ATCC 44373&#46; Similarly&#44; other isolates&#44; R1O44 and B1010&#44; showed activity against <span class="elsevierStyleItalic">C&#46; albicans</span> ATCC 44373 in YDA&#59; however&#44; no activity was observed against <span class="elsevierStyleItalic">C&#46; albicans</span> ATCC MY-204276&#46;</p><p id="par0155" class="elsevierStylePara elsevierViewall">In some studies&#44; mainly members of the genus <span class="elsevierStyleItalic">Streptomyces</span> were detected by screening for antifungal actinomycetes from the rhizosphere soil of different plants including medicinal and forage plants&#46;<a class="elsevierStyleCrossRefs" href="#bib0235"><span class="elsevierStyleSup">14&#44;33</span></a> Similarly&#44; our results of the 16S rDNA analyses revealed that most of the selected antifungal isolates belong to the genus <span class="elsevierStyleItalic">Streptomyces</span>&#44; except for eleven isolates that showed a best identity match with actinobacterium 17a-5&#46; After actinobacterium 17a-5&#44; <span class="elsevierStyleItalic">Streptomyces luteogriseus</span> and <span class="elsevierStyleItalic">S&#46; tuirus</span> followed in the search&#44; each with lower scores and percent sequence identity &#40;data not shown&#41;&#44; suggesting that those eleven isolates may be members of a new <span class="elsevierStyleItalic">Streptomyces</span> species not yet identified&#46; Furthermore&#44; the phylogenetic analysis showed that all the isolates identified with actinobacterium 17a-5 were in a very defined terminal clade&#46; On the other hand&#44; all the antifungal isolates with 98&#37; identity with <span class="elsevierStyleItalic">Streptomyces</span> sp&#46; were in one of the major clusters of the neighbor-joining tree&#59; they are potentially novel species&#59; however&#44; further analysis are required to determine that&#46; In addition&#44; almost all the strains of antifungal group one&#44; which also exhibited anti-<span class="elsevierStyleItalic">Candida</span> activity &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#44; were in close proximity on the phylogenetic tree &#40;R1O41&#44; R1O4-2&#44; R1O7-2&#44; R1O4-3-2 B1Y54&#44; R1Y10&#44; R1Y9 and B1O9&#41;&#44; suggesting the presence of a potential clade of strong antifungal <span class="elsevierStyleItalic">Streptomyces</span> with potential novel bioactive metabolites&#46; The isolate denominated R1O41&#44; isolated from RSOP&#44; seems to be a novel actinomycete isolate with strong broad antifungal activity against the three phytopathogens and the two drug-resistant <span class="elsevierStyleItalic">Candida</span> strains&#44; showing a great potential that can be exploited for use in agriculture and medicine&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Conclusions</span><p id="par0160" class="elsevierStylePara elsevierViewall">Our study showed that the rhizosphere soil of sagebrush plants may preferentially favor antifungal actinomycete colonizers&#44; particularly plants with high rhizosphere effect&#46; The isolates with strong antifungal activities were identified as members of the genus <span class="elsevierStyleItalic">Streptomyces</span>&#46; A relationship was detected by phylogenetic analysis between the genetic relatedness and the antifungal activities of those actinomycetes exhibiting strong antifungal activity against all the filamentous fungi tested along with anti-<span class="elsevierStyleItalic">Candida</span> activity&#46; Finally&#44; the rhizosphere soil of <span class="elsevierStyleItalic">A&#46; tridentata</span> seems to be a great source of novel actinomycetes with strong antifungal activity that can be exploited for use in agriculture and medicine&#46;</p></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Conflict of interest</span><p id="par0165" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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        7 => array:3 [
          "identificador" => "sec0040"
          "titulo" => "Results"
          "secciones" => array:3 [
            0 => array:2 [
              "identificador" => "sec0045"
              "titulo" => "Selected isolates"
            ]
            1 => array:2 [
              "identificador" => "sec0050"
              "titulo" => "Anti-Candida activities"
            ]
            2 => array:2 [
              "identificador" => "sec0055"
              "titulo" => "16S rDNA sequence analysis"
            ]
          ]
        ]
        8 => array:2 [
          "identificador" => "sec0060"
          "titulo" => "Discussion"
        ]
        9 => array:2 [
          "identificador" => "sec0065"
          "titulo" => "Conclusions"
        ]
        10 => array:2 [
          "identificador" => "sec0070"
          "titulo" => "Conflict of interest"
        ]
        11 => array:2 [
          "identificador" => "xack641884"
          "titulo" => "Acknowledgements"
        ]
        12 => array:1 [
          "titulo" => "References"
        ]
      ]
    ]
    "pdfFichero" => "main.pdf"
    "tienePdf" => true
    "fechaRecibido" => "2021-08-31"
    "fechaAceptado" => "2022-05-02"
    "PalabrasClave" => array:2 [
      "en" => array:1 [
        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Keywords"
          "identificador" => "xpalclavsec1588123"
          "palabras" => array:5 [
            0 => "Antimicrobial activities"
            1 => "Desert plants"
            2 => "Rhizosphere soil"
            3 => "Anti-<span class="elsevierStyleItalic">Candida</span> activity"
            4 => "<span class="elsevierStyleItalic">Streptomyces</span>"
          ]
        ]
      ]
      "es" => array:1 [
        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Palabras clave"
          "identificador" => "xpalclavsec1588124"
          "palabras" => array:5 [
            0 => "Actividades antimicrobianas"
            1 => "Plantas des&#233;rticas"
            2 => "Suelo rizosf&#233;rico"
            3 => "Actividad anti-Candida"
            4 => "<span class="elsevierStyleItalic">Streptomyces</span>"
          ]
        ]
      ]
    ]
    "tieneResumen" => true
    "highlights" => array:2 [
      "titulo" => "Highlights"
      "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall"><ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005"><span class="elsevierStyleLabel">&#8226;</span><p id="par0005" class="elsevierStylePara elsevierViewall">Rhizosphere soil of sagebrush is a source of novel strong antifungal actinomycetes&#46;</p></li><li class="elsevierStyleListItem" id="lsti0010"><span class="elsevierStyleLabel">&#8226;</span><p id="par0010" class="elsevierStylePara elsevierViewall">Strong antifungal <span class="elsevierStyleItalic">Streptomyces</span> can be exploited for agriculture and medicine&#46;</p></li><li class="elsevierStyleListItem" id="lsti0015"><span class="elsevierStyleLabel">&#8226;</span><p id="par0015" class="elsevierStylePara elsevierViewall">A clade of antifungal <span class="elsevierStyleItalic">Streptomyces</span> is revealed by analyzing the16S rDNA sequences&#46;</p></li></ul></p></span>"
    ]
    "resumen" => array:2 [
      "en" => array:2 [
        "titulo" => "Abstract"
        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Diverse habitats have been screened for novel antimicrobial actinomycetes&#44; while others remain unexplored&#46; In this study&#44; we analyzed the bioactivities of actinomycetes cultured from rhizosphere soils of the desert plant <span class="elsevierStyleItalic">Artemisia tridentata</span> and the nearby bulk soils&#46; Actinomycetes were screened for antifungal and antibacterial activities toward a panel of plant pathogens&#59; all comparisons were between activities of rhizosphere soil isolates toward those of its counterpart bulk soil&#46; A selected group of the strongest antifungal isolates were also tested against two antifungal-drug resistant strains of <span class="elsevierStyleItalic">Candida albicans</span>&#46; 16S rDNA partial sequences and phylogenetic analysis of isolates that showed broad-spectrum antifungal activities were performed&#46; Forty-two out of 200 and two soil isolated actinomycetes were selected for their strong antifungal activities&#46; The highest proportion of isolates &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41; from rhizosphere soil of an old plant showed antagonism against gram-positive bacteria &#40;0&#46;483 and 0&#46;224 proportions against <span class="elsevierStyleItalic">Bacillus subtilis</span> and <span class="elsevierStyleItalic">Rathayibacter tritici</span>&#44; respectively&#41;&#44; and phytopathogenic fungi &#40;0&#46;259&#44; 0&#46;431&#44; and 0&#46;345 proportions against <span class="elsevierStyleItalic">Fusarium oxysporum&#44; Rhizoctonia solani</span> and <span class="elsevierStyleItalic">Pythium ultimum</span>&#44; respectively&#41;&#44; while the highest antagonism against the gram-negative bacteria predominated in isolates from the bulk soils&#46; Isolates from a rhizosphere soil of a young plant were characterized for strong antagonist activities against <span class="elsevierStyleItalic">Fusarium oxysporum</span> &#40;0&#46;333 proportion&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#46; Phylogenetic analysis of 16S rDNA sequences showed that isolates that exhibited strong antifungal activity were genetically similar&#46; We conclude that the rhizosphere soil of <span class="elsevierStyleItalic">A&#46; tridentata</span> is an excellent source for discovery of actinomycetes with potentially novel antifungal compounds&#46;</p></span>"
      ]
      "es" => array:2 [
        "titulo" => "Resumen"
        "resumen" => "<span id="abst0015" class="elsevierStyleSection elsevierViewall"><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">En la b&#250;squeda de actinomicetos antimicrobianos se han estudiado diversos h&#225;bitats&#44; pero muchos permanecen a&#250;n sin explorar&#46; En este estudio analizamos las actividades biol&#243;gicas de cultivos de actinomicetos provenientes de suelos rizosf&#233;ricos de la planta des&#233;rtica <span class="elsevierStyleItalic">Artemisia</span><span class="elsevierStyleItalic">tridentata</span> y de suelos no asociados a sus ra&#237;ces&#46; Los actinomicetos fueron seleccionados por sus actividades antif&#250;ngicas y antibacterianas contra un panel de pat&#243;genos de plantas&#46; Todas las comparaciones fueron entre las actividades de los aislados rizosf&#233;ricos y aquellas de los aislados no asociados a las ra&#237;ces&#46; Un grupo selecto de los aislados con las mayores actividades antif&#250;ngicas fueron tambi&#233;n evaluados contra 2 cepas de <span class="elsevierStyleItalic">Candida albicans</span> resistentes a antif&#250;ngicos&#46; Se realiz&#243; la secuenciaci&#243;n parcial del ARNr 16S y el an&#225;lisis filogen&#233;tico de los aislados que mostraron actividades antif&#250;ngicas de amplio espectro&#46; Se seleccionaron 42 de 202 actinomicetos aislados por sus fuertes actividades antif&#250;ngicas&#46; La mayor proporci&#243;n de aislados de suelo rizosf&#233;rico de plantas viejas mostraron antagonismo contra bacterias gram positivas y hongos fitopat&#243;genos &#40;proporciones de 0&#44;259&#59; 0&#44;431 y 0&#44;345 contra <span class="elsevierStyleItalic">Fusarium oxysporum&#44; Rhizoctonia solani</span> y <span class="elsevierStyleItalic">Pythium ultimum</span>&#44; respectivamente&#41;&#44; mientras que la mayor actividad antag&#243;nica contra las bacterias gram negativas predominaron en aislados de suelo no asociado a ra&#237;ces&#46; Los aislados de suelo rizosf&#233;rico de plantas j&#243;venes se caracterizaron por una fuerte actividad antag&#243;nica contra <span class="elsevierStyleItalic">F&#46; oxysporum</span> &#40;proporci&#243;n de 0&#44;333&#44; p<span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#44;05&#41;&#46; El an&#225;lisis filogen&#233;tico de secuencias del ADNr 16S mostr&#243; que los aislados que presentaron fuerte actividad antif&#250;ngica fueron gen&#233;ticamente similares&#46; Concluimos que el suelo rizosf&#233;rico de <span class="elsevierStyleItalic">A&#46;</span><span class="elsevierStyleItalic">tridentata</span> es una fuente excelente para el descubrimiento de actinomicetos productores de compuestos antif&#250;ngicos potencialmente novedosos&#46;</p></span>"
      ]
    ]
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      0 => array:3 [
        "etiqueta" => "1"
        "nota" => "<p class="elsevierStyleNotepara" id="npar0015">Permanent address&#58; Universidad Aut&#243;noma de Chihuahua&#44; Facultad de Ciencias Agrotecnol&#243;gicas&#44; Ciudad Universitaria S&#47;N Campus 1&#44; Chihuahua&#44; Chih 31310&#44; Mexico&#46;</p>"
        "identificador" => "fn0005"
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        "figura" => array:1 [
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        "descripcion" => array:1 [
          "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Anti-<span class="elsevierStyleItalic">Candida</span> activity of selected actinomycetes from four soils of a sagebrush habitat in two different media&#46; The data presented are the means of quadruplicate measurements of inhibition zones&#46; Bars represent their standard deviations&#46; Mean values with equal letters are not statistically different &#40;Tukey&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41; within each isolate&#46;</p>"
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        "figura" => array:1 [
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        "descripcion" => array:1 [
          "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Phylogenetic relationship of partial 16S rRNA gene sequences of 41 streptomycetes in a neighbor-joining tree&#46; L and P indicate branches that were also found when we used the maximum-likelihood and maximum-parsimony methods&#44; respectively&#59; the asterisks indicate branches recovered with all three methods&#46; The numbers at the nodes indicate the level of bootstrap support based on a neighbor-joining analysis&#59; only values that were &#62;50&#37; are given&#46; The scale bar indicates 0&#46;01 substitutions per nucleotide position&#46; The bracket &#40;A&#41; indicates the isolates with antimicrobial activity against filamentous fungi and <span class="elsevierStyleItalic">C&#46; albicans</span> and &#40;B&#41; indicates the clade of isolates identified with actinobacterium 17a-5&#46;</p>"
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        "etiqueta" => "Table 1"
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          "leyenda" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">The data presented are proportions of the active isolates with respect to the total population in each soil &#40;RSYP&#44; n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>27&#59; B1Y&#44; n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>74&#59; RSOP&#44; n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>58&#59; B1O&#44; n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>43&#41;&#46; RSYP and RSOP are rhizosphere soils from a young and old sagebrush plants&#44; respectively&#59; B1Y and B1O are their counterpart bulk soils&#44; respectively&#46; Different letters within a column indicate significant difference at <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#46; All comparisons are based on logit transformations &#91;&#40;<span class="elsevierStyleItalic">P</span>&#47;1<span class="elsevierStyleHsp" style=""></span>&#8722;P&#41;&#44; where <span class="elsevierStyleItalic">P</span> is the transformation values of active isolates&#93;&#46;</p>"
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                  \t\t\t\t" scope="col">Soil samples&nbsp;\t\t\t\t\t\t\n
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          "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Distribution of antifungal activities in four soils of a sagebrush habitat&#46;</p>"
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          "leyenda" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">The data presented are proportions of the active isolates with respect to the total population in each soil &#40;RSYP&#44; n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>27&#59; B1Y&#44; n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>74&#59; RSOP&#44; n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>58&#59; B1O&#44; n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>43&#41;&#46; RSYP and RSOP are rhizosphere soils from a young and an old sagebrush plants respectively&#59; B1Y and B1O are the counterpart bulk soils respectively&#46; Different letters within a column indicate a significant difference at <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#46; All comparisons are based on logit transformations&#46;</p>"
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                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces</span> sp&#46; LK4-2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">680&#47;687 &#40;98&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629029&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>R1O7-2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces</span> sp&#46; LK4-2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">709&#47;716 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629030&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>B1O9&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces erumpens</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">771&#47;773&#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629048&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>B1O10&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces luteogriseus</span>Actinobacterium 17a-5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">768&#47;772 &#40;99&#37;&#41;765&#47;768 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629049&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " colspan="4" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " colspan="4" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Group 2</span></td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>R1Y11&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Actinobacterium 17a-5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">740&#47;742 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629038&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>R1Y25&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces griseocarneus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">771&#47;782 &#40;98&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629039&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>B1Y4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Actinobacterium 17a-5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">767&#47;771 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629053&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>B1Y37&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces ciscaucasicus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">732&#47;732 &#40;100&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629054&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>B1Y40&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Actinobacterium 17a-5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">740&#47;742 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629055&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>B1Y42&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Stretomyces</span> sp&#46; KN-0647&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">724&#47;730 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629056&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>B1Y43&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Stretomyces</span> sp&#46; KN-0647&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">726&#47;732 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629057&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>R1O4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Actinobacterium 17a-5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">767&#47;770 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629034&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>R1O23&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Actinobacterium 17a-5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">737&#47;739 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629035&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>R1O24&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces cyaneus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">703&#47;704 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629036&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>R1O46&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces turgidiscabies</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">681&#47;686 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629037&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " colspan="4" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " colspan="4" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Group 3</span></td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>B1Y2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces</span> sp&#46; IM-8062&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">763&#47;769 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629062&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>B1Y3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Actinobacterium 17a-5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">733&#47;733 &#40;100&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629063&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>B1Y16&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces</span> sp&#46; KN-0647&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">730&#47;736 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629064&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>B1Y21&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces</span> sp&#46; IM-6899&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">729&#47;740 &#40;98&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629065&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>B1Y33&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces</span> sp&#46; KN-0647&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">746&#47;752 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629066&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>B1Y48&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces</span> sp&#46; IM-8062&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">683&#47;688 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629067&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>B1Y64&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces platensis</span><span class="elsevierStyleItalic">S&#46; catenulae</span><span class="elsevierStyleItalic">S&#46; tubercidicus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">765&#47;778 &#40;98&#37;&#41;765&#47;778 &#40;98&#37;&#41;765&#47;778 &#40;98&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629068&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>R1O3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces</span> sp&#46; Sm22<span class="elsevierStyleItalic">Streptomyces</span> sp&#46; IM-6784&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">657&#47;661 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629040&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>R1O31&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces</span> sp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">709&#47;718 &#40;98&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629041&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>R1O195&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Actinobacterium 17a-5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">737&#47;739 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629047&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>R1O37&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces lincolnensis</span><span class="elsevierStyleItalic">Streptomyces ciscaucasicus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">721&#47;723 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629042&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>R1O45&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">S&#46; peruviensis</span><span class="elsevierStyleItalic">S&#46; ciscaucasicus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">706&#47;713 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629043&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>R1O49&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptomyces africanus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">655&#47;655 &#40;100&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629044&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>R1O54&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Actinobacterium 17a-5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">661&#47;661 &#40;100&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629045&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>R1O59&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Actinobacterium 17a-5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">722&#47;722 &#40;100&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">DQ629046&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="middle"><span class="elsevierStyleHsp" style=""></span>B1O22&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="middle"><span class="elsevierStyleItalic">Streptomyces coerulescens</span><span class="elsevierStyleItalic">Streptomyces bellus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="middle">749&#47;750 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="middle">DQ629058&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="middle"><span class="elsevierStyleHsp" style=""></span>B1O26&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="middle"><span class="elsevierStyleItalic">Streptomyces</span> sp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="middle">745&#47;750 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="middle">DQ629059&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="middle"><span class="elsevierStyleHsp" style=""></span>B1O27&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="middle"><span class="elsevierStyleItalic">Streptomyces</span> sp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="middle">693&#47;697 &#40;99&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="middle">DQ629060&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="middle"><span class="elsevierStyleHsp" style=""></span>B1O32&nbsp;\t\t\t\t\t\t\n
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          "en" => "<p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">Blast search of partial sequences of the 16s RNA gene of selected isolates&#46;</p>"
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es en pt

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