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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Fungal-Bacterial Networks in the <italic>Populus</italic> Rhizobiome Are Impacted by Soil Properties and Host Genotype</title><author><name sortKey="Bonito, Gregory" sort="Bonito, Gregory" uniqKey="Bonito G" first="Gregory" last="Bonito">Gregory Bonito</name><affiliation><nlm:aff id="aff1"><institution>Department of Plant Soil and Microbial Sciences, Michigan State University</institution>,<addr-line>East Lansing, MI</addr-line>,<country>United States</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution>Great Lakes Bioenergy Research Center</institution>,<addr-line>East Lansing, MI</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Benucci, Gian Maria Niccol" sort="Benucci, Gian Maria Niccol" uniqKey="Benucci G" first="Gian Maria Niccol" last="Benucci">Gian Maria Niccol Benucci</name><affiliation><nlm:aff id="aff1"><institution>Department of Plant Soil and Microbial Sciences, Michigan State University</institution>,<addr-line>East Lansing, MI</addr-line>,<country>United States</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution>Great Lakes Bioenergy Research Center</institution>,<addr-line>East Lansing, MI</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Hameed, Khalid" sort="Hameed, Khalid" uniqKey="Hameed K" first="Khalid" last="Hameed">Khalid Hameed</name><affiliation><nlm:aff id="aff3"><institution>Department of Biology, Duke University</institution>,<addr-line>Durham, NC</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Weighill, Deborah" sort="Weighill, Deborah" uniqKey="Weighill D" first="Deborah" last="Weighill">Deborah Weighill</name><affiliation><nlm:aff id="aff4"><institution>Biosciences Division, Oak Ridge National Laboratory</institution>,<addr-line>Oak Ridge, TN</addr-line>,<country>United States</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>The Bredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee, Knoxville</institution>,<addr-line>Knoxville, TN</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Jones, Piet" sort="Jones, Piet" uniqKey="Jones P" first="Piet" last="Jones">Piet Jones</name><affiliation><nlm:aff id="aff4"><institution>Biosciences Division, Oak Ridge National Laboratory</institution>,<addr-line>Oak Ridge, TN</addr-line>,<country>United States</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>The Bredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee, Knoxville</institution>,<addr-line>Knoxville, TN</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Chen, Ko Hsuan" sort="Chen, Ko Hsuan" uniqKey="Chen K" first="Ko-Hsuan" last="Chen">Ko-Hsuan Chen</name><affiliation><nlm:aff id="aff6"><institution>Department of Soil and Water Sciences, University of Florida</institution>,<addr-line>Quincy, FL</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Jacobson, Daniel" sort="Jacobson, Daniel" uniqKey="Jacobson D" first="Daniel" last="Jacobson">Daniel Jacobson</name><affiliation><nlm:aff id="aff4"><institution>Biosciences Division, Oak Ridge National Laboratory</institution>,<addr-line>Oak Ridge, TN</addr-line>,<country>United States</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>The Bredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee, Knoxville</institution>,<addr-line>Knoxville, TN</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Schadt, Christopher" sort="Schadt, Christopher" uniqKey="Schadt C" first="Christopher" last="Schadt">Christopher Schadt</name><affiliation><nlm:aff id="aff4"><institution>Biosciences Division, Oak Ridge National Laboratory</institution>,<addr-line>Oak Ridge, TN</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Vilgalys, Rytas" sort="Vilgalys, Rytas" uniqKey="Vilgalys R" first="Rytas" last="Vilgalys">Rytas Vilgalys</name><affiliation><nlm:aff id="aff3"><institution>Department of Biology, Duke University</institution>,<addr-line>Durham, NC</addr-line>,<country>United States</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">30984119</idno><idno type="pmc">6450171</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6450171</idno><idno type="RBID">PMC:6450171</idno><idno type="doi">10.3389/fmicb.2019.00481</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">000799</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000799</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Fungal-Bacterial Networks in the <italic>Populus</italic> Rhizobiome Are Impacted by Soil Properties and Host Genotype</title><author><name sortKey="Bonito, Gregory" sort="Bonito, Gregory" uniqKey="Bonito G" first="Gregory" last="Bonito">Gregory Bonito</name><affiliation><nlm:aff id="aff1"><institution>Department of Plant Soil and Microbial Sciences, Michigan State University</institution>,<addr-line>East Lansing, MI</addr-line>,<country>United States</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution>Great Lakes Bioenergy Research Center</institution>,<addr-line>East Lansing, MI</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Benucci, Gian Maria Niccol" sort="Benucci, Gian Maria Niccol" uniqKey="Benucci G" first="Gian Maria Niccol" last="Benucci">Gian Maria Niccol Benucci</name><affiliation><nlm:aff id="aff1"><institution>Department of Plant Soil and Microbial Sciences, Michigan State University</institution>,<addr-line>East Lansing, MI</addr-line>,<country>United States</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution>Great Lakes Bioenergy Research Center</institution>,<addr-line>East Lansing, MI</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Hameed, Khalid" sort="Hameed, Khalid" uniqKey="Hameed K" first="Khalid" last="Hameed">Khalid Hameed</name><affiliation><nlm:aff id="aff3"><institution>Department of Biology, Duke University</institution>,<addr-line>Durham, NC</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Weighill, Deborah" sort="Weighill, Deborah" uniqKey="Weighill D" first="Deborah" last="Weighill">Deborah Weighill</name><affiliation><nlm:aff id="aff4"><institution>Biosciences Division, Oak Ridge National Laboratory</institution>,<addr-line>Oak Ridge, TN</addr-line>,<country>United States</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>The Bredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee, Knoxville</institution>,<addr-line>Knoxville, TN</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Jones, Piet" sort="Jones, Piet" uniqKey="Jones P" first="Piet" last="Jones">Piet Jones</name><affiliation><nlm:aff id="aff4"><institution>Biosciences Division, Oak Ridge National Laboratory</institution>,<addr-line>Oak Ridge, TN</addr-line>,<country>United States</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>The Bredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee, Knoxville</institution>,<addr-line>Knoxville, TN</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Chen, Ko Hsuan" sort="Chen, Ko Hsuan" uniqKey="Chen K" first="Ko-Hsuan" last="Chen">Ko-Hsuan Chen</name><affiliation><nlm:aff id="aff6"><institution>Department of Soil and Water Sciences, University of Florida</institution>,<addr-line>Quincy, FL</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Jacobson, Daniel" sort="Jacobson, Daniel" uniqKey="Jacobson D" first="Daniel" last="Jacobson">Daniel Jacobson</name><affiliation><nlm:aff id="aff4"><institution>Biosciences Division, Oak Ridge National Laboratory</institution>,<addr-line>Oak Ridge, TN</addr-line>,<country>United States</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>The Bredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee, Knoxville</institution>,<addr-line>Knoxville, TN</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Schadt, Christopher" sort="Schadt, Christopher" uniqKey="Schadt C" first="Christopher" last="Schadt">Christopher Schadt</name><affiliation><nlm:aff id="aff4"><institution>Biosciences Division, Oak Ridge National Laboratory</institution>,<addr-line>Oak Ridge, TN</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Vilgalys, Rytas" sort="Vilgalys, Rytas" uniqKey="Vilgalys R" first="Rytas" last="Vilgalys">Rytas Vilgalys</name><affiliation><nlm:aff id="aff3"><institution>Department of Biology, Duke University</institution>,<addr-line>Durham, NC</addr-line>,<country>United States</country></nlm:aff></affiliation></author></analytic><series><title level="j">Frontiers in Microbiology</title><idno type="eISSN">1664-302X</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Plant root-associated microbial symbionts comprise the plant rhizobiome. These microbes function in provisioning nutrients and water to their hosts, impacting plant health and disease. The plant microbiome is shaped by plant species, plant genotype, soil and environmental conditions, but the contributions of these variables are hard to disentangle from each other in natural systems. We used bioassay common garden experiments to decouple plant genotype and soil property impacts on fungal and bacterial community structure in the <italic>Populus</italic> rhizobiome. High throughput amplification and sequencing of 16S, ITS, 28S and 18S rDNA was accomplished through 454 pyrosequencing. Co-association patterns of fungal and bacterial taxa were assessed with 16S and ITS datasets. Community bipartite fungal-bacterial networks and PERMANOVA results attribute significant difference in fungal or bacterial communities to soil origin, soil chemical properties and plant genotype. Indicator species analysis identified a common set of root bacteria as well as endophytic and ectomycorrhizal fungi associated with <italic>Populus</italic> in different soils. However, no single taxon, or consortium of microbes, was indicative of a particular <italic>Populus</italic> genotype. Fungal-bacterial networks were over-represented in arbuscular mycorrhizal, endophytic, and ectomycorrhizal fungi, as well as bacteria belonging to the orders Rhizobiales, Chitinophagales, Cytophagales, and Burkholderiales. These results demonstrate the importance of soil and plant genotype on fungal-bacterial networks in the belowground plant microbiome.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Agler, M T" uniqKey="Agler M">M. T. Agler</name></author><author><name sortKey="Ruhe, J" uniqKey="Ruhe J">J. Ruhe</name></author><author><name sortKey="Kroll, S" uniqKey="Kroll S">S. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Microbiol</journal-id><journal-id journal-id-type="iso-abbrev">Front Microbiol</journal-id><journal-id journal-id-type="publisher-id">Front. Microbiol.</journal-id><journal-title-group><journal-title>Frontiers in Microbiology</journal-title></journal-title-group><issn pub-type="epub">1664-302X</issn><publisher><publisher-name>Frontiers Media S.A.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">30984119</article-id><article-id pub-id-type="pmc">6450171</article-id><article-id pub-id-type="doi">10.3389/fmicb.2019.00481</article-id><article-categories><subj-group subj-group-type="heading"><subject>Microbiology</subject><subj-group><subject>Original Research</subject></subj-group></subj-group></article-categories><title-group><article-title>Fungal-Bacterial Networks in the <italic>Populus</italic> Rhizobiome Are Impacted by Soil Properties and Host Genotype</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Bonito</surname><given-names>Gregory</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="corresp" rid="c001"><sup>*</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/637581/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Benucci</surname><given-names>Gian Maria Niccolò</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/703241/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Hameed</surname><given-names>Khalid</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/702507/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Weighill</surname><given-names>Deborah</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref><xref ref-type="aff" rid="aff5"><sup>5</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/436495/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Jones</surname><given-names>Piet</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref><xref ref-type="aff" rid="aff5"><sup>5</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/537637/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Chen</surname><given-names>Ko-Hsuan</given-names></name><xref ref-type="aff" rid="aff6"><sup>6</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/672043/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Jacobson</surname><given-names>Daniel</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref><xref ref-type="aff" rid="aff5"><sup>5</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/274608/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Schadt</surname><given-names>Christopher</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/23200/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Vilgalys</surname><given-names>Rytas</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/14990/overview"></uri></contrib></contrib-group><aff id="aff1"><sup>1</sup><institution>Department of Plant Soil and Microbial Sciences, Michigan State University</institution>,<addr-line>East Lansing, MI</addr-line>,<country>United States</country></aff><aff id="aff2"><sup>2</sup><institution>Great Lakes Bioenergy Research Center</institution>,<addr-line>East Lansing, MI</addr-line>,<country>United States</country></aff><aff id="aff3"><sup>3</sup><institution>Department of Biology, Duke University</institution>,<addr-line>Durham, NC</addr-line>,<country>United States</country></aff><aff id="aff4"><sup>4</sup><institution>Biosciences Division, Oak Ridge National Laboratory</institution>,<addr-line>Oak Ridge, TN</addr-line>,<country>United States</country></aff><aff id="aff5"><sup>5</sup><institution>The Bredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee, Knoxville</institution>,<addr-line>Knoxville, TN</addr-line>,<country>United States</country></aff><aff id="aff6"><sup>6</sup><institution>Department of Soil and Water Sciences, University of Florida</institution>,<addr-line>Quincy, FL</addr-line>,<country>United States</country></aff><author-notes><fn fn-type="edited-by"><p>Edited by: Gustavo Henrique Goldman, University of São Paulo, Brazil</p></fn><fn fn-type="edited-by"><p>Reviewed by: Devin Coleman-Derr, United States Department of Agriculture, United States; Ye Deng, Research Center for Eco-Environmental Sciences (CAS), China</p></fn><corresp id="c001">*Correspondence: Gregory Bonito, <email>bonito@msu.edu</email></corresp><fn fn-type="other" id="fn002"><p>This article was submitted to Fungi and Their Interactions, a section of the journal Frontiers in Microbiology</p></fn></author-notes><pub-date pub-type="epub"><day>29</day><month>3</month><year>2019</year></pub-date><pub-date pub-type="collection"><year>2019</year></pub-date><volume>10</volume><elocation-id>481</elocation-id><history><date date-type="received"><day>02</day><month>11</month><year>2018</year></date><date date-type="accepted"><day>25</day><month>2</month><year>2019</year></date></history><permissions><copyright-statement>Copyright © 2019 Bonito, Benucci, Hameed, Weighill, Jones, Chen, Jacobson, Schadt and Vilgalys.</copyright-statement><copyright-year>2019</copyright-year><copyright-holder>Bonito, Benucci, Hameed, Weighill, Jones, Chen, Jacobson, Schadt and Vilgalys</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p></license></permissions><abstract><p>Plant root-associated microbial symbionts comprise the plant rhizobiome. These microbes function in provisioning nutrients and water to their hosts, impacting plant health and disease. The plant microbiome is shaped by plant species, plant genotype, soil and environmental conditions, but the contributions of these variables are hard to disentangle from each other in natural systems. We used bioassay common garden experiments to decouple plant genotype and soil property impacts on fungal and bacterial community structure in the <italic>Populus</italic> rhizobiome. High throughput amplification and sequencing of 16S, ITS, 28S and 18S rDNA was accomplished through 454 pyrosequencing. Co-association patterns of fungal and bacterial taxa were assessed with 16S and ITS datasets. Community bipartite fungal-bacterial networks and PERMANOVA results attribute significant difference in fungal or bacterial communities to soil origin, soil chemical properties and plant genotype. Indicator species analysis identified a common set of root bacteria as well as endophytic and ectomycorrhizal fungi associated with <italic>Populus</italic> in different soils. However, no single taxon, or consortium of microbes, was indicative of a particular <italic>Populus</italic> genotype. Fungal-bacterial networks were over-represented in arbuscular mycorrhizal, endophytic, and ectomycorrhizal fungi, as well as bacteria belonging to the orders Rhizobiales, Chitinophagales, Cytophagales, and Burkholderiales. These results demonstrate the importance of soil and plant genotype on fungal-bacterial networks in the belowground plant microbiome.</p></abstract><kwd-group><kwd><italic>Populus deltoides</italic></kwd><kwd>fungal communities</kwd><kwd>bacterial communities</kwd><kwd>microbiome</kwd><kwd>NGS sequencing</kwd><kwd>arbuscular mycorrhizal fungi</kwd><kwd>endophytes</kwd><kwd>rhizosphere</kwd></kwd-group><counts><fig-count count="10"></fig-count><table-count count="1"></table-count><equation-count count="0"></equation-count><ref-count count="68"></ref-count><page-count count="21"></page-count><word-count count="0"></word-count></counts></article-meta></front><body><sec><title>Introduction</title><p>Living plants, soils and microbiota interact and function in a zone known as the root microbiome (<xref rid="B45" ref-type="bibr">Lundberg et al., 2012</xref>). This zone of biological activity is characterized by elevated rates of respiration, nutrient turnover, and carbon sequestration, highlighting its importance to the functioning of terrestrial ecosystems. Root microbiomes continue to be characterized for model and non-model plant species. While rooting, growth, and disease susceptibility are under strong genetic controls in plants (<xref rid="B36" ref-type="bibr">Jorge et al., 2005</xref>; <xref rid="B68" ref-type="bibr">Zalesny et al., 2005</xref>; <xref rid="B56" ref-type="bibr">Raj et al., 2011</xref>), discerning the contribution of host genotype relevant to other ecologically factors in a community context remains a formidable challenge (<xref rid="B45" ref-type="bibr">Lundberg et al., 2012</xref>; <xref rid="B52" ref-type="bibr">Peiffer et al., 2013</xref>; <xref rid="B58" ref-type="bibr">Shakya et al., 2013</xref>; <xref rid="B25" ref-type="bibr">Fonseca-García et al., 2016</xref>; <xref rid="B16" ref-type="bibr">Cregger et al., 2018</xref>; <xref rid="B24" ref-type="bibr">Fitzpatrick et al., 2018</xref>). Here we report on common garden “trap-plant” experiments aimed at disentangling effects of host genotype and soil origin on networks of fungal and bacterial communities that comprise the root microbiome of <italic>Populus deltoides.</italic></p><p><italic>Populus deltoides</italic> (Poplar/Eastern Cottonwood) is a woody plant that grows along rivers and waterways across much of central and eastern North America (<xref rid="B13" ref-type="bibr">Braatne et al., 2006</xref>; <xref rid="B30" ref-type="bibr">Gottel et al., 2011</xref>). <italic>Populus deltoides</italic> is particularly well adapted to riparian habitats. This tree species functions in a pioneer and late-stage niche along river banks, establishing from seed or from branches that fall, root and become partially buried during flooding events (<xref rid="B58" ref-type="bibr">Shakya et al., 2013</xref>). The disruption of natural flooding cycles may limit the ability of <italic>P. deltoides</italic> to naturally establish (<xref rid="B39" ref-type="bibr">Kranjcec et al., 1998</xref>); however, once established <italic>P. deltoides</italic> may persist for centuries. Recruitment processes for <italic>P. deltoides</italic> root-microbiome associates, and their stability and change over time and space, are still not well understood.</p><p>Recent efforts have been made to characterize the root microbiome of <italic>Populus</italic> using high throughput sequencing (<xref rid="B30" ref-type="bibr">Gottel et al., 2011</xref>; <xref rid="B17" ref-type="bibr">Danielsen et al., 2012</xref>; <xref rid="B58" ref-type="bibr">Shakya et al., 2013</xref>; <xref rid="B16" ref-type="bibr">Cregger et al., 2018</xref>). <xref rid="B30" ref-type="bibr">Gottel et al. (2011)</xref> and <xref rid="B58" ref-type="bibr">Shakya et al. (2013)</xref> used multiple rDNA regions to target fungal and bacterial rhizosphere and endosphere communities from adult <italic>P. deltoides</italic> trees in their natural habitats. Distinct habitat, seasonal, and geographic differences in the endosphere and rhizosphere communities of <italic>P. deltoides</italic> were found, particularly among bacterial communities. Similar results were reported for pine, agave and <italic>Arabidopsis</italic> (<xref rid="B45" ref-type="bibr">Lundberg et al., 2012</xref>; <xref rid="B61" ref-type="bibr">Talbot et al., 2014</xref>; <xref rid="B25" ref-type="bibr">Fonseca-García et al., 2016</xref>). Host species has also been found to impact the structure of fungi and bacteria within the plant rhizobiome, indicating plant genetic effects (<xref rid="B69" ref-type="bibr">Bonito et al., 2014</xref>). The impact of plant genotype on its microbiome appears to be much more important in aboveground tissues (e.g., leaves, stems), compared to in belowground root tissues (<xref rid="B6" ref-type="bibr">Bálint et al., 2013</xref>; <xref rid="B16" ref-type="bibr">Cregger et al., 2018</xref>). However, differentiating the effects of soil properties from those of host plant genotype still has not been sufficiently addressed.</p><p>In this study, two experiments were conducted. The first experiment assessed differences in fungal and bacterial community structure and networks among multiple <italic>Populus</italic> genotypes grown in common soils. The second experiment assessed the influence of fungal and bacterial community structure in the absence of host genetic factors, by growing a single <italic>P. deltoides</italic> genotype in multiple soils in a common environment. In this work, we define the rhizobiome to include fungi and bacteria intimately associated with root tissues, including the rhizoplane and root endosphere, but excluding soil particles associated with the rhizosphere. We used these data to compare levels of α-diversity within genotypes, β-diversity between <italic>Populus</italic> genotypes, and β-diversity levels between a single <italic>Populus</italic> genotype grown in soils originating from different locales. We assessed the fungal-bacterial network structure of root-associated fungal-bacterial communities to determine OTU co-occurance patterns. This research provides a foundation for understanding multi-Kingdom microbial interactions within plant rhizobiomes.</p></sec><sec sec-type="materials|methods" id="s1"><title>Materials and Methods</title><sec><title>Trap-Plant Bioassays</title><p>Trap-plant bioassay experiments were designed to discern effects of host genotype and soil origin on root microbiomes of <italic>Populus.</italic> In these assays, plant roots serve as “bait” for compatible microbial communities in test soils. Microbes compatible with the plant host persist and grow during the experiment to the point of detection through environmental DNA sequencing, as previously described (<xref rid="B69" ref-type="bibr">Bonito et al., 2014</xref>). Field soils from natural <italic>P. deltoides</italic> riparian habitats were collected along the Caney Fork River in TN and the Yadkin River in NC, sites previously sampled by <xref rid="B58" ref-type="bibr">Shakya et al. (2013)</xref>. Upon collection, fresh soils were refrigerated and used within 5 days by diluting 50% with washed and sterilized fine quartz sand, and homogenized by mixing.</p></sec><sec><title>Experiment 1: Effect of <italic>Populus</italic> Genotype on the Root Microbiome</title><p>To examine effects of host genotype on the <italic>Populus deltoides</italic> rhizobiome we used four genotypes that were available: <italic>P. deltoides</italic> D110, D117, D133, and <italic>P. deltoides</italic> × <italic>P. trichocarpa</italic> hybrid 93-968. Winter-harvested cuttings were stored at 4°C for 2 months; 3–4 internode segments of each cutting were rooted by placing in sterile water for 4 weeks under 12 h light. After primary leaves emerged, rooted cuttings were transplanted in triplicate into D40 Deepot cone-tainer Deepots (Stuewe & Sons, Inc.) containing soils collected under <italic>P. deltoides</italic> sites (NC1 and NC2) along the Yadkin River in North Carolina (<xref rid="B58" ref-type="bibr">Shakya et al., 2013</xref>). Uninoculated control cuttings (genotypes D110, D112, D113) were planted in sterilized sand alongside experimental treatments. All plants were grown under uniform conditions for the duration of the experiment.</p></sec><sec><title>Experiment 2: Effect of Soil Origin on the Root Microbiome of a Single <italic>Populus</italic> Genotype</title><p>A single <italic>Populus</italic> genotype (D124) was planted into 8 soils (TNPo1, TNPo3, TNPo4, TNPo5, TNPo6, TNPo7 TNPo8, TNPo11) collected from along the Caney Fork River in Tennessee (TN), United States, to remove host genotype effects on the development of root-associated microbial communities (<xref ref-type="supplementary-material" rid="SM9">Supplementary Table S1</xref>). This genotype was chosen because it roots well, and we had a sufficient number of cuttings available for the experimental design. Four replicate cuttings were planted into each of the eight soils, totaling 32 plants. Plants were grown in uniform conditions for the duration of the experiment.</p></sec><sec><title>Soil Collection</title><p>An auger core was used to collect samples of approximately 10 L of soil to a depth of 15 cm from each of the ten field sites. Soils were air-dried in paper bags for 1 week and sieved through a 2-mm mesh to homogenize and remove roots. Physical and chemical soil characteristics were determined by the University of Georgia’s Agricultural and Environmental Services Laboratory (AESL)<sup><xref ref-type="fn" rid="fn01">1</xref></sup> on composited soil samples from three cores at each site (presented in <xref ref-type="supplementary-material" rid="SM9">Supplementary Table S1</xref>).</p><p>Before planting, soils were mixed to a concentration of 50% by volume into fine textured quartz sand to facilitate water drainage. Incorporated sand had been washed and autoclaved twice over a 2-day period prior to mixing with field soil. Cleanly raised plants were planted into mixed soils using cone-tainer “D-pots” (Steuwe and Sons, Corvallis, OR, United States), which were hung in racks to prevent microbial spread between pots via water. A layer of sterile sand (1-cm) was spread across the surface of each planting to prevent aerial cross-contamination of soils between pots.</p></sec><sec><title>Planting Seedings and Cuttings</title><p><italic>Populus</italic> cuttings (listed above) were stored at 4<sup>°</sup>C in double ziplock bags until use. Before rooting, cuttings were washed in 5% Tween 20 solution to remove adhering particles, the surface was sterilized by submerging in 6% H<sub>2</sub>O<sub>2</sub> for 10 min and then triple rinsed in tap water. The bottom half of each cutting was soaked in tap water for 24 h in darkness to initiate rooting before planting.</p></sec><sec><title>Growth Conditions, Measurements and Sample Preparations</title><p>Plants were grown in the Duke Phytotron under uniform conditions of 18 h days with light levels of 400 μmol/m<sup>2</sup>/s and 6 h nights. Day temperatures were 21.1°C, with humidity of 60%; night temperatures were 15.6°C with 85% humidity. Plants were watered daily and fertilized biweekly with half-strength Hoagland solution. Plants were removed from the growth chamber every month to remove fallen leaf material. At these times, racks were reordered to reduce block effects. Plants were grown for 118 days (Experiment 1) and 165 days (Experiment 2). After this period, plant height was measured as the sum of their shoot length(s) measured from the tip of the apical bud to where it emerged from the rooted cutting.</p><p><italic>Populus</italic> roots were harvested using a retractable razor blade to cut and remove a vertical section of approximately half of the root system. The razor was rinsed in ethanol and flamed between samples to minimize cross-contamination. Soil particles associated with the rhizosphere were removed by placing sampled roots in ziplock bags and washing multiple times with Tween 20. A fine spray of tap water was used to remove any additional adhered soil particles.</p></sec><sec><title>DNA Extractions and Fungal and Bacterial PCR Amplification</title><p>Harvested root samples were freeze-dried and ground to a powder in a 2 ml Eppendorf tube using a bead beater and 3 large steel beads. DNA was extracted from ∼500 mg of pulverized root tissue from each plant using the CTAB-based chloroform-isoamyl alcohol (24:1) extraction method (<xref rid="B26" ref-type="bibr">Gardes and Bruns, 1993</xref>). To help improve DNA quality, a second sodium acetate ethanol precipitation was done. DNA pellets were eluted in 100 μl of TE buffer. Dilutions of DNA made at 1:3 were used for PCR.</p><p>We performed 454 sequencing of amplicon libraries with FLX titanium chemistry and a Roche genome sequencer (Indianapolis, IN, United States). For the genotype experiment, four loci were amplified from each sample: 16S rDNA (V4 region) to target bacteria utilizing primers designed to exclude plastid and mitochondrial organelles (<xref rid="B34" ref-type="bibr">Hodkinson et al., 2012</xref>); ITS rDNA to target fungi; 28S rDNA as a second fungal marker, and 18S rDNA to target Glomeromycotina (i.e., arbuscular mycorrhiza taxa) with taxon-specific primers (<xref rid="B41" ref-type="bibr">Lee et al., 2008</xref>). A reverse primer (AMrev1_GB) was designed to be specific to AMF and to shorten the amplicon length to be more compatible with 454 sequencing (<xref rid="B69" ref-type="bibr">Bonito et al., 2014</xref>). Primer pairs and their sequences were modified to contain the 454 A and B primer, with one of 96 10-bp DNA barcodes on the A primer (see <xref ref-type="supplementary-material" rid="SM10">Supplementary Table S2</xref> for complete primer sequence information). The 18S region was not sequenced for the soil origin experiment (Experiment 2).</p><p>PCR was carried out in 25 μl reactions using High Fidelity PCR buffer (Invitrogen, Carlsbad, CA, United States), 0.2 mM (each) deoxynucleoside triphosphates (dNTPs), 2 mM MgCl<sub>2</sub>, 0.6 mM forward and reverse primers, 2.5 mg/ml bovine serum albumin (BSA) and 1 unit of Platinum <italic>Taq</italic> (Invitrogen, Carlsbad, CA, United States). To each 25 μl reaction mixture, 1 μl of template DNA (diluted 1:3 in 1x Tris buffer) was added. Thermocycler settings were 5 min at 95°C, then 30 cycles of 95°C for 1 min, 52–62°C for 45 s (annealing temperature differed for each primer pair) and 72°C for 1 min, with a final extension for 7 min at 72°C. Annealing temperatures were optimized with gradient PCR for each primer pair to maximize target amplification and minimize primer dimer. Annealing temperatures were as follows: 58°C for ITS, 62°C for 28S, 52°C for 16S and 55°C for 18S. PCR products were visualized through gel electrophoresis. PCR products from each experiment were then normalized separately by locus (ITS, 28S, 18S, or 16S) to achieve equal molar concentrations of target PCR product for each sample. Pooled PCR products were normalized by molarity into a single library for each experiment such that the library for Experiment 1 included ITS, 16S, 18S, and 28S amplicons, and the library for experiment two included ITS, 16S, and 28S amplicons. Unincorporated primers, dNTPs and primer dimers were removed through two successive rounds with the Agencourt AMPure purification system (Beckman Coulter, Danvers, MA, United States). Product purity and concentration were checked with an Agilent 2100 Bioanalyzer (Santa Clara, CA, United States). Emulsion reactions were performed in paired samples containing two sample PCR amplicons that were matched for template quantity and quality. The two prepared libraries were each loaded into 1/8 of a 454 plate and sequencing was performed on the GS-FLX with Titanium series reagents (Roche), sequencing from the ‘A’ adaptor only (Lib-L) according to manufacturer’s recommended conditions. Sequence data generated during this study have been submitted to GenBank’s sequence read archive under the study accession number <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="SRP106691">SRP106691</ext-link>.</p></sec><sec><title>Assessments of Arbuscular Mycorrhizal Fungal Diversity</title><p>Arbuscular mycorrhizal fungi (AMF) are an important and distinct function guild in the <italic>Populus</italic> rhizobiome (<xref rid="B43" ref-type="bibr">Lodge, 1989</xref>). To propagate and assess the diversity of <italic>Populus</italic> associated AMF, bioassay plant roots and spores extracted from them were propagated onto sorghum, a host that has been extensively used for maintaining AMF isolates (<xref rid="B57" ref-type="bibr">Selvakumar et al., 2016</xref>). After 5 months of growth, sorghum roots were harvested and AMF spores were extracted, sorted morphologically and assessed phylogenetically via 18S rDNA sequencing and analysis (described in Supplementary File <xref ref-type="supplementary-material" rid="SM18">S1</xref>).</p></sec><sec><title>Bioinformatic Analyses</title><p>Raw reads (i.e., <italic>sff</italic>, standard flowgram format) were demultiplexed, cleaned of short and low-quality reads with the spilt_libraries.py script in <italic>QIIME</italic> v1.9 (<xref rid="B14" ref-type="bibr">Caporaso et al., 2010</xref>). Default parameters were used with these exceptions: homopolymers were not allowed to exceed 10 bases in length and sequences < 150 and > 1000 bp in length were excluded. Read denoising was done with <italic>ampliconnoise</italic> (<xref rid="B54" ref-type="bibr">Quince et al., 2011</xref>) and primer sequences were removed with <italic>cutadapt</italic> (<xref rid="B47" ref-type="bibr">Martin, 2011</xref>). For 16S reads, the most hypervariable region was extracted using <italic>metaxa</italic> (<xref rid="B8" ref-type="bibr">Bengtsson et al., 2011</xref>). All the reads were then filtered, trimmed and clustered into OTUs at 97% similarity (unless otherwise noted) using the UPARSE pipeline in USEARCH (<xref rid="B21" ref-type="bibr">Edgar, 2010</xref>, <xref rid="B22" ref-type="bibr">2013</xref>). OTUs representative sequences of ITS and 16S rDNA were then identified taxonomically inside <italic>QIIME</italic> (with 0.8 bootstrap confidence) with <italic>parallel_assign_taxonomy_rdp.py</italic> script that uses the naïve Bayesian RDP classifier (<xref rid="B65" ref-type="bibr">Wang et al., 2007</xref>) against the UNITE sequence reference database (<xref rid="B38" ref-type="bibr">Kõljalg et al., 2013</xref>).</p><p>We chose to sequence fungal 28S rDNA (LSU) because this region (a) can be aligned across the Kingdom Fungi, allowing for the phylogenetic placement of unknown/understudied taxa, (b) amplifies and sequences easily, and (c) includes variable domains informative at the genus (and sometimes species) level for identification of taxa. 28S rDNA sequences were processed with QIIME (<xref rid="B14" ref-type="bibr">Caporaso et al., 2010</xref>). Chimeric sequences were removed with USEARCH (<xref rid="B21" ref-type="bibr">Edgar, 2010</xref>). Sequences were mapped according to the eukaryotic SILVA LSU reference database that was parsed locally to include fungal and non-fungal representative sequences. Sequences mapping to non-fungal taxa were filtered from the dataset. OTUs were assigned by clustering the sequences at 99% similarity, as recommended by <xref rid="B69" ref-type="bibr">Bonito et al. (2014)</xref>. Taxonomy was assigned to representative sequences with a 28S rDNA reference sequences database compiled from the curated RDP dataset. Taxonomies of abundant taxa were verified by comparing sequences to the NCBI database with the BLAST algorithm. Neighbor joining trees were built using PAUP 4.0 (<xref rid="B60" ref-type="bibr">Swofford, 2003</xref>). Trees were analyzed using the unweighted UniFrac metric calculated with Fast UniFrac (<xref rid="B31" ref-type="bibr">Hamady et al., 2009</xref>) and samples were categorized according to sample host genotype and soil origin. The UniFrac significance test allows one to examine differences among treatments based solely on branch length data while the P-test is based on a phylogenetic tree to test whether two environments are significantly different by using parsimony-based scoring significances (<xref rid="B44" ref-type="bibr">Lozupone and Knight, 2005</xref>). Both of these tests were used to assess for phylogenetic differences in the fungal communities associated with different host genotypes and soils based on 1,000 permutations and calculated with the Fast UniFrac as implemented in QIIME.</p><p>We sequenced 18S rDNA (SSU) with the aim of selectively detecting Glomeromycotina (AMF). Chimeric sequences were first removed with USEARCH (<xref rid="B21" ref-type="bibr">Edgar, 2010</xref>). The sequences were then mapped to a version of the eukaryotic SILVA SSU reference database, which includes fungal and non-fungal representative sequences. Sequences not mapping to Glomeromycotina from the dataset were excluded. Remaining OTUs were assigned by clustering the sequences at 98% similarity following <xref rid="B69" ref-type="bibr">Bonito et al. (2014)</xref>. To ascertain the phylogenetic placement of these OTUs a representative sequence from each OTU was aligned with sequences belonging to reference taxa from across the Glomeromycotina (<xref rid="B40" ref-type="bibr">Kruger et al., 2012</xref>) with the alignment program MUSCLE (<xref rid="B20" ref-type="bibr">Edgar, 2004</xref>). Phylogenetic analyses were carried out in PAUP 4.0 (<xref rid="B60" ref-type="bibr">Swofford, 2003</xref>) as previously described.</p></sec><sec><title>Statistical Analysis</title><p>Rarefaction curves were assessed for each sample (<xref ref-type="supplementary-material" rid="SM1">Supplementary Figure S1</xref>) and OTU table values were normalized though Hellinger transformation (<xref rid="B42" ref-type="bibr">Legendre and Gallagher, 2001</xref>; <xref rid="B53" ref-type="bibr">Pezzolla et al., 2015</xref>). Principal coordinates analysis (PCoA) was used to represent inter-sample Bray Curtis dissimilarity. The ordinate function of the R (<xref rid="B55" ref-type="bibr">R Core Team, 2018</xref>) package “phyloseq” (<xref rid="B49" ref-type="bibr">McMurdie and Holmes, 2013</xref>) was used to produce graphs. Permutational multivariate analysis of variance (PERMANOVA; <xref rid="B3" ref-type="bibr">Anderson, 2001</xref>) was used to test the null hypothesis of no differences among <italic>a priori</italic> defined groups with the function adonis in the “vegan” R package (<xref rid="B51" ref-type="bibr">Oksanen et al., 2015</xref>) with 9999 permutations. Permutational analysis of multivariate dispersions (<xref rid="B4" ref-type="bibr">Anderson, 2006</xref>) was used to test for variance heterogeneity between the <italic>a priori</italic> selected groups using the function betadisper in the “vegan” R package. A taxon-group association analysis was used to assess the degree of preference (at <italic>P</italic> ≤ 0.05, after FDR correction) of each OTU for the target group in relation to other groups using the multipath function of the “indicspecies” R package (<xref rid="B18" ref-type="bibr">De Cáceres et al., 2010</xref>). Bar plots of relative abundance taxonomic distribution were calculated using the R package RAM (<xref rid="B15" ref-type="bibr">Chen et al., 2016</xref>).</p></sec><sec><title>Experiment 1: Effect of <italic>Populus</italic> Genotype on the Root Microbiome</title><p>OTU networks have been used in the study of plant and microbial communities (<xref rid="B46" ref-type="bibr">Maestre et al., 2009</xref>; <xref rid="B23" ref-type="bibr">Faust and Raes, 2016</xref>). We constructed microbial OTU networks in order to investigate the effect of the <italic>Populus</italic> genotype on the root microbiome. Data were represented in the form of a Hellinger-transformed OTU matrix in which rows represented OTUs and columns represented samples. Networks were visualized in Cytoscape (<xref rid="B59" ref-type="bibr">Shannon et al., 2003</xref>) (Supplementary File <xref ref-type="supplementary-material" rid="SM19">S2</xref>).</p></sec><sec><title>Raw Bipartite and Sample Correlation Networks</title><p>Bipartite networks were constructed from the OTU matrix by representing OTUs and samples as nodes and connecting an OTU node to a sample node if the OTU was present in that sample. Sample similarity networks were constructed by calculating the similarity between all pairs of columns (samples) of the OTU matrix and then constructing a Maximum Spanning Tree (MST). Two similarity metrics were used, the Pearson correlation coefficient and Proportional Similarity (<xref rid="B10" ref-type="bibr">Bloom, 1981</xref>; <xref rid="B66" ref-type="bibr">Weighill and Jacobson, 2017</xref>). Pearson correlation coefficients were calculated using the mcxarray and mcxdump programs from the MCL-Edge software package (<xref rid="B62" ref-type="bibr">Van Dongen, 2008</xref>) available from <ext-link ext-link-type="uri" xlink:href="http://micans.org/mcl/">http://micans.org/mcl/</ext-link>. MST construction was performed by converting Pearson correlations to distance measures by taking (1 – pearson) and then making use of the Dijkstra minimum spanning tree algorithm in the Graph Perl module (Jarkko Hietaniemi)<sup><xref ref-type="fn" rid="fn02">2</xref></sup>. Resulting MSTs were visualized as networks in Cytoscape (<xref rid="B59" ref-type="bibr">Shannon et al., 2003</xref>) and sample nodes were colored according to genotype and soil.</p></sec><sec><title>OTU-Sample Enrichment Networks (Hypergraphs)</title><p>OTU-Sample enrichment networks (hypergraphs) were constructed using the Fisher Exact Test, similar to the enrichment networks/hypergraphs constructed previously (<xref rid="B67" ref-type="bibr">Weighill and Jacobson, 2015</xref>). The samples for Experiment 1 were separated into control samples and non-control samples (including NC1 and NC2), resulting in a matrix M in which rows represented OTUs and columns represented non-control samples. For each non-control sample and for each OTU, the contingency table (<xref ref-type="supplementary-material" rid="SM2">Supplementary Figure S2</xref>) was constructed and the Fisher Exact test was performed on the contingency table. The Text::NSP::Measures::2D::Fisher Perl module (<xref rid="B7" ref-type="bibr">Banerjee and Pedersen, 2003</xref>), available from Comprehensive Perl Archive Network (CPAN) at <ext-link ext-link-type="uri" xlink:href="http://search.cpan.org/dist/Text-NSP/lib/Text/NSP/Measures/2D/Fisher.pm">http://search.cpan.org/dist/Text-</ext-link><ext-link ext-link-type="uri" xlink:href="http://search.cpan.org/dist/Text-NSP/lib/Text/NSP/Measures/2D/Fisher.pm">xNSP/lib/Text/NSP/Measures/2D/Fisher.pm</ext-link>, was used to calculate the Fisher Exact Test. False discovery rate correction of <italic>p</italic>-values (<xref rid="B9" ref-type="bibr">Benjamini and Hochberg, 1995</xref>) at a level of 0.01 determined which OTUs were enriched in which samples. An enrichment network was constructed by connecting a sample node to an OTU node if that OTU was significantly enriched in that sample. Similarly, enrichment of OTUs in control samples was performed.</p></sec><sec><title>Binned Enrichment Networks</title><p>We constructed binned enrichment networks to determine which OTUs were enriched in which genotypes, separately within each soil. Within each soil (i.e., Control, NC1, and NC2) the data were binned by genotype. This resulted in a separate matrix for each soil in which rows represented OTUs, columns represented genotypes and each entry represented the collective amount of that OTU present in that genotype in that particular soil. Enrichment and FDR correction were performed separately for each soil. For each OTU and each genotype within a particular soil, the Fisher Exact test was calculated similarly as described above, and FDR correction at a level of 0.01 was performed. This was repeated for each soil. An enrichment network was then constructed representing the enrichment of OTUs in genotypes within each soil.</p></sec><sec><title>Community Construction</title><p>Communities of OTUs were constructed as follows: OTUs with less than 3 non-zero values were removed, and the Pearson correlation between all pairs of remaining OTUs was calculated across all samples of experiment 1 focused on plant genotype impacts on the plant microbiome. This made use of the ‘mcxarray’ and ‘mcxdump’ programs from the MCL-Edge software package (<xref rid="B62" ref-type="bibr">Van Dongen, 2008</xref>) available from <ext-link ext-link-type="uri" xlink:href="http://micans.org/mcl/">http://micans.org/mcl/</ext-link>. An absolute threshold of 0.6 was set, and numerous topology measures were calculated for the correlation network with the NetworkAnalyzer Cytoscape app (<xref rid="B5" ref-type="bibr">Assenov et al., 2008</xref>). Communities were constructed by clustering the network with the Markov Cluster (MCL) algorithm (<xref rid="B62" ref-type="bibr">Van Dongen, 2008</xref>), with an inflation value of 2.5 using the cluster Maker Cytoscape app (<xref rid="B50" ref-type="bibr">Morris et al., 2011</xref>) (Supplementary File <xref ref-type="supplementary-material" rid="SM20">S3</xref>).</p></sec><sec><title>Differential Analysis</title><p>The differential relative abundance was estimated using the Fold Change Rank Order Statistic (FCROS) package in R (<xref rid="B19" ref-type="bibr">Dembélé and Kastner, 2014</xref>). To control for the bias of rare OTUs we required that an OTU’s abundance measurement be present in at least 3 of the samples. A variation stabilization transformation, as suggested in <xref rid="B48" ref-type="bibr">McMurdie and Holmes (2014)</xref>, was applied by performing a log transform. A quantile-normalization procedure (<xref rid="B2" ref-type="bibr">Amaratunga and Cabrera, 2001</xref>) was applied to transformed abundance values to account for noise between sample replicates, while maintaining variation between sample classes. The normalized matrix of values was analyzed using FCROS for differential relative abundance of OTUs between sample classes. A <italic>p</italic>-value threshold of 0.05 was applied and using <italic>f</italic>-value output of FCROS, OTUs with a probability of over/under abundance greater than 0.9, respectively, was maintained for further analysis.</p></sec><sec><title>Experiment 2: Effect of Soil Origin on the Root Microbiome of a Single <italic>Populus</italic> Genotype</title><p>A similar series of analyses were performed for Experiment 2 as described for Experiment 1. Data were first summarized in the form of a Hellinger-transformed OTU matrix in which rows represented OTUs and columns represented samples of <italic>Populus</italic> roots grown in different soil samples.</p></sec><sec><title>Sample Similarity and OTU-Sample Enrichment Networks (Hypergraphs)</title><p>Sample similarity MSTs were constructed for the samples in Experiment 2 using the Pearson correlation coefficient and proportional similarity, in a similar manner as described for Experiment 1. The resulting MSTs were represented as networks in Cytoscape (<xref rid="B59" ref-type="bibr">Shannon et al., 2003</xref>) and nodes were colored based on various properties. OTU-sample enrichment networks representing the enrichment of OTUs in samples were constructed similarly as described in Experiment 1, making use of the Fisher Exact test and false discovery rate correction.</p></sec><sec><title>Community Construction</title><p>OTU communities were constructed for Experiment 2 in a similar manner as described for Experiment 1, by removing OTUs with fewer than 3 non-zero values across samples, calculating the Pearson correlation between all pairs of OTUs across all Experiment 2 samples, applying an absolute threshold of 0.6 and clustering with MCL. Network topology measures were again calculated using the NetworkAnalyzer Cytoscape app (<xref rid="B50" ref-type="bibr">Morris et al., 2011</xref>).</p></sec><sec><title>Soil Property Correlation</title><p>A soil property similarity network was constructed by calculating the Pearson correlation coefficient between all pairs of soil properties across all soils in Experiment 2. This made use of the mcxarray and mcxdump programs from the MCL-Edge software package (<xref rid="B62" ref-type="bibr">Van Dongen, 2008</xref>) available from <ext-link ext-link-type="uri" xlink:href="http://micans.org/mcl/">http://micans.org/mcl/</ext-link>. A maximum spanning tree was constructed from the resulting network using the Dijkstra algorithm in the Graph Perl module (Jarkko Hietaniemi)<sup><xref ref-type="fn" rid="fn03">3</xref></sup>. In addition, the Pearson correlation between all soil properties and OTUs was calculated. After applying a threshold of |Pearson|≥ 0.6, soil properties correlating with OTUs were mapped onto the corresponding communities.</p></sec><sec><title>Differential Analysis</title><p>Significant differences in the root microbiome under the effect of different soils were assessed through differential analysis, similar to Experiment 1. Filtering out rare OTUs that only occur in fewer than 3 samples, a variance stabilization transformation and quantile normalization were performed to mitigate noise between sample replicates. Relative abundances of OTUs in the respective sample classes, different soils, were then compared using FCROS. A <italic>p</italic>-value threshold of 0.05 and <italic>f</italic>-value threshold of 0.9 were applied.</p></sec><sec><title>Plant Growth Analyses</title><p>Effects of eight different soils on the growth of a single cottonwood genotype (D124) were assessed with a one-way ANOVA using R version 2.15.2. Normality was checked graphically with normal quantile–quantile plots and computationally with the Shapiro–Wilk test of normality. Homoscedasticity was assessed by calculating the variances of the data grouped by the levels of each factor and comparing the values to see if any were more than twice any of the others. Since this was often the case, a Bartlett test of homoscedasticity was used, which evaluates the null hypothesis of equal variances. Differences between means in ANOVAs were checked <italic>a posteriori</italic> with the Tukey HSD test. Growth data were right-skewed slightly, so they were log-transformed to meet the assumptions of normality and homoscedasticity. Chi-square tests were used to check whether differences in OTUs detected between different host genotypes and soils were significant.</p></sec></sec><sec><title>Results</title><sec><title>PCR and 454 Sequencing</title><p>Sixty-four plants were grown and harvested for the two experiments described above. Two 454 libraries were prepared with amplicon pools from multiplexed samples and were successfully sequenced. The first library was prepared for the host genotype experiment and included amplicon pools of ITS, 18S, 28S and 16S rDNA from 34 samples and resulted in 113,869 reads. After error-correction and filtering for quality, length and chimeras 14,847 sequences of ITS, 16,671 of 18S (374 of which mapped to Glomeromycotina), 44,817 sequences of 28S and 9,822 sequences of 16S were recovered. The 34 samples had between 68 and 1950 reads per sample per locus (mean = 643). The second library was prepared for the soil origin experiment and included amplicon pools of ITS, 28S, and 16S rDNA from 30 samples and resulted in 129,674 reads. After error-correction and filtering for quality, length and chimeras, 44,938 sequences of ITS, 44,155 of 28S and 21,948 sequences of 16S were recovered. One sample failed to amplify and/or sequence well and was excluded from further analyses. The remaining 29 samples had between 346 and 4065 reads per sample per locus (mean = 1276).</p></sec><sec><title>Experiment 1: Effect of <italic>Populus</italic> Genotype on the Root Microbiome</title><p>Significant differences in fungal root-associated communities could be attributed to host genotype, but were not associated with specific OTUs. The most abundant fungal OTUs (based on ITS1) belonged to Chaetothyriales sp.1, <italic>Cylindrocarpon pauciseptatum</italic> ( = <italic>Ilyonectria</italic>), <italic>Fusarium oxysporum</italic>, Pezizaceae sp. 1 and <italic>Inocybe curvipes</italic> and were detected on all genotypes assayed in this experiment (<xref ref-type="fig" rid="F1">Figure 1A</xref>). ITS1 data revealed 161 OTUs in this dataset. Only 5–8 unique OTUs were detected on any particular genotype, and 99% of these were rare—that is detected < 10 times and on fewer than half of the replicates (<xref ref-type="supplementary-material" rid="SM11">Supplementary Table S3</xref>). PCoA of ITS and 28S rDNA showed that samples were separated by soil, rather than by genotype, in ordinal space (<xref ref-type="fig" rid="F2">Figure 2A,B</xref>). No significant differences in OTU richness or UniFrac distances based on 28S were realized between the tested genotypes. PERMANOVA of the fungal ITS (<italic>R</italic><sup>2</sup> = 0.13, <italic>p</italic> = 0.157, perm = 9999) and 16S (<italic>R</italic><sup>2</sup> = 0.13, <italic>p</italic> = 0.10, perm = 9999) data showed no significant interactions between soil and plant genotype. Therefore, genotype effects were tested separately on the two soils used in this experiment. For the NC1 soil, significant effects of plant genotype were found for fungal (<italic>R</italic><sup>2</sup> = 0.40, <italic>p</italic> = 0.040, perm = 9999) and bacterial communities (<italic>R</italic><sup>2</sup> = 0.37, <italic>p</italic> = 0.038, perm = 9999). Multivariate dispersion (variances) of sample groups did not differ statistically for fungi (<italic>F</italic> = 0.245, <italic>p</italic> = 0.868) or bacteria (<italic>F</italic> = 0.565, <italic>p</italic> = 0.625), respectively, validating results of PERMANOVA. However, for the NC2 soil no significant genotype effects were found for either fungal (<italic>R</italic><sup>2</sup> = 0.252, <italic>p</italic> = 0.140, perm = 9999) or bacterial communities (<italic>R</italic><sup>2</sup> = 0.365, <italic>p</italic> = 0.166, perm = 9999). Significant effects of soil origin were found for both fungal (<italic>R</italic><sup>2</sup> = 0.123, <italic>p</italic> = 0.0008, perm = 9999) and bacterial communities (<italic>R</italic><sup>2</sup> = 0.134, <italic>p</italic> = 0.0001, perm = 9999). No difference in group dispersion was detected for fungal (<italic>F</italic> = 1.30, <italic>p</italic> = 0.269) or bacterial (<italic>F</italic> = 0.497, <italic>p</italic> = 0.493) communities. All <italic>Populus</italic> genotypes tested harbored a diverse community of root-associated bacteria dominated by <italic>Niastella</italic>, Micromonosporineae, and <italic>Bradyrhizobium</italic> (<xref ref-type="supplementary-material" rid="SM3">Supplementary Figure S3</xref>).</p><fig id="F1" position="float"><label>FIGURE 1</label><caption><p>Rank abundance of fungi in <italic>Populus</italic> roots based on ITS rDNA amplicon sequencing. <bold>(A)</bold> Across different genotypes (Experiment 1); <bold>(B)</bold> Across different soils (Experiment 2); <bold>(C)</bold> In uninoculated control plants.</p></caption><graphic xlink:href="fmicb-10-00481-g001"></graphic></fig><fig id="F2" position="float"><label>FIGURE 2</label><caption><p>Principle coordinates analysis (PCoA) showing beta-diversity of fungal and prokaryotic communities in the rhizosphere of <italic>Populus</italic>. <bold>(A)</bold> Fungal communities in different soils (Experiment 2); <bold>(B)</bold> Fungal communities in different <italic>Populus</italic> genotypes (Experiment 1); <bold>(C)</bold> Prokaryotic communities in different soils (Experiment 2); <bold>(D)</bold> Prokaryotic communities in different <italic>Populus</italic> genotypes (Experiment 1).</p></caption><graphic xlink:href="fmicb-10-00481-g002"></graphic></fig><p>Fungal and bacterial communities of the root microbiome between treatment and control plants grown without soil inoculum differed drastically. Control plants largely clustered together in PCoA (<xref ref-type="fig" rid="F2">Figure 2B,C</xref>). In general, uninoculated control plants were colonized by a lower diversity of bacteria than plants grown in soil. <italic>Flavobacterium</italic>, Streptomycineae, Rhizobiaceae, and <italic>Stenotrophomonas</italic> were most abundant on control plants. Eight fungal species belonging to the genera <italic>Phoma, Acremonium, Plectosphaerella, Alternaria, Ceratobasidium, Paraphoma, Cadophora</italic>, and <italic>Fusarium</italic> were most abundant in the control plants, independent of plant genotype (<xref ref-type="fig" rid="F1">Figure 1C</xref>). Of these, only <italic>Fusarium oxysporum</italic> and <italic>Paraphoma radicina</italic> were detected at modest levels in both control and treatment plants. Bacterial communities in the controls were all varied across genotype but different between cuttings planted in soil (<xref ref-type="fig" rid="F2">Figure 2</xref>).</p></sec><sec><title>Indicator Species Analysis</title><p>No indicator species of fungi or bacteria were found to be associated to any specific genotype (<xref rid="T1" ref-type="table">Table 1</xref>). However, two dominant fungal OTUs, Chaetothyriales sp., and <italic>Cylindrocarpon pauciseptatum</italic>, were significantly associated with the two NC soils used in Experiment 1. OTUs belonging to <italic>Polyscytalum pustulans</italic>, Pleosporales sp., <italic>Sarocladium strictum, Cladosporium ramotenellum</italic>, <italic>Lecythophora fasciculata</italic>, and <italic>Cadophora luteo-olivacea</italic> were found to be significantly associated with uninoculated control plants. Likewise, numerous bacterial OTUs were associated with control plants (<xref rid="T1" ref-type="table">Table 1</xref>). Conversely, bacteria belonging to Micromonosporaceae, Chitinophagaceae, and Oxalobacteraceae were significantly associated with experimental soils, but not uninoculated control plants.</p><table-wrap id="T1" position="float"><label>Table 1</label><caption><p>Indicator species analysis of fungal and bacteria operational taxonomic units (OTUs) that are statistically associated with a particular <italic>Populus</italic> genotype.</p></caption><table frame="hsides" rules="groups" cellspacing="5" cellpadding="5"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1">Soil fungi</th><th valign="top" align="left" rowspan="1" colspan="1">OTU</th><th valign="top" align="center" rowspan="1" colspan="1">Treatment</th><th valign="top" align="left" rowspan="1" colspan="1"><italic>p</italic>-value after FDR</th><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_52</td><td valign="top" align="center" rowspan="1" colspan="1">TNP11</td><td valign="top" align="left" rowspan="1" colspan="1">0.00891</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_52</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Basidiomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Agaricomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Thelephorales</td><td valign="top" align="left" rowspan="1" colspan="1">Thelephoraceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_40</td><td valign="top" align="center" rowspan="1" colspan="1">TNPo1</td><td valign="top" align="left" rowspan="1" colspan="1">0.026</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_40</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Pezizomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Pezizales</td><td valign="top" align="left" rowspan="1" colspan="1">Pyronemataceae</td><td valign="top" align="left" rowspan="1" colspan="1">Unidentified</td><td valign="top" align="left" rowspan="1" colspan="1">Pyronemataceae sp</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_118</td><td valign="top" align="center" rowspan="1" colspan="1">TNPo3</td><td valign="top" align="left" rowspan="1" colspan="1">0.0078</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_118</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Basidiomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Agaricomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Agaricales</td><td valign="top" align="left" rowspan="1" colspan="1">Niaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Flagelloscypha</td><td valign="top" align="left" rowspan="1" colspan="1">Flagelloscypha minutissima</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_30</td><td valign="top" align="center" rowspan="1" colspan="1">TNPo6</td><td valign="top" align="left" rowspan="1" colspan="1">0.0468</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_30</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Basidiomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Agaricomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Agaricales</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_51</td><td valign="top" align="center" rowspan="1" colspan="1">TNPo6</td><td valign="top" align="left" rowspan="1" colspan="1">0.0481</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_51</td><td valign="top" align="left" rowspan="1" colspan="1">FungiPMI</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Sordariomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">unclassified</td><td valign="top" align="left" rowspan="1" colspan="1">Unclassified</td><td valign="top" align="left" rowspan="1" colspan="1">Unclassified</td><td valign="top" align="left" rowspan="1" colspan="1">Sordariomycetes_sp_PMI488</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_22</td><td valign="top" align="center" rowspan="1" colspan="1">TNPo7</td><td valign="top" align="left" rowspan="1" colspan="1">0.0078</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_22</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Pezizomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Pezizales</td><td valign="top" align="left" rowspan="1" colspan="1">Tuberaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Tuber</td><td valign="top" align="left" rowspan="1" colspan="1">Tuber mexiusanum</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_16</td><td valign="top" align="center" rowspan="1" colspan="1">TNPo7</td><td valign="top" align="left" rowspan="1" colspan="1">0.0281</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_16</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Pezizomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Pezizales</td><td valign="top" align="left" rowspan="1" colspan="1">Incertae</td><td valign="top" align="left" rowspan="1" colspan="1">Sedis</td><td valign="top" align="left" rowspan="1" colspan="1">Pulvinula sp</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_4</td><td valign="top" align="center" rowspan="1" colspan="1">TNP11+TNPo7</td><td valign="top" align="left" rowspan="1" colspan="1">0.0234</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_4</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Basidiomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Agaricomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Agaricales</td><td valign="top" align="left" rowspan="1" colspan="1">Strophariaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Hebeloma</td><td valign="top" align="left" rowspan="1" colspan="1">Hebeloma cavipes</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_2</td><td valign="top" align="center" rowspan="1" colspan="1">TNP11+TNPo1+TNPo7</td><td valign="top" align="left" rowspan="1" colspan="1">0.0052</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_2</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Pezizomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Pezizales</td><td valign="top" align="left" rowspan="1" colspan="1">Pyronemataceae</td><td valign="top" align="left" rowspan="1" colspan="1">Geopora</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_56</td><td valign="top" align="center" rowspan="1" colspan="1">TNPo5+TNPo6+TNPo8</td><td valign="top" align="left" rowspan="1" colspan="1">0.0078</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_56</td><td valign="top" align="left" rowspan="1" colspan="1">FungiPMI</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Sordariomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Magnaporthales</td><td valign="top" align="left" rowspan="1" colspan="1">Magnaporthaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Mycoleptodiscus</td><td valign="top" align="left" rowspan="1" colspan="1">Mycoleptodiscus_sp_PMI219</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_8</td><td valign="top" align="center" rowspan="1" colspan="1">TNP11+TNPo6+TNPo7+TNPo8</td><td valign="top" align="left" rowspan="1" colspan="1">0.0052</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_8</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Basidiomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Agaricomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Agaricales</td><td valign="top" align="left" rowspan="1" colspan="1">Inocybaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Inocybe</td><td valign="top" align="left" rowspan="1" colspan="1">Inocybe curvipes</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_1</td><td valign="top" align="center" rowspan="1" colspan="1">TNPo3+TNPo4+TNPo5+TNPo6+TNPo8</td><td valign="top" align="left" rowspan="1" colspan="1">0.0052</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_1</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Basidiomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Atractiellomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Atractiellales</td><td valign="top" align="left" rowspan="1" colspan="1">Unidentified</td><td valign="top" align="left" rowspan="1" colspan="1">Unidentified</td><td valign="top" align="left" rowspan="1" colspan="1">Atractiellales sp</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Soil genotype</td><td valign="top" align="left" rowspan="1" colspan="1">None</td><td valign="top" align="center" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Soil genotype by soil</td><td valign="top" align="left" rowspan="1" colspan="1">OTU_14</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00144</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_14</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Incertae sedis</td><td valign="top" align="left" rowspan="1" colspan="1">Incertae sedis</td><td valign="top" align="left" rowspan="1" colspan="1">Incertae sedis</td><td valign="top" align="left" rowspan="1" colspan="1">Polyscytalum</td><td valign="top" align="left" rowspan="1" colspan="1">Polyscytalum pustulans</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_18</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00144</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_18</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Dothideomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Pleosporales</td><td valign="top" align="left" rowspan="1" colspan="1">Incertae sedis</td><td valign="top" align="left" rowspan="1" colspan="1">Phoma</td><td valign="top" align="left" rowspan="1" colspan="1">NA</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_8</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00144</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_8</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Dothideomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Pleosporales</td><td valign="top" align="left" rowspan="1" colspan="1">Unclassified</td><td valign="top" align="left" rowspan="1" colspan="1">Unclassified</td><td valign="top" align="left" rowspan="1" colspan="1">PleosporalePMI117</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_5</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00144</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_5</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Sordariomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Hypocreales</td><td valign="top" align="left" rowspan="1" colspan="1">Incertae sedis</td><td valign="top" align="left" rowspan="1" colspan="1">Sarocladium</td><td valign="top" align="left" rowspan="1" colspan="1">Sarocladium strictum</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_1</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00144</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_1</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Dothideomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Pleosporales</td><td valign="top" align="left" rowspan="1" colspan="1">Incertae sedis</td><td valign="top" align="left" rowspan="1" colspan="1">Phoma</td><td valign="top" align="left" rowspan="1" colspan="1">NA</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_9</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.01313</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_9</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Sordariomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">NA</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_16</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00253</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_16</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Dothideomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Capnodiales</td><td valign="top" align="left" rowspan="1" colspan="1">Davidiellaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Cladosporium</td><td valign="top" align="left" rowspan="1" colspan="1">Cladosporium ramotenellum</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_46</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00337</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_47</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Dothideomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Pleosporales</td><td valign="top" align="left" rowspan="1" colspan="1">Unclassified</td><td valign="top" align="left" rowspan="1" colspan="1">Unclassified</td><td valign="top" align="left" rowspan="1" colspan="1">PleosporalePMI628</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_31</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.02693</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_31</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Sordariomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Coniochaetales</td><td valign="top" align="left" rowspan="1" colspan="1">Coniochaetaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Lecythophora</td><td valign="top" align="left" rowspan="1" colspan="1">Lecythophora fasciculata</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_21</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.0202</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_21</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Leotiomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Helotiales</td><td valign="top" align="left" rowspan="1" colspan="1">Incertae_sedis</td><td valign="top" align="left" rowspan="1" colspan="1">Cadophora</td><td valign="top" align="left" rowspan="1" colspan="1">Cadophora_luteo-olivacea__PMI1442</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_3</td><td valign="top" align="center" rowspan="1" colspan="1">NC1+NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.00144</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_3</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">NA</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_2</td><td valign="top" align="center" rowspan="1" colspan="1">NC1+NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.00144</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_2</td><td valign="top" align="left" rowspan="1" colspan="1">Fungi</td><td valign="top" align="left" rowspan="1" colspan="1">Ascomycota</td><td valign="top" align="left" rowspan="1" colspan="1">Sordariomycetes</td><td valign="top" align="left" rowspan="1" colspan="1">Hypocreales</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Bacteria soil</td><td valign="top" align="left" rowspan="1" colspan="1">OTU_319</td><td valign="top" align="center" rowspan="1" colspan="1">TNP11+TNPo1+TNPo4</td><td valign="top" align="left" rowspan="1" colspan="1">0.0171</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_229</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Alphaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Rhodobacterales</td><td valign="top" align="left" rowspan="1" colspan="1">Hyphomonadaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_229</td><td valign="top" align="center" rowspan="1" colspan="1">TNP11+TNPo4+TNPo5+TNPo6+TNPo8</td><td valign="top" align="left" rowspan="1" colspan="1">0.0171</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_319</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteroidetes</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirae]</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirales]</td><td valign="top" align="left" rowspan="1" colspan="1">Chitinophagaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Bacteria genotype</td><td valign="top" align="left" rowspan="1" colspan="1">None</td><td valign="top" align="center" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Bacteria genotype by soil</td><td valign="top" align="left" rowspan="1" colspan="1">OTU_36</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00223</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_36</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Betaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Burkholderiales</td><td valign="top" align="left" rowspan="1" colspan="1">Comamodaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_46</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00394</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_46</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Betaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Burkholderiales</td><td valign="top" align="left" rowspan="1" colspan="1">Comamodaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Stenotrophomos</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_41</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00582</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">TU_41</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Gammaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Xanthomodales</td><td valign="top" align="left" rowspan="1" colspan="1">Xanthomodaceae</td><td valign="top" align="left" colspan="2" rowspan="1">Janthinobacterium</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_6</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.01195</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_6</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Betaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Burkholderiales</td><td valign="top" align="left" rowspan="1" colspan="1">Oxalobacteraceae</td><td valign="top" align="left" rowspan="1" colspan="1">Salinispora</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_21</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00223</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_21</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Betaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Burkholderiales</td><td valign="top" align="left" rowspan="1" colspan="1">Burkholderiaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Flavobacterium</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>Flavobacterium succinicans</italic></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_1</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00223</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_1</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteroidetes</td><td valign="top" align="left" rowspan="1" colspan="1">Flavobacteriia</td><td valign="top" align="left" rowspan="1" colspan="1">Flavobacteriales</td><td valign="top" align="left" rowspan="1" colspan="1">Flavobacteriaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Nocardioides</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_166</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00394</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_166</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinomycetales</td><td valign="top" align="left" rowspan="1" colspan="1">Nocardioidaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Cytophaga</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_44</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00319</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_44</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteroidetes</td><td valign="top" align="left" rowspan="1" colspan="1">Cytophagia</td><td valign="top" align="left" rowspan="1" colspan="1">Cytophagales</td><td valign="top" align="left" rowspan="1" colspan="1">Cytophagaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Asticcacaulis</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_52</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.01402</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_52</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Alphaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Caulobacterales</td><td valign="top" align="left" rowspan="1" colspan="1">Caulobacteraceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_51</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00803</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_51</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteroidetes</td><td valign="top" align="left" rowspan="1" colspan="1">Sphingobacteriia</td><td valign="top" align="left" rowspan="1" colspan="1">Sphingobacteriales</td><td valign="top" align="left" rowspan="1" colspan="1">Sphingobacteriaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Prosthecobacter</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_33</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00394</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_33</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Verrucomicrobia</td><td valign="top" align="left" rowspan="1" colspan="1">Verrucomicrobiae</td><td valign="top" align="left" rowspan="1" colspan="1">Verrucomicrobiales</td><td valign="top" align="left" rowspan="1" colspan="1">Verrucomicrobiaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Aminobacter</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_39</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00582</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_39</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Alphaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Rhizobiales</td><td valign="top" align="left" rowspan="1" colspan="1">Phyllobacteriaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Pseudonocardia</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>Pseudonocardia-halophobica</italic></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_11</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.01223</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_11</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinomycetales</td><td valign="top" align="left" colspan="2" rowspan="1">Pseudonocardiaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_15</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.04733</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_15</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Alphaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Ellin329</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">Sphingobium</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_180</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.00909</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_180</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Alphaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Sphingomodales</td><td valign="top" align="left" rowspan="1" colspan="1">Sphingomodaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Novosphingobium</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_60</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.04262</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_60</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Alphaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Sphingomodales</td><td valign="top" align="left" rowspan="1" colspan="1">Sphingomodaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_212</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.04733</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_212</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Gammaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Pseudomodales</td><td valign="top" align="left" rowspan="1" colspan="1">Pseudomodaceae</td><td valign="top" align="left" colspan="2" rowspan="1">Chryseobacterium</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_183</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.04555</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_183</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteroidetes</td><td valign="top" align="left" rowspan="1" colspan="1">Flavobacteriia</td><td valign="top" align="left" rowspan="1" colspan="1">Flavobacteriales</td><td valign="top" align="left" rowspan="1" colspan="1">[Weeksellaceae]</td><td valign="top" align="left" rowspan="1" colspan="1">Alicyclobacillus</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_167</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.01402</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_167</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Firmicutes</td><td valign="top" align="left" rowspan="1" colspan="1">Bacilli</td><td valign="top" align="left" rowspan="1" colspan="1">Bacillales</td><td valign="top" align="left" rowspan="1" colspan="1">Alicyclobacillaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_176</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.02058</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_176</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Verrucomicrobia</td><td valign="top" align="left" rowspan="1" colspan="1">[Pedosphaerae]</td><td valign="top" align="left" rowspan="1" colspan="1">[Pedosphaerales]</td><td valign="top" align="left" rowspan="1" colspan="1">auto67_4W</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_69</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.01567</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_69</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Alphaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Rhodospirillales</td><td valign="top" align="left" rowspan="1" colspan="1">Acetobacteraceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_170</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.02973</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_170</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteroidetes</td><td valign="top" align="left" rowspan="1" colspan="1">Sphingobacteriia</td><td valign="top" align="left" rowspan="1" colspan="1">Sphingobacteriales</td><td valign="top" align="left" colspan="2" rowspan="1">Sphingobacteriaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_7</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.01549</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_7</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteroidetes</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirae]</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirales]</td><td valign="top" align="left" rowspan="1" colspan="1">Chitinophagaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_35</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.02883</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_35</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Alphaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Rhizobiales</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_10</td><td valign="top" align="center" rowspan="1" colspan="1">Control</td><td valign="top" align="left" rowspan="1" colspan="1">0.0363</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_10</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Acidobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Solibacteres</td><td valign="top" align="left" rowspan="1" colspan="1">Solibacterales</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">Chitinophaga</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_113</td><td valign="top" align="center" rowspan="1" colspan="1">NC1</td><td valign="top" align="left" rowspan="1" colspan="1">0.00223</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_113</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteroidetes</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirae]</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirales]</td><td valign="top" align="left" rowspan="1" colspan="1">Chitinophagaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_108</td><td valign="top" align="center" rowspan="1" colspan="1">NC1</td><td valign="top" align="left" rowspan="1" colspan="1">0.00858</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_108</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Armatimodetes</td><td valign="top" align="left" rowspan="1" colspan="1">Armatimodia</td><td valign="top" align="left" rowspan="1" colspan="1">Armatimodales</td><td valign="top" align="left" rowspan="1" colspan="1">Armatimodaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_270</td><td valign="top" align="center" rowspan="1" colspan="1">NC1</td><td valign="top" align="left" rowspan="1" colspan="1">0.04555</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_270</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteroidetes</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirae]</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirales]</td><td valign="top" align="left" rowspan="1" colspan="1">Chitinophagaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_130</td><td valign="top" align="center" rowspan="1" colspan="1">NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.00223</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_130</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinomycetales</td><td valign="top" align="left" colspan="2" rowspan="1">Micromonosporaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_159</td><td valign="top" align="center" rowspan="1" colspan="1">NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.00469</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_159</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteroidetes</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirae]</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirales]</td><td valign="top" align="left" rowspan="1" colspan="1">Chitinophagaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_138</td><td valign="top" align="center" rowspan="1" colspan="1">NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.00469</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_138</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Betaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Burkholderiales</td><td valign="top" align="left" rowspan="1" colspan="1">Oxalobacteraceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_226</td><td valign="top" align="center" rowspan="1" colspan="1">NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.00319</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_226</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteroidetes</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirae]</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirales]</td><td valign="top" align="left" rowspan="1" colspan="1">Chitinophagaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Asticcacaulis</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_142</td><td valign="top" align="center" rowspan="1" colspan="1">NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.00582</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_142</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Alphaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Caulobacterales</td><td valign="top" align="left" rowspan="1" colspan="1">Caulobacteraceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_139</td><td valign="top" align="center" rowspan="1" colspan="1">NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.01702</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_139</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Chloroflexi</td><td valign="top" align="left" rowspan="1" colspan="1">Ktedonobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Ktedonobacterales</td><td valign="top" align="left" rowspan="1" colspan="1">Ktedonobacteraceae</td><td valign="top" align="left" colspan="2" rowspan="1">Phenylobacterium</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_145</td><td valign="top" align="center" rowspan="1" colspan="1">NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.04207</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_145</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Alphaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Caulobacterales</td><td valign="top" align="left" rowspan="1" colspan="1">Caulobacteraceae</td><td valign="top" align="left" rowspan="1" colspan="1">Caulobacter</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_17</td><td valign="top" align="center" rowspan="1" colspan="1">Control+NC1</td><td valign="top" align="left" rowspan="1" colspan="1">0.014</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_17</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Alphaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Caulobacterales</td><td valign="top" align="left" rowspan="1" colspan="1">Caulobacteraceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_16</td><td valign="top" align="center" rowspan="1" colspan="1">Control+NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.00743</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_16</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Alphaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Rhizobiales</td><td valign="top" align="left" rowspan="1" colspan="1">Rhizobiaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Asticcacaulis</td><td valign="top" align="left" rowspan="1" colspan="1">Asticcacaulis biprosthecium</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_40</td><td valign="top" align="center" rowspan="1" colspan="1">Control+NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.02883</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_40</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Alphaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Caulobacterales</td><td valign="top" align="left" rowspan="1" colspan="1">Caulobacteraceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_76</td><td valign="top" align="center" rowspan="1" colspan="1">NC1+NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.00223</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_76</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteroidetes</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirae]</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirales]</td><td valign="top" align="left" rowspan="1" colspan="1">Chitinophagaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_129</td><td valign="top" align="center" rowspan="1" colspan="1">NC1+NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.00223</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_129</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Betaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Burkholderiales</td><td valign="top" align="left" rowspan="1" colspan="1">Comamodaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_99</td><td valign="top" align="center" rowspan="1" colspan="1">NC1+NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.00223</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_99</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinomycetales</td><td valign="top" align="left" colspan="2" rowspan="1">Micromonosporaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_93</td><td valign="top" align="center" rowspan="1" colspan="1">NC1+NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.00223</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_93</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinomycetales</td><td valign="top" align="left" colspan="2" rowspan="1">Micromonosporaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_80</td><td valign="top" align="center" rowspan="1" colspan="1">NC1+NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.00319</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_80</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Gammaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Xanthomodales</td><td valign="top" align="left" rowspan="1" colspan="1">Sinobacteraceae</td><td valign="top" align="left" rowspan="1" colspan="1">Telmatospirillum</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_88</td><td valign="top" align="center" rowspan="1" colspan="1">NC1+NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.00223</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_88</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Proteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Alphaproteobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Rhodospirillales</td><td valign="top" align="left" rowspan="1" colspan="1">Rhodospirillaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_77</td><td valign="top" align="center" rowspan="1" colspan="1">NC1+NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.00319</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_77</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinomycetales</td><td valign="top" align="left" rowspan="1" colspan="1">Actinospicaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_79</td><td valign="top" align="center" rowspan="1" colspan="1">NC1+NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.00558</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_79</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Armatimodetes</td><td valign="top" align="left" rowspan="1" colspan="1">Armatimodia</td><td valign="top" align="left" rowspan="1" colspan="1">FW68</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_75</td><td valign="top" align="center" rowspan="1" colspan="1">NC1+NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.01223</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_75</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinobacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Actinomycetales</td><td valign="top" align="left" rowspan="1" colspan="1">Actinospicaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_106</td><td valign="top" align="center" rowspan="1" colspan="1">NC1+NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.01402</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_106</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteroidetes</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirae]</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirales]</td><td valign="top" align="left" rowspan="1" colspan="1">Chitinophagaceae</td><td valign="top" align="left" rowspan="1" colspan="1">Niastella</td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_112</td><td valign="top" align="center" rowspan="1" colspan="1">NC1+NC2</td><td valign="top" align="left" rowspan="1" colspan="1">0.01223</td><td valign="top" align="left" rowspan="1" colspan="1"><sup>∗</sup></td><td valign="top" align="left" rowspan="1" colspan="1">OTU_112</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteria</td><td valign="top" align="left" rowspan="1" colspan="1">Bacteroidetes</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirae]</td><td valign="top" align="left" rowspan="1" colspan="1">[Saprospirales]</td><td valign="top" align="left" rowspan="1" colspan="1">Chitinophagaceae</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="left" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"></td></tr></tbody></table><table-wrap-foot><attrib><italic>Significance codes: “<sup>∗</sup>” 0.05, “<sup>∗∗</sup>” 0.01 fater 9999 permutations.</italic></attrib></table-wrap-foot></table-wrap></sec><sec><title>Arbuscular Mycorrhizal Communities</title><p>In total, 22 OTUs belonging to the Glomeromycotina were detected across these genotypes (<xref ref-type="fig" rid="F3">Figure 3</xref> and Supplementary File <xref ref-type="supplementary-material" rid="SM18">S1</xref>); aside from a single OTU belonging to <italic>Gigaspora</italic> detected on the hybrid genotype, no discernable effects of genotype on their distribution were evident. By genotyping arbuscular mycorrhizal spores (60 sequences, 10 OTUs), we detected that sorghum enriches for a different AMF community compared to <italic>Populus</italic> (only 3 overlap OTU between <italic>Populus</italic> root pyrosequencing and Sanger genotyping of sorghum roots). The most prevalent AMF orders detected on <italic>Populus</italic> were Glomerales, Paraglomerales, Diversisporales and Archaeosporales, respectively (Supplementary File <xref ref-type="supplementary-material" rid="SM18">S1</xref>).</p><fig id="F3" position="float"><label>FIGURE 3</label><caption><p>Phylogeny of Glomeromycotina showing the phylogenetic position of arbuscular mycorrhizal fungi detected in this study. Taxonomic families are denoted by colored branches. Black branches denote Diversisporaceae; orange branches denote Gigasporaceae; blue branches denote Glomeraceae; green branches denote Paraglomeraceae; and red branches denote Archaeosporaceae.</p></caption><graphic xlink:href="fmicb-10-00481-g003"></graphic></fig></sec><sec><title>Plant Genotype Impact on Fungal and Bacterial Networks</title><p>Bipartite fungal-bacterial networks show that soil origin and soil properties structured microbial communities more than host genotype, which is also reflected in sample correlations based on maximum spanning trees (<xref ref-type="fig" rid="F4">Figure 4</xref>, <xref ref-type="supplementary-material" rid="SM4">Supplementary Figure S4</xref>, and <xref ref-type="supplementary-material" rid="SM12">Supplementary Table S4</xref>). Fisher’s Exact tests, investigating the enrichment of OTUs in genotypes separately within each soil type, reveal that the OTUs which are enriched in genotype samples vary based on the soil in which the genotype was grown (<xref ref-type="supplementary-material" rid="SM5">Supplementary Figure S5</xref>). This is contrary to expectations of a strong genotype effect, or evidence for vertical transmission of a pre-existing community. The enrichment bipartite network (<xref ref-type="fig" rid="F5">Figure 5</xref> and <xref ref-type="supplementary-material" rid="SM13">Supplementary Table S5</xref>) for Experiment 1 does not show any obvious grouping of genotypes based on their significant OTU associations. This indicates that OTUs that are enriched in a sample cannot be used to discriminate plant genotype. However, there are a few OTUs which do appear to be relatively genotype-specific. We calculated the quotient coefficient for each OTU by dividing the degree of each OTU node in the enrichment network by the total number of different genotypes that the OTU was enriched in <xref ref-type="supplementary-material" rid="SM13">Supplementary Table S5</xref>. Selecting only OTUs that were significantly associated with samples spanning ≤ 2 genotypes and with a quotient ≥ 2, one can see the effect of genotype grouping by considering only these “genotype-specific” OTUs (<xref ref-type="fig" rid="F5">Figure 5B,C</xref>).</p><fig id="F4" position="float"><label>FIGURE 4</label><caption><p>Experiment 1 sample similarity Maximum Spanning Trees (MSTs), constructed using the Proportional Similarity metric, representing similarity of samples based on their Operational taxonomic unit (OTU) content, colored by <bold>(A)</bold> soil and <bold>(B)</bold> genotype.</p></caption><graphic xlink:href="fmicb-10-00481-g004"></graphic></fig><fig id="F5" position="float"><label>FIGURE 5</label><caption><p><bold>(A)</bold> Operational taxonomic unit (OTU)-sample enrichment networks representing the enrichment of OTUs in samples for Experiment 1, determined using the Fisher Exact test. <bold>(B)</bold> Subnetwork of the enrichment network involving genotype-specific OTUs, i.e., OTUs which were enriched in ≤ 2 genotypes and had a quotient ≥ 2 (see Materials and Methods and <xref ref-type="supplementary-material" rid="SM13">Supplementary Table S5</xref>). <bold>(C)</bold> Abundance line plots of selected OTUs which appear to be enriched in genotypes D110 and D133.</p></caption><graphic xlink:href="fmicb-10-00481-g005"></graphic></fig><p>Correlation analysis of the abundance of OTUs across samples resulted in a network with an obvious modular structure (<xref ref-type="fig" rid="F6">Figure 6A</xref>). This was evident not only visually, but also quantitatively by looking at the distributions of various topology measures (<xref ref-type="supplementary-material" rid="SM14">Supplementary Table S6</xref> and <xref ref-type="supplementary-material" rid="SM6">Supplementary Figure S6</xref>). The degree of a node indicates the number of neighbors it has in the correlation network. The degree distribution clearly indicates that most OTUs have a low degree, with a few OTUs representing hubs of high degree. The clustering coefficient of a node indicates the extent to which its neighbors are connected. The topological coefficient of a node indicates the extent to which a node shares neighbors with other nodes. The betweenness centrality of a node is an indicator of how many shortest paths pass through the node and is thus an indicator of “bottleneck nodes.” Betweenness is often high for nodes that form bridges between communities but are not within communities. The distributions of these network topology measures support the existence of a certain level of modular structure within the network, involving hub OTUs and communities. A small number of OTUs, even some that are not within communities, appear to serve as “bridges” between communities. Community construction based on Markov Cluster Algorithms (I = 2.5) resulted in 39 communities (<xref ref-type="fig" rid="F6">Figure 6B</xref> and <xref ref-type="supplementary-material" rid="SM14">Supplementary Table S6</xref>). An example of the correlated abundances of OTUs within a community can be seen in <xref ref-type="fig" rid="F6">Figure 6C</xref>. Communities varied in size within the smallest communities consisting of 2 OTUs and the largest community consisting of 25 OTUs. More than half of the communities (20 out of 39) consisted of both fungi and bacteria, with only one community lacking bacteria and 18 communities lacking fungi (<xref ref-type="fig" rid="F6">Figure 6A</xref> and <xref ref-type="supplementary-material" rid="SM15">Supplementary Table S7</xref>). Taxa in the bacterial orders Rhizobiales, Chitinophagales, Cytophagales, and Burkholderiales were present in a majority of the networks. Ectomycorrhizal fungi, (i.e., <italic>Hebeloma</italic>, <italic>Inocybe</italic>, and <italic>Thelephoraceae</italic>) were included in three of the networks, each of which had more orders of bacterial taxa that differed than were shared (<xref ref-type="supplementary-material" rid="SM14">Supplementary Table S6</xref>). Many networks were comprised of endophytic fungi including species of <italic>Atractiella, Fusarium</italic>, Helotiales and bacteria, many of which have previously been reported and isolated from <italic>Populus</italic> roots (<xref rid="B58" ref-type="bibr">Shakya et al., 2013</xref>; <xref rid="B69" ref-type="bibr">Bonito et al. 2014</xref>, <xref rid="B12" ref-type="bibr">2016</xref>).</p><fig id="F6" position="float"><label>FIGURE 6</label><caption><p><bold>(A)</bold> Operational taxonomic unit (OTU) Pearson correlation network for Experiment 1, indicating the correlations between OTUs across samples. <bold>(B)</bold> Markov Cluster (MCL) community clusters of OTUs constructed from clustering of the network in <xref ref-type="fig" rid="F6">Figure 6A</xref>. <bold>(C)</bold> Example line plot of 3 OTUs in MCL community 3, illustrating their correlated abundances.</p></caption><graphic xlink:href="fmicb-10-00481-g006"></graphic></fig></sec><sec><title>Experiment 2: Effect of Soil Origin on the Root Microbiome of a Single <italic>Populus</italic> Genotype</title><p>Differences in fungal root-associated communities were evident in samples of a single <italic>Populus</italic> genotype grown in soils collected from different locales (<xref ref-type="fig" rid="F2">Figure 2</xref>). There were distinct differences in the fungal community composition detected between assayed soils, and even some of the most abundant taxa (i.e., <italic>Atractiella</italic> sp. nov, <italic>Geopora</italic> sp.1) were not in every soil (<xref ref-type="fig" rid="F1">Figure 1</xref>). Only a single OTU (<italic>Ilyonectria</italic> sp.1) was detected in every sample. Likewise, there was much more variation in the root-associated bacterial communities of this single genotype grown in these eight different soils (<xref ref-type="fig" rid="F2">Figure 2</xref>) than was observed for the different genotypes assayed in Experiment 1. Plants grown in the TN soils were more enriched in Micromonosporaceae and Flavisolibacter (Chitinophagaceae) compared to samples in Experiment 1 that were grown in soils from NC (<xref ref-type="supplementary-material" rid="SM3">Supplementary Figure S3</xref>). In particular, fungal and bacterial communities of samples grown in the soil TNPo1 were distinct from other samples. We calculated the average growth rate of <italic>Populus</italic> genotype D124 for plants grown in these different soil types (data not shown). A one-way ANOVA showed that these growth rates were not significantly different (<italic>F</italic> = 1.856, <italic>p</italic> = 0.129). Regarding fungal communities, PERMANOVA results support PCoA graphs and show that ∼68% of the sums of squares can be explained by the soil origin (<italic>R</italic><sup>2</sup> = 0.682, <italic>p</italic> = 0.0001, perm = 9999). Multivariate dispersions of sample groups did not differ statistically (<italic>F</italic> = 1.226, <italic>p</italic> = 0.344). Bacterial OTUs clustered according to soil origin (<italic>R</italic><sup>2</sup> = 0.519, <italic>p</italic> = 0.0001, perm = 9999), and no heterogeneity within group variances was detected (<italic>F</italic> = 0.362, <italic>p</italic> = 0.911).</p></sec><sec><title>Indicator Species Analysis</title><p>Indicator species analysis identified twelve fungal taxa associated to specific soils, half of which were of ectomycorrhizal species including <italic>Tuber mexiusanum, Hebeloma cavipes, Inocybe curvipes, Geopora</italic> sp., <italic>Pulvinula</italic> sp, and Thelephoraceae sp. The root endophytic fungus <italic>Atractiella rhizophila</italic> was significantly associated with five of the sampled plots. Four bacterial taxa belonging to the Cytophagaceae, Chitinophagaceae, Acidimicrobiales, and Hyphomonadaceae were identified by species indicator analysis (<xref rid="T1" ref-type="table">Table 1</xref>) to be statistically associated (<italic>P</italic> < 0.05) to a particular soil.</p></sec><sec><title>Impact of Soils on Fungal and Bacterial Networks</title><p>Maximum spanning tree networks representing sample similarity based on OTU content revealed that root-associated microbial communities are largely structured by soil (<xref ref-type="fig" rid="F7">Figure 7</xref>). Soil characteristics such as calcium and magnesium appeared to have a large influence on the structure of fungal-bacterial networks, as one can see that samples tend to segregate based on these variables (<xref ref-type="fig" rid="F7">Figure 7B,C</xref>). OTU enrichment bipartite networks also tend to group samples by soil (<xref ref-type="fig" rid="F8">Figure 8A</xref>) and segregation of sample nodes appears to follow a calcium gradient (<xref ref-type="fig" rid="F8">Figure 8B</xref>). Correlation analysis of OTU abundances across samples resulted in a network with a modular structure (<xref ref-type="fig" rid="F9">Figure 9A</xref>). Again, topological analysis of the network through various network topology measures quantitatively supports the existence of some modularity, and thus, potential communities (<xref ref-type="supplementary-material" rid="SM7">Supplementary Figure S7</xref> and <xref ref-type="supplementary-material" rid="SM16">Supplementary Table S8</xref>). Community construction using MCL (<italic>I</italic> = 2.5) resulted in 66 communities (<xref ref-type="fig" rid="F9">Figure 9B</xref>). Communities represent groups of OTUs with correlated abundances across samples (For example, <xref ref-type="fig" rid="F9">Figure 9C</xref>). OTU communities varied in size, with the largest community consisting of 24 members and the smallest communities consisting of 2 members. Of the 66 communities, 28 consisted of both bacteria and fungi, 33 consisted of only bacteria and 5 consisted of only fungi (<xref ref-type="supplementary-material" rid="SM17">Supplementary Table S9</xref>). <italic>Atractiella</italic> was associated with one fungal-bacterial network composed of <italic>Atractiella</italic> and the bacterium Chitinophagaceae. Arbuscular mycorrhizal fungi were included in three of the networks. While some ectomycorrhizal taxa such as <italic>Tuber</italic> and <italic>Tomentella</italic> were shared between networks, most ectomycorrhizal taxa overrepresented in fungal-bacterial networks belonged to different sub-networks.</p><fig id="F7" position="float"><label>FIGURE 7</label><caption><p>Experiment 2 (soil origin) sample similarity MSTs (constructed using the Proportional Similarity metric) representing similarity of samples based on their operational taxonomic unit (OTU) content, colored by <bold>(A)</bold> soil, <bold>(B)</bold> magnesium ppm of soil, and <bold>(C)</bold> calcium content of soil.</p></caption><graphic xlink:href="fmicb-10-00481-g007"></graphic></fig><fig id="F8" position="float"><label>FIGURE 8</label><caption><p>Operational taxonomic unit (OTU)-sample enrichment networks representing the enrichment of OTUs in samples for Experiment 2: Soil origin. An OTU node is connected to a sample node via an edge if the OTU is significantly enriched in that sample. Sample nodes are colored by <bold>(A)</bold> soil and <bold>(B)</bold> calcium content.</p></caption><graphic xlink:href="fmicb-10-00481-g008"></graphic></fig><fig id="F9" position="float"><label>FIGURE 9</label><caption><p><bold>(A)</bold> Operational taxonomic unit (OTU) Pearson correlation network for Experiment 2 (soil origin), indicating the correlations between OTUs across samples. <bold>(B)</bold> Markov Cluster (MCL) community clusters of OTUs constructed from clustering of the network in <xref ref-type="fig" rid="F9">Figure 9A</xref>. <bold>(C)</bold> Example line plot of 3 OTUs in MCL community 2, illustrating their correlated abundances.</p></caption><graphic xlink:href="fmicb-10-00481-g009"></graphic></fig><p>Certain soil properties correlated with one another (<xref ref-type="supplementary-material" rid="SM8">Supplementary Figure S8</xref>) and with certain OTU abundances and appear to be potentially driving communities (<xref ref-type="fig" rid="F10">Figure 10A</xref>). For example, distance to the river is correlated with two Chitinophagaceae 16S OTUs in MCL community 32 as well as an <italic>Methylotenera mobilis</italic> OTU in community 20 (<xref ref-type="fig" rid="F10">Figure 10B</xref>), and calcium percentage is correlated with OTUs of ECM fungi (e.g., <italic>Hebeloma cavipes</italic>, <italic>Pulvinua</italic> sp.) in MCL community 3 (<xref ref-type="fig" rid="F10">Figure 10C</xref>), indicating potential drivers of these communities.</p><fig id="F10" position="float"><label>FIGURE 10</label><caption><p><bold>(A)</bold> Pearson correlation network of operational taxonomic unit (OTU) communities and soil physicochemical/environmental parameters at a threshold of | Pearson|≥ 0.6, indicating the correlation between the various soil properties with OTU abundance across samples in Experiment 2: Soil origin. <bold>(B)</bold> Example of 3 OTUs whose abundances correlate with distance from the river. <bold>(C)</bold> Example of three OTUs whose abundances correlate with calcium content of soil.</p></caption><graphic xlink:href="fmicb-10-00481-g010"></graphic></fig></sec></sec><sec><title>Discussion</title><p>Plant microbiomes are diverse and complex in structure and function. In this study, we assessed the impact of plant genotype and soil on root microbiome of <italic>Populus</italic> using natural soils as inoculum and plant bioassay experiments in a common garden design. Results show that bacterial diversity in the <italic>Populus</italic> rhizobiome is many times higher than fungal diversity. Genetic variation of plant hosts is known to be important to herbivore and pathogen resistance (<xref rid="B37" ref-type="bibr">Keith and Mitchell-Olds, 2013</xref>), and host genetics have been shown to be important in plant selection for mutualistic ectomycorrhizal fungi and their functioning (<xref rid="B27" ref-type="bibr">Gehring et al., 2017</xref>). We found that the impact of host genotype was dependent on soil, and that the effect was at the community level, with no apparent impact on specific ITS or 16S OTUs. For example, the top 20 most abundant fungi were found on all genotypes, and no taxon responding to host genotype was observed across all sample replicates of any genotype. Additionally, indicator species analysis failed to detect any OTUs of ITS or 16S statistically associated to a specific <italic>Populus</italic> genotype. Similar results were obtained for prokaryotes, with <italic>Niastella</italic>, Micromonosporineae, and <italic>Bradyrhizobium</italic> being particularly well represented in the <italic>Populus</italic> rhizobiome across treatments. In contrast, despite the fact that many fungal root endophytes of <italic>Populus</italic> appear to have widespread distributions, soil origin and soil physicochemical characteristics explained most of the measurable variation in fungal and bacterial communities and multi-kingdom bipartite networks. In particular, fungal-bacterial networks clustered in relation to geographic location, soil texture and soil phosphorus level. These results indicate that microbial taxa are not evenly distributed across the landscape, and plant microbiome composition is largely influenced by edaphic factors and local environment.</p><p><italic>Populus</italic> can establish both ectomycorrhizal and arbuscular mycorrhizal symbiosis (<xref rid="B64" ref-type="bibr">Vozzo and Hacskaylo, 1974</xref>; <xref rid="B43" ref-type="bibr">Lodge, 1989</xref>). We detected several ectomycorrhizal fungi in <italic>P. deltoides</italic> and <italic>P. deltoides</italic> x <italic>P. trichocarpa</italic> hybrid genotypes include <italic>Inocybe</italic> spp, <italic>Hebeloma</italic> spp., Pezizales spp., <italic>Geopora</italic> spp. and Thelephoraceae. Arbuscular mycorrhizal fungi were detected in the diverse soil treatments, including Glomeraceae and Paraglomeraceae, as previously shown (<xref rid="B69" ref-type="bibr">Bonito et al., 2014</xref>). No impact of genotype or soil was observed for arbuscular mycorrhizal fungi. This result was expected since, ecologically, most arbuscular mycorrhizal fungi are considered to be host-generalists. <italic>Populus deltoides</italic> associates with a variety of fungal symbionts, rather than specializing with specific taxa. Despite the presence of arbuscular and ectomycorrhizal fungi, our data demonstrate that the rhizobiome of <italic>Populus</italic> is dominated by facultative endophytes (∼85% OTUs), most of which appear to be culturable and have saprotrophic activity. For example, <italic>Atractiella rhizophila</italic> was first described from <italic>Populus</italic> and detected as an abundant OTU in natural habitats through molecular assessments (<xref rid="B30" ref-type="bibr">Gottel et al., 2011</xref>; <xref rid="B11" ref-type="bibr">Bonito et al., 2017</xref>). We found this taxon to be dominant (in terms of relative sequence abundance) in five of the eight soils used in the bioassay experiments, and this taxon was present in soils from both North Carolina and Tennessee. Other endophytic fungi commonly detected in <italic>Populus</italic> include <italic>Ilyonectria</italic> spp.(= <italic>Cylindrocarpon</italic>), <italic>Fusarium oxysporum</italic>, <italic>Phoma herbarum</italic>, Chaetothyriales sp., and <italic>Sebacina</italic> sp. Ecologically, many of these genera are regarded as plant pathogens (e.g., <italic>Fusarium</italic> spp., <italic>Ilyonectria</italic> spp., <italic>Phoma</italic> spp.), yet there is no indication that these specific fungi are pathogenic to <italic>Populus</italic>. In fact, some species within these genera are even reported as plant growth-promoting fungi (<xref rid="B32" ref-type="bibr">Hamayun et al., 2009</xref>). For these reasons, we were cautious about trying to overclassify the function(s) of these OTUs. The ability of <italic>Populus</italic> to host fungi in high abundance that are considered to be generalist pathogens to other plants may offer a competitive advantage to <italic>Populus</italic> in certain environments. Further, virulence of potential pathogens could be dictated by multi-partner interactions and environmental conditions that may be detectable through network analyses (<xref rid="B33" ref-type="bibr">Hersh et al., 2012</xref>). Further, disease susceptibility can vary between hosts and may interact with host genotype. A large number of OTUs and groups of endophytes on <italic>Populus</italic> are similar to those endophytic communities found in the rhizosphere of non-mycorrhizal <italic>Microthlaspi</italic> species (<xref rid="B55" ref-type="bibr">R Core Team, 2018</xref>). We hypothesize that these fungi are widespread in the rhizosphere of other plant species. Although some of the fungal taxa have been studied in pairwise situations with host plants (<xref rid="B11" ref-type="bibr">Bonito et al., 2017</xref>), the functioning of most of these species in multi-species interactions and plant rhizospheres is still relatively unexplored (<xref rid="B63" ref-type="bibr">Vélez et al., 2017</xref>).</p><p>Network analyses provide a powerful tool for distilling information from large datasets to generate hypotheses on keystone taxa that impact the assembly and functioning of multi-kingdom microbiome communities (<xref rid="B35" ref-type="bibr">Hoppe et al., 2014</xref>). Multi-Kingdom hypotheses generated through network analyses can then be tested directly through various experimental approaches, including through baiting or manipulative experiments (<xref rid="B28" ref-type="bibr">Ghodsalavi et al., 2017</xref>). Such an approach was used to study the phyllosphere microbiome of <italic>Arabidopsis thaliana</italic>. Manipulation of the pathogenic oomycete <italic>Albugo</italic>, a “hub” taxa with high inter-connectivity with other taxa, was shown to have dramatic impacts on the assembly of epiphytic and endophytic bacterial communities (<xref rid="B1" ref-type="bibr">Agler et al., 2016</xref>). Constructed fungal-bacterial communities in our study helped to identify hub taxa, having a high degree of connectivity (<xref ref-type="supplementary-material" rid="SM5">Supplementary Figure S5</xref>), which included a higher number of bacteria (e.g., <italic>Leptospira, Cytophagaceae, Chitinophagaceae, Micromonosporaceae</italic>) compared to fungi (e.g., <italic>Geopora</italic>, <italic>Fusarium</italic>, Sordariomycete) (<xref ref-type="supplementary-material" rid="SM16">Supplementary Table S8</xref>), and a few bridge taxa that have a high betweenness distribution. Network analysis also helped to identify microbial taxa that correlate with particular plant genotypes, soils, and soil characters (e.g., % Ca) (<xref ref-type="fig" rid="F5">Figure 5</xref>–<xref ref-type="fig" rid="F10">10</xref>). Hub and bridge taxa did not overlap between the two conducted experiments, possibly due to the fact that there was no overlap in plant genotype or soils between the two experiments. Over-represented taxa in microbial networks were disproportionately organisms representing different ecological guilds (e.g., saprotrophs, pathogens, ectomycorrhizal, arbuscular mycorrhizal); however, the taxonomic identification of many of these taxa is stuffiest to make strong ecological predictions. Although many indicator fungal species were ectomycorrhizal taxa, most ectomycorrhizal taxa belonged to different networks, comprised of different 16S OTUs, indicating that the rhizobiome niche may be partitioned in between different niches comprised of alternate sets of microbial consortia. Identifying and understanding the function of keystone microbial species in plant microbiomes offers new approaches for managing plant microbiomes for health and sustainability.</p></sec><sec><title>Conclusion</title><p>Data from two experiments provide assessments on impacts of soil and <italic>Populus’</italic> genotype on fungal and bacterial communities comprising the rhizobiome. The impact of host genotype on the composition of root microbial communities was stronger for bacteria than for fungi, and was dependent upon the particular soil the plants were grown in. In contrast, soil origin was shown to be a significant factor driving the composition of fungal and bacterial communities and networks in <italic>Populus</italic> roots, which was previously reported (<xref rid="B69" ref-type="bibr">Bonito et al., 2014</xref>; <xref rid="B16" ref-type="bibr">Cregger et al., 2018</xref>). Soil physicochemical parameters including texture and calcium concentration contribute to this soil effect, but other unmeasured factors likely play a role in the <italic>Populus</italic> root microbiome assembly. Importantly, uninoculated control plants were distinct from communities on treatment plants indicating that results are not due to methodological artifacts. Finally, network analyses identified fungal-bacterial consortia that were statistically overrepresented in the dataset, providing hypotheses for testing and a framework for expanding this research from mesocosms to the field.</p></sec><sec sec-type="data-availability"><title>Data Availability</title><p>The 454 sequences have been submitted to GenBank’s sequence read archive under the study accession number <ext-link ext-link-type="DDBJ/EMBL/GenBank" xlink:href="SRP106691">SRP106691</ext-link>.</p></sec><sec><title>Author Contributions</title><p>GB, RV, KH, CS, and K-HC contributed to the experimental design and carrying out the experiments. GB, GMNB, PJ, DW, DJ carried out the data and statistical analysis. All authors contributed to the writing of this manuscript.</p></sec><sec><title>Conflict of Interest Statement</title><p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p></sec></body><back><fn-group><fn fn-type="financial-disclosure"><p><bold>Funding.</bold> This research was sponsored by the Genomic Science Program, U.S. Department of Energy, Office of Science – Biological and Environmental Research as part of the Plant Microbe Interfaces Scientific Focus Area (<ext-link ext-link-type="uri" xlink:href="http://pmi.ornl.gov">http://pmi.ornl.gov</ext-link>). Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the U.S. Department of Energy under contract DE-AC05-00OR22725. GB and GMNB were supported through the Michigan State University AgBioResearch project MICL02416 and USDA NIFA project MICL08541. GB and GMNB also acknowledge NSF grant DEB-1441728 and the DOE Office of Science Great Lakes BioEnergy Research Center BER DE-SC0018409.</p></fn></fn-group><ack><p>The authors would like to thank Lee Gunter, Jud Isebrands, Zachary Moore, Paul Bloese and Bernard McMahon for supplying <italic>Populus</italic> cuttings, and Natalie Vande Pol for bioinformatic assistance. The authors of the manuscript are employed by Oak Ridge National Laboratory, which is managed by UT-Battelle, LLC, for the U.S. Department of Energy under contract DE-AC05- 00OR22725.</p></ack><fn-group><fn id="fn01"><label>1</label><p><ext-link ext-link-type="uri" xlink:href="http://aesl.ces.uga.edu/">http://aesl.ces.uga.edu/</ext-link></p></fn><fn id="fn02"><label>2</label><p><ext-link ext-link-type="uri" xlink:href="http://www.cpan.org/">http://www.cpan.org/</ext-link></p></fn><fn id="fn03"><label>3</label><p><ext-link ext-link-type="uri" xlink:href="http://www.cpan.org/">http://www.cpan.org/</ext-link></p></fn></fn-group><sec sec-type="supplementary material"><title>Supplementary Material</title><p>The Supplementary Material for this article can be found online at: <ext-link ext-link-type="uri" xlink:href="https://www.frontiersin.org/articles/10.3389/fmicb.2019.00481/full#supplementary-material">https://www.frontiersin.org/articles/10.3389/fmicb.2019.00481/full#supplementary-material</ext-link></p><supplementary-material content-type="local-data" id="SM1"><label>Figure S1</label><caption><p>Rarefaction curves for ITS and 16S rDNA from Experiments 1 and 2.</p></caption><media xlink:href="Image_1.pdf"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM2"><label>Figure S2</label><caption><p>Contingency table used in the calculation of Fisher Exact Tests. Each mij is entry ij of an operational taxonomic unit (out) matrix/binned OTU matrix M.</p></caption><media xlink:href="Image_2.pdf"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM3"><label>Figure S3</label><caption><p>Boxplots showing the relative abundance of fungi and bacteria across different hierarchical classification for the two experiments. <bold>(A)</bold> Fungi across different soils (Experiment 2: Soil origin); <bold>(B)</bold> Fungi across different Populus genotypes; <bold>(C)</bold> Bacteria across different soils (Experiment 2: Soil origin); <bold>(D)</bold> Bacteria across different Populus genotypes.</p></caption><media xlink:href="Image_3.tif"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM4"><label>Figure S4</label><caption><p>Raw bipartite networks representing the occurrence of operational taxonomic units (OTUs) within samples for Experiment 1: Plant genotype. Sample nodes are colored by <bold>(A)</bold> genotype and <bold>(B)</bold> soil. Samples clearly separate by soil and not be genotype.</p></caption><media xlink:href="Image_4.pdf"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM5"><label>Figure S5</label><caption><p>Enrichment of operational taxonomic units (OTUs) in genotypes, within each soil. OTU nodes are connected to genotype nodes via colored “soil specific” edges. An edge between an OTU and a genotype represents that the OTU is enriched in that genotype within the soil denoted by the edge color. One can clearly see that the enrichment of OTUs in genotypes is very heavilty influenced by the soil in which the genotype was grown.</p></caption><media xlink:href="Image_5.pdf"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM6"><label>Figure S6</label><caption><p>Distributions of selected network topology measures for the Experiment 1 operational taxonomic unit (OTU) correlation network.</p></caption><media xlink:href="Image_6.pdf"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM7"><label>Figure S7</label><caption><p>Distributions of selected network topology measures for the Experiment 2 operational taxonomic unit (OTU) correlation network.</p></caption><media xlink:href="Image_7.pdf"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM8"><label>Figure S8</label><caption><p>Correlation network maximum spanning tree of soil physicochemical and environmental parameters.</p></caption><media xlink:href="Image_8.pdf"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM9"><label>Table S1</label><caption><p>Characteristics of soils used in this study.</p></caption><media xlink:href="Table_1.xlsx"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM10"><label>Table S2</label><caption><p>Primer sequence information for 454 primers used in this study.</p></caption><media xlink:href="Table_2.xlsx"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM11"><label>Table S3</label><caption><p>Unique fungal operational taxonomic units (OTUs) recovered from uninoculated control plants.</p></caption><media xlink:href="Table_3.xlsx"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM12"><label>Table S4</label><caption><p>Degree of each operational taxonomic unit (OTU) in the Experiment 1 bipartite network, as well as the number of different genotypes the OTU is found in.</p></caption><media xlink:href="Table_4.xlsx"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM13"><label>Table S5</label><caption><p>Degree of each operational taxonomic unit (OTU) in the Experiment 1 enrichment network, the number of different genotypes the OTU is significantly enriched in, as well as the quotient of degree/#genotypes. The quotient gives an indication of how genotype-specific the OTU is.</p></caption><media xlink:href="Table_5.xlsx"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM14"><label>Table S6</label><caption><p>Operational taxonomic units (OTUs) assigned to Markov Cluster (MCL) communities for Experiment 1, as well as various network topology measures each OTU node in the pearson correlation network the communities were constructed from.</p></caption><media xlink:href="Table_6.xlsx"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM15"><label>Table S7</label><caption><p>Summary of the sizes of Markov Cluster (MCL) communities for Experiment 1, as we as the number of fungi vs bacterial members.</p></caption><media xlink:href="Table_7.xlsx"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM16"><label>Table S8</label><caption><p>Operational taxonomic units (OTUs) assigned to Markov Cluster (MCL) communities for Experiment 2, as well as various network topology measures each OTU node in the pearson correlation network the communities were constructed from.</p></caption><media xlink:href="Table_8.xlsx"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM17"><label>Table S9</label><caption><p>Summary of the sizes of Markov Cluster (MCL) communities for Experiment 2, as we as the number of fungi vs bacterial members.</p></caption><media xlink:href="Table_9.xlsx"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM18"><label>FILE S1</label><caption><p>Assessments of arbuscular mycorrhizal fungal diversity.</p></caption><media xlink:href="Data_Sheet_1.docx"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM19"><label>FILE S2</label><caption><p>Cytoscape session containing the networks for Experiment 1.</p></caption><media xlink:href="Data_Sheet_2.zip"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="SM20"><label>FILE S3</label><caption><p>Cytoscape session containing the networks for Experiment 2.</p></caption><media xlink:href="Data_Sheet_3.zip"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material></sec><ref-list><title>References</title><ref id="B1"><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Agler</surname><given-names>M. 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