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Metagenomic Profiling Reveals Lignocellulose Degrading System in a Microbial Community Associated with a Wood-Feeding Beetle

Identifieur interne : 000625 ( Pmc/Curation ); précédent : 000624; suivant : 000626

Metagenomic Profiling Reveals Lignocellulose Degrading System in a Microbial Community Associated with a Wood-Feeding Beetle

Auteurs : Erin D. Scully [États-Unis] ; Scott M. Geib [États-Unis] ; Kelli Hoover [États-Unis] ; Ming Tien [États-Unis] ; Susannah G. Tringe [États-Unis] ; Kerrie W. Barry [États-Unis] ; Tijana Glavina Del Rio [États-Unis] ; Mansi Chovatia [États-Unis] ; Joshua R. Herr [États-Unis] ; John E. Carlson [États-Unis, Corée du Sud]

Source :

RBID : PMC:3762729

Abstract

The Asian longhorned beetle (Anoplophoraglabripennis) is an invasive, wood-boring pest that thrives in the heartwood of deciduous tree species. A large impediment faced by A. glabripennis as it feeds on woody tissue is lignin, a highly recalcitrant biopolymer that reduces access to sugars and other nutrients locked in cellulose and hemicellulose. We previously demonstrated that lignin, cellulose, and hemicellulose are actively deconstructed in the beetle gut and that the gut harbors an assemblage of microbes hypothesized to make significant contributions to these processes. While lignin degrading mechanisms have been well characterized in pure cultures of white rot basidiomycetes, little is known about such processes in microbial communities associated with wood-feeding insects. The goals of this study were to develop a taxonomic and functional profile of a gut community derived from an invasive population of larval A. glabripennis collected from infested host trees and to identify genes that could be relevant for the digestion of woody tissue and nutrient acquisition. To accomplish this goal, we taxonomically and functionally characterized the A. glabripennis midgut microbiota through amplicon and shotgun metagenome sequencing and conducted a large-scale comparison with the metagenomes from a variety of other herbivore-associated communities. This analysis distinguished the A. glabripennis larval gut metagenome from the gut communities of other herbivores, including previously sequenced termite hindgut metagenomes. Genes encoding enzymes were identified in the A. glabripennis gut metagenome that could have key roles in woody tissue digestion including candidate lignin degrading genes (laccases, dye-decolorizing peroxidases, novel peroxidases and β-etherases), 36 families of glycoside hydrolases (such as cellulases and xylanases), and genes that could facilitate nutrient recovery, essential nutrient synthesis, and detoxification. This community could serve as a reservoir of novel enzymes to enhance industrial cellulosic biofuels production or targets for novel control methods for this invasive and highly destructive insect.


Url:
DOI: 10.1371/journal.pone.0073827
PubMed: 24023907
PubMed Central: 3762729

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<p>The Asian longhorned beetle (
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<named-content content-type="genus-species">
<named-content content-type="genus">Anoplophora</named-content>
<named-content content-type="species">glabripennis</named-content>
</named-content>
</named-content>
) is an invasive, wood-boring pest that thrives in the heartwood of deciduous tree species. A large impediment faced by
<named-content content-type="genus-species">
<named-content content-type="genus">A</named-content>
<italic>.
<named-content content-type="species">glabripennis</named-content>
</italic>
</named-content>
as it feeds on woody tissue is lignin, a highly recalcitrant biopolymer that reduces access to sugars and other nutrients locked in cellulose and hemicellulose. We previously demonstrated that lignin, cellulose, and hemicellulose are actively deconstructed in the beetle gut and that the gut harbors an assemblage of microbes hypothesized to make significant contributions to these processes. While lignin degrading mechanisms have been well characterized in pure cultures of white rot basidiomycetes, little is known about such processes in microbial communities associated with wood-feeding insects. The goals of this study were to develop a taxonomic and functional profile of a gut community derived from an invasive population of larval
<named-content content-type="genus-species">
<named-content content-type="genus">A</named-content>
<italic>.
<named-content content-type="species">glabripennis</named-content>
</italic>
</named-content>
collected from infested host trees and to identify genes that could be relevant for the digestion of woody tissue and nutrient acquisition. To accomplish this goal, we taxonomically and functionally characterized the
<named-content content-type="genus-species">
<named-content content-type="genus">A</named-content>
<italic>.
<named-content content-type="species">glabripennis</named-content>
</italic>
</named-content>
midgut microbiota through amplicon and shotgun metagenome sequencing and conducted a large-scale comparison with the metagenomes from a variety of other herbivore-associated communities. This analysis distinguished the
<italic>A</italic>
.
<italic>glabripennis</italic>
larval gut metagenome from the gut communities of other herbivores, including previously sequenced termite hindgut metagenomes. Genes encoding enzymes were identified in the
<named-content content-type="genus-species">
<named-content content-type="genus">A</named-content>
<italic>.
<named-content content-type="species">glabripennis</named-content>
</italic>
</named-content>
gut metagenome that could have key roles in woody tissue digestion including candidate lignin degrading genes (laccases, dye-decolorizing peroxidases, novel peroxidases and β-etherases), 36 families of glycoside hydrolases (such as cellulases and xylanases), and genes that could facilitate nutrient recovery, essential nutrient synthesis, and detoxification. This community could serve as a reservoir of novel enzymes to enhance industrial cellulosic biofuels production or targets for novel control methods for this invasive and highly destructive insect.</p>
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<name sortKey="Chu, C C" uniqKey="Chu C">C-C Chu</name>
</author>
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<name sortKey="Spencer, Jl" uniqKey="Spencer J">JL Spencer</name>
</author>
<author>
<name sortKey="Curzi, Mj" uniqKey="Curzi M">MJ Curzi</name>
</author>
<author>
<name sortKey="Zavala, Ja" uniqKey="Zavala J">JA Zavala</name>
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<name sortKey="Seufferheld, Mj" uniqKey="Seufferheld M">MJ Seufferheld</name>
</author>
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<name sortKey="Lehman, Rm" uniqKey="Lehman R">RM Lehman</name>
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<name sortKey="Lundgren, Jg" uniqKey="Lundgren J">JG Lundgren</name>
</author>
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<name sortKey="Petzke, Lm" uniqKey="Petzke L">LM Petzke</name>
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</TEI>
<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group>
<journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher>
<publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">24023907</article-id>
<article-id pub-id-type="pmc">3762729</article-id>
<article-id pub-id-type="publisher-id">PONE-D-13-13077</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0073827</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Metagenomic Profiling Reveals Lignocellulose Degrading System in a Microbial Community Associated with a Wood-Feeding Beetle</article-title>
<alt-title alt-title-type="running-head">Metagenomic Profiling of a Wood-Boring Beetle</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Scully</surname>
<given-names>Erin D.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Geib</surname>
<given-names>Scott M.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Hoover</surname>
<given-names>Kelli</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Tien</surname>
<given-names>Ming</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Tringe</surname>
<given-names>Susannah G.</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Barry</surname>
<given-names>Kerrie W.</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Glavina del Rio</surname>
<given-names>Tijana</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Chovatia</surname>
<given-names>Mansi</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Herr</surname>
<given-names>Joshua R.</given-names>
</name>
<xref ref-type="aff" rid="aff6">
<sup>6</sup>
</xref>
<xref ref-type="aff" rid="aff7">
<sup>7</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Carlson</surname>
<given-names>John E.</given-names>
</name>
<xref ref-type="aff" rid="aff7">
<sup>7</sup>
</xref>
<xref ref-type="aff" rid="aff8">
<sup>8</sup>
</xref>
<xref ref-type="corresp" rid="cor1">
<sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1">
<label>1</label>
<addr-line>Intercollege Graduate Program in Genetics, Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, Pennsylvania, United States of America</addr-line>
</aff>
<aff id="aff2">
<label>2</label>
<addr-line>Tropical Crop and Commodity Protection Research Unit, United States Department of Agriculture Agriculture Research Service Pacific Basin Agricultural Research Center, Hilo, Hawaii, United States of America</addr-line>
</aff>
<aff id="aff3">
<label>3</label>
<addr-line>Department of Entomology and Center for Chemical Ecology, The Pennsylvania State University, University Park, Pennsylvania, United States of America</addr-line>
</aff>
<aff id="aff4">
<label>4</label>
<addr-line>Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania, United States of America</addr-line>
</aff>
<aff id="aff5">
<label>5</label>
<addr-line>Department of Energy (DOE) Joint Genome Institute, Walnut Creek, California, United States of America</addr-line>
</aff>
<aff id="aff6">
<label>6</label>
<addr-line>Intercollege Graduate Program in Plant Biology, Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, Pennsylvania, United States of America</addr-line>
</aff>
<aff id="aff7">
<label>7</label>
<addr-line>The Schatz Center for Tree Molecular Genetics, Department of Ecosystem Science and Management, The Pennsylvania State University, University Park, Pennsylvania, United States of America</addr-line>
</aff>
<aff id="aff8">
<label>8</label>
<addr-line>Department of Bioenergy Science and Technology, Chonnam National University, Gwangju, South Korea</addr-line>
</aff>
<contrib-group>
<contrib contrib-type="editor">
<name>
<surname>Oliveira</surname>
<given-names>Pedro Lagerblad</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">
<addr-line>Universidade Federal do Rio de Janeiro, Brazil</addr-line>
</aff>
<author-notes>
<corresp id="cor1">* E-mail:
<email>jec16@psu.edu</email>
</corresp>
<fn fn-type="conflict">
<p>
<bold>Competing Interests: </bold>
The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con">
<p>Conceived and designed the experiments: EDS KH MT SGT JEC. Performed the experiments: EDS SMG SGT TGdR MC KWB. Analyzed the data: EDS SMG JRH. Contributed reagents/materials/analysis tools: EDS SMG KH JEC. Wrote the manuscript: EDS SMG KH MT JEC. </p>
</fn>
</author-notes>
<pub-date pub-type="collection">
<year>2013</year>
</pub-date>
<pub-date pub-type="epub">
<day>4</day>
<month>9</month>
<year>2013</year>
</pub-date>
<volume>8</volume>
<issue>9</issue>
<elocation-id>e73827</elocation-id>
<history>
<date date-type="received">
<day>29</day>
<month>3</month>
<year>2013</year>
</date>
<date date-type="accepted">
<day>25</day>
<month>7</month>
<year>2013</year>
</date>
</history>
<permissions>
<copyright-year>2013</copyright-year>
<license>
<license-p>This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.</license-p>
</license>
</permissions>
<abstract>
<p>The Asian longhorned beetle (
<named-content content-type="genus-species">
<named-content content-type="genus-species">
<named-content content-type="genus">Anoplophora</named-content>
<named-content content-type="species">glabripennis</named-content>
</named-content>
</named-content>
) is an invasive, wood-boring pest that thrives in the heartwood of deciduous tree species. A large impediment faced by
<named-content content-type="genus-species">
<named-content content-type="genus">A</named-content>
<italic>.
<named-content content-type="species">glabripennis</named-content>
</italic>
</named-content>
as it feeds on woody tissue is lignin, a highly recalcitrant biopolymer that reduces access to sugars and other nutrients locked in cellulose and hemicellulose. We previously demonstrated that lignin, cellulose, and hemicellulose are actively deconstructed in the beetle gut and that the gut harbors an assemblage of microbes hypothesized to make significant contributions to these processes. While lignin degrading mechanisms have been well characterized in pure cultures of white rot basidiomycetes, little is known about such processes in microbial communities associated with wood-feeding insects. The goals of this study were to develop a taxonomic and functional profile of a gut community derived from an invasive population of larval
<named-content content-type="genus-species">
<named-content content-type="genus">A</named-content>
<italic>.
<named-content content-type="species">glabripennis</named-content>
</italic>
</named-content>
collected from infested host trees and to identify genes that could be relevant for the digestion of woody tissue and nutrient acquisition. To accomplish this goal, we taxonomically and functionally characterized the
<named-content content-type="genus-species">
<named-content content-type="genus">A</named-content>
<italic>.
<named-content content-type="species">glabripennis</named-content>
</italic>
</named-content>
midgut microbiota through amplicon and shotgun metagenome sequencing and conducted a large-scale comparison with the metagenomes from a variety of other herbivore-associated communities. This analysis distinguished the
<italic>A</italic>
.
<italic>glabripennis</italic>
larval gut metagenome from the gut communities of other herbivores, including previously sequenced termite hindgut metagenomes. Genes encoding enzymes were identified in the
<named-content content-type="genus-species">
<named-content content-type="genus">A</named-content>
<italic>.
<named-content content-type="species">glabripennis</named-content>
</italic>
</named-content>
gut metagenome that could have key roles in woody tissue digestion including candidate lignin degrading genes (laccases, dye-decolorizing peroxidases, novel peroxidases and β-etherases), 36 families of glycoside hydrolases (such as cellulases and xylanases), and genes that could facilitate nutrient recovery, essential nutrient synthesis, and detoxification. This community could serve as a reservoir of novel enzymes to enhance industrial cellulosic biofuels production or targets for novel control methods for this invasive and highly destructive insect.</p>
</abstract>
<funding-group>
<funding-statement>Funding for this project was provided by USDA-NRI-CRSEES grant 2008-35504-04464, USDA-NRI-CREES grant 2009-35302-05286, the Alphawood Foundation, a Seed Grant to KH from the Pennsylvania State University College of Agricultural Sciences, and a Microbial Genomics Fellowship from USDA-AFRI to EDS and JRH. JEC was partially supported by World Class University Project R31-2009-000-20025-0 grant from the Ministry of Education, Science and Technology of South Korea. Opinions, findings, conclusions or recommendations expressed in this publication are those of the authors and do not necessarily reflect the views of the USDA. USDA is an equal opportunity provider and employer. The work conducted by the U.S. Department of Energy Joint Genome Institute is supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. The funders had no role in study design, data collection, and analysis, decision to publish, or preparation of the manuscript. </funding-statement>
</funding-group>
</article-meta>
</front>
</pmc>
</record>

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