Cellulose-degrading bacteria associated with the invasive woodwasp Sirex noctilio
Sirex noctilio is an invasive wood-feeding wasp that threatens the world's commercial and natural pine forests. Successful tree colonization by this insect is contingent on the decline of host defenses and the ability to utilize the woody substrate as a source of energy. We explored its potenti...
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creator | Adams, Aaron S Jordan, Michelle S Adams, Sandye M Suen, Garret Goodwin, Lynne A Davenport, Karen W Currie, Cameron R Raffa, Kenneth F |
description | Sirex noctilio
is an invasive wood-feeding wasp that threatens the world's commercial and natural pine forests. Successful tree colonization by this insect is contingent on the decline of host defenses and the ability to utilize the woody substrate as a source of energy. We explored its potential association with bacterial symbionts that may assist in nutrient acquisition via plant biomass deconstruction using growth assays, culture-dependent and -independent analysis of bacterial frequency of association and whole-genome analysis. We identified
Streptomyces
and γ-Proteobacteria that were each associated with 94% and 88% of wasps, respectively.
Streptomyces
isolates grew on all three cellulose substrates tested and across a range of pH 5.6 to 9. On the basis of whole-genome sequencing, three
Streptomyces
isolates have some of the highest proportions of genes predicted to encode for carbohydrate-active enzymes (CAZyme) of sequenced Actinobacteria. γ-Proteobacteria isolates grew on a cellulose derivative and a structurally diverse substrate, ammonia fiber explosion-treated corn stover, but not on microcrystalline cellulose. Analysis of the genome of a
Pantoea
isolate detected genes putatively encoding for CAZymes, the majority predicted to be active on hemicellulose and more simple sugars. We propose that a consortium of microorganisms, including the described bacteria and the fungal symbiont
Amylostereum areolatum
, has complementary functions for degrading woody substrates and that such degradation may assist in nutrient acquisition by
S. noctilio
, thus contributing to its ability to be established in forested habitats worldwide. |
doi_str_mv | 10.1038/ismej.2011.14 |
format | Article |
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is an invasive wood-feeding wasp that threatens the world's commercial and natural pine forests. Successful tree colonization by this insect is contingent on the decline of host defenses and the ability to utilize the woody substrate as a source of energy. We explored its potential association with bacterial symbionts that may assist in nutrient acquisition via plant biomass deconstruction using growth assays, culture-dependent and -independent analysis of bacterial frequency of association and whole-genome analysis. We identified
Streptomyces
and γ-Proteobacteria that were each associated with 94% and 88% of wasps, respectively.
Streptomyces
isolates grew on all three cellulose substrates tested and across a range of pH 5.6 to 9. On the basis of whole-genome sequencing, three
Streptomyces
isolates have some of the highest proportions of genes predicted to encode for carbohydrate-active enzymes (CAZyme) of sequenced Actinobacteria. γ-Proteobacteria isolates grew on a cellulose derivative and a structurally diverse substrate, ammonia fiber explosion-treated corn stover, but not on microcrystalline cellulose. Analysis of the genome of a
Pantoea
isolate detected genes putatively encoding for CAZymes, the majority predicted to be active on hemicellulose and more simple sugars. We propose that a consortium of microorganisms, including the described bacteria and the fungal symbiont
Amylostereum areolatum
, has complementary functions for degrading woody substrates and that such degradation may assist in nutrient acquisition by
S. noctilio
, thus contributing to its ability to be established in forested habitats worldwide.</description><identifier>ISSN: 1751-7362</identifier><identifier>ISSN: 1751-7370</identifier><identifier>EISSN: 1751-7370</identifier><identifier>DOI: 10.1038/ismej.2011.14</identifier><identifier>PMID: 21368904</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/158/2178 ; 631/158/853 ; 631/326/2565/547 ; 631/326/41 ; Actinobacteria ; Ammonia ; Animals ; Bacteria ; Bacteria - classification ; Bacteria - genetics ; Bacteria - isolation & purification ; Bacteria - metabolism ; Basidiomycota - genetics ; Basidiomycota - isolation & purification ; Basidiomycota - metabolism ; Biodegradation ; Biomass ; Biomedical and Life Sciences ; Cellulose ; Cellulose - metabolism ; Colonization ; Coniferous forests ; Corn ; Ecology ; Energy ; Enzymes ; Evolutionary Biology ; Fibers ; Forests ; Genomes ; Habitat ; hemicellulose ; Hymenoptera ; Insects ; Larva - microbiology ; Life Sciences ; Microbial Ecology ; Microbial Genetics and Genomics ; Microbiology ; Microorganisms ; Noctilio ; Nutrients ; Original ; original-article ; pH effects ; Plant biomass ; Sirex ; Stover ; Streptomyces ; Streptomyces - genetics ; Streptomyces - isolation & purification ; Streptomyces - metabolism ; Substrates ; Sugar ; Symbionts ; Trees ; Trees - microbiology ; Wasps - growth & development ; Wasps - microbiology ; Wood</subject><ispartof>The ISME Journal, 2011-08, Vol.5 (8), p.1323-1331</ispartof><rights>International Society for Microbial Ecology 2011</rights><rights>Copyright Nature Publishing Group Aug 2011</rights><rights>Copyright © 2011 International Society for Microbial Ecology 2011 International Society for Microbial Ecology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c512t-ed8116ff563bf4265096eaf6af78480a87ec01654c3da07c19a353ec2c1674b93</citedby><cites>FETCH-LOGICAL-c512t-ed8116ff563bf4265096eaf6af78480a87ec01654c3da07c19a353ec2c1674b93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3146269/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3146269/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27903,27904,53770,53772</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21368904$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/biblio/1152885$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Adams, Aaron S</creatorcontrib><creatorcontrib>Jordan, Michelle S</creatorcontrib><creatorcontrib>Adams, Sandye M</creatorcontrib><creatorcontrib>Suen, Garret</creatorcontrib><creatorcontrib>Goodwin, Lynne A</creatorcontrib><creatorcontrib>Davenport, Karen W</creatorcontrib><creatorcontrib>Currie, Cameron R</creatorcontrib><creatorcontrib>Raffa, Kenneth F</creatorcontrib><creatorcontrib>Great Lakes Bioenergy Research Center (GLBRC)</creatorcontrib><title>Cellulose-degrading bacteria associated with the invasive woodwasp Sirex noctilio</title><title>The ISME Journal</title><addtitle>ISME J</addtitle><addtitle>ISME J</addtitle><description>Sirex noctilio
is an invasive wood-feeding wasp that threatens the world's commercial and natural pine forests. Successful tree colonization by this insect is contingent on the decline of host defenses and the ability to utilize the woody substrate as a source of energy. We explored its potential association with bacterial symbionts that may assist in nutrient acquisition via plant biomass deconstruction using growth assays, culture-dependent and -independent analysis of bacterial frequency of association and whole-genome analysis. We identified
Streptomyces
and γ-Proteobacteria that were each associated with 94% and 88% of wasps, respectively.
Streptomyces
isolates grew on all three cellulose substrates tested and across a range of pH 5.6 to 9. On the basis of whole-genome sequencing, three
Streptomyces
isolates have some of the highest proportions of genes predicted to encode for carbohydrate-active enzymes (CAZyme) of sequenced Actinobacteria. γ-Proteobacteria isolates grew on a cellulose derivative and a structurally diverse substrate, ammonia fiber explosion-treated corn stover, but not on microcrystalline cellulose. Analysis of the genome of a
Pantoea
isolate detected genes putatively encoding for CAZymes, the majority predicted to be active on hemicellulose and more simple sugars. We propose that a consortium of microorganisms, including the described bacteria and the fungal symbiont
Amylostereum areolatum
, has complementary functions for degrading woody substrates and that such degradation may assist in nutrient acquisition by
S. noctilio
, thus contributing to its ability to be established in forested habitats worldwide.</description><subject>631/158/2178</subject><subject>631/158/853</subject><subject>631/326/2565/547</subject><subject>631/326/41</subject><subject>Actinobacteria</subject><subject>Ammonia</subject><subject>Animals</subject><subject>Bacteria</subject><subject>Bacteria - classification</subject><subject>Bacteria - genetics</subject><subject>Bacteria - isolation & purification</subject><subject>Bacteria - metabolism</subject><subject>Basidiomycota - genetics</subject><subject>Basidiomycota - isolation & purification</subject><subject>Basidiomycota - metabolism</subject><subject>Biodegradation</subject><subject>Biomass</subject><subject>Biomedical and Life Sciences</subject><subject>Cellulose</subject><subject>Cellulose - metabolism</subject><subject>Colonization</subject><subject>Coniferous forests</subject><subject>Corn</subject><subject>Ecology</subject><subject>Energy</subject><subject>Enzymes</subject><subject>Evolutionary Biology</subject><subject>Fibers</subject><subject>Forests</subject><subject>Genomes</subject><subject>Habitat</subject><subject>hemicellulose</subject><subject>Hymenoptera</subject><subject>Insects</subject><subject>Larva - microbiology</subject><subject>Life Sciences</subject><subject>Microbial Ecology</subject><subject>Microbial Genetics and Genomics</subject><subject>Microbiology</subject><subject>Microorganisms</subject><subject>Noctilio</subject><subject>Nutrients</subject><subject>Original</subject><subject>original-article</subject><subject>pH effects</subject><subject>Plant biomass</subject><subject>Sirex</subject><subject>Stover</subject><subject>Streptomyces</subject><subject>Streptomyces - genetics</subject><subject>Streptomyces - isolation & purification</subject><subject>Streptomyces - metabolism</subject><subject>Substrates</subject><subject>Sugar</subject><subject>Symbionts</subject><subject>Trees</subject><subject>Trees - microbiology</subject><subject>Wasps - growth & development</subject><subject>Wasps - microbiology</subject><subject>Wood</subject><issn>1751-7362</issn><issn>1751-7370</issn><issn>1751-7370</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kc2LE0EQxQdxcdfVo1cZvOhlYld_z0VYwvoBCyLquen01CQdJt2xuydx_3snZs2uIJ6qoH68R71XVS-AzIAw_dbnDa5nlADMgD-qLkAJaBRT5PFpl_S8eprzmhChpFRPqnMKTOqW8IvqyxyHYRxixqbDZbKdD8t6YV3B5G1tc47O24JdvfdlVZcV1j7sbPY7rPcxdnubt_VXn_BnHaIrfvDxWXXW2yHj87t5WX1_f_1t_rG5-fzh0_zqpnECaGmw0wCy74Vki55TKUgr0fbS9kpzTaxW6AhIwR3rLFEOWssEQ0cdSMUXLbus3h11t-Nig53DUJIdzDb5jU23Jlpv_r4EvzLLuDMMuKTyIPDqKBBz8SY7X9CtXAwBXTEAgmotJuj1nUuKP0bMxWx8dlNmNmAcs9FKUyW5IBP55r8kEOCk1SDJvfMJXccxhSmtSU9pPRXFJ6g5Qi7FnBP2p9eAmEP15nf15lC9gQP_8mEeJ_pP1xMwOwJ5OoUlpnvXfyv-AnUYupI</recordid><startdate>20110801</startdate><enddate>20110801</enddate><creator>Adams, Aaron S</creator><creator>Jordan, Michelle S</creator><creator>Adams, Sandye M</creator><creator>Suen, Garret</creator><creator>Goodwin, Lynne A</creator><creator>Davenport, Karen W</creator><creator>Currie, Cameron R</creator><creator>Raffa, Kenneth F</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QL</scope><scope>7SN</scope><scope>7ST</scope><scope>7T7</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PYCSY</scope><scope>SOI</scope><scope>7SS</scope><scope>7X8</scope><scope>OTOTI</scope><scope>5PM</scope></search><sort><creationdate>20110801</creationdate><title>Cellulose-degrading bacteria associated with the invasive woodwasp Sirex noctilio</title><author>Adams, Aaron S ; Jordan, Michelle S ; Adams, Sandye M ; Suen, Garret ; Goodwin, Lynne A ; Davenport, Karen W ; Currie, Cameron R ; Raffa, Kenneth F</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c512t-ed8116ff563bf4265096eaf6af78480a87ec01654c3da07c19a353ec2c1674b93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>631/158/2178</topic><topic>631/158/853</topic><topic>631/326/2565/547</topic><topic>631/326/41</topic><topic>Actinobacteria</topic><topic>Ammonia</topic><topic>Animals</topic><topic>Bacteria</topic><topic>Bacteria - classification</topic><topic>Bacteria - genetics</topic><topic>Bacteria - isolation & purification</topic><topic>Bacteria - metabolism</topic><topic>Basidiomycota - genetics</topic><topic>Basidiomycota - isolation & purification</topic><topic>Basidiomycota - metabolism</topic><topic>Biodegradation</topic><topic>Biomass</topic><topic>Biomedical and Life Sciences</topic><topic>Cellulose</topic><topic>Cellulose - metabolism</topic><topic>Colonization</topic><topic>Coniferous forests</topic><topic>Corn</topic><topic>Ecology</topic><topic>Energy</topic><topic>Enzymes</topic><topic>Evolutionary Biology</topic><topic>Fibers</topic><topic>Forests</topic><topic>Genomes</topic><topic>Habitat</topic><topic>hemicellulose</topic><topic>Hymenoptera</topic><topic>Insects</topic><topic>Larva - microbiology</topic><topic>Life Sciences</topic><topic>Microbial Ecology</topic><topic>Microbial Genetics and Genomics</topic><topic>Microbiology</topic><topic>Microorganisms</topic><topic>Noctilio</topic><topic>Nutrients</topic><topic>Original</topic><topic>original-article</topic><topic>pH effects</topic><topic>Plant biomass</topic><topic>Sirex</topic><topic>Stover</topic><topic>Streptomyces</topic><topic>Streptomyces - genetics</topic><topic>Streptomyces - isolation & purification</topic><topic>Streptomyces - metabolism</topic><topic>Substrates</topic><topic>Sugar</topic><topic>Symbionts</topic><topic>Trees</topic><topic>Trees - microbiology</topic><topic>Wasps - growth & development</topic><topic>Wasps - microbiology</topic><topic>Wood</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Adams, Aaron S</creatorcontrib><creatorcontrib>Jordan, Michelle S</creatorcontrib><creatorcontrib>Adams, Sandye M</creatorcontrib><creatorcontrib>Suen, Garret</creatorcontrib><creatorcontrib>Goodwin, Lynne A</creatorcontrib><creatorcontrib>Davenport, Karen W</creatorcontrib><creatorcontrib>Currie, Cameron R</creatorcontrib><creatorcontrib>Raffa, Kenneth F</creatorcontrib><creatorcontrib>Great Lakes Bioenergy Research Center (GLBRC)</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Environmental Science Collection</collection><collection>Environment Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>MEDLINE - Academic</collection><collection>OSTI.GOV</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The ISME Journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Adams, Aaron S</au><au>Jordan, Michelle S</au><au>Adams, Sandye M</au><au>Suen, Garret</au><au>Goodwin, Lynne A</au><au>Davenport, Karen W</au><au>Currie, Cameron R</au><au>Raffa, Kenneth F</au><aucorp>Great Lakes Bioenergy Research Center (GLBRC)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cellulose-degrading bacteria associated with the invasive woodwasp Sirex noctilio</atitle><jtitle>The ISME Journal</jtitle><stitle>ISME J</stitle><addtitle>ISME J</addtitle><date>2011-08-01</date><risdate>2011</risdate><volume>5</volume><issue>8</issue><spage>1323</spage><epage>1331</epage><pages>1323-1331</pages><issn>1751-7362</issn><issn>1751-7370</issn><eissn>1751-7370</eissn><abstract>Sirex noctilio
is an invasive wood-feeding wasp that threatens the world's commercial and natural pine forests. Successful tree colonization by this insect is contingent on the decline of host defenses and the ability to utilize the woody substrate as a source of energy. We explored its potential association with bacterial symbionts that may assist in nutrient acquisition via plant biomass deconstruction using growth assays, culture-dependent and -independent analysis of bacterial frequency of association and whole-genome analysis. We identified
Streptomyces
and γ-Proteobacteria that were each associated with 94% and 88% of wasps, respectively.
Streptomyces
isolates grew on all three cellulose substrates tested and across a range of pH 5.6 to 9. On the basis of whole-genome sequencing, three
Streptomyces
isolates have some of the highest proportions of genes predicted to encode for carbohydrate-active enzymes (CAZyme) of sequenced Actinobacteria. γ-Proteobacteria isolates grew on a cellulose derivative and a structurally diverse substrate, ammonia fiber explosion-treated corn stover, but not on microcrystalline cellulose. Analysis of the genome of a
Pantoea
isolate detected genes putatively encoding for CAZymes, the majority predicted to be active on hemicellulose and more simple sugars. We propose that a consortium of microorganisms, including the described bacteria and the fungal symbiont
Amylostereum areolatum
, has complementary functions for degrading woody substrates and that such degradation may assist in nutrient acquisition by
S. noctilio
, thus contributing to its ability to be established in forested habitats worldwide.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>21368904</pmid><doi>10.1038/ismej.2011.14</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record> |
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subjects | 631/158/2178 631/158/853 631/326/2565/547 631/326/41 Actinobacteria Ammonia Animals Bacteria Bacteria - classification Bacteria - genetics Bacteria - isolation & purification Bacteria - metabolism Basidiomycota - genetics Basidiomycota - isolation & purification Basidiomycota - metabolism Biodegradation Biomass Biomedical and Life Sciences Cellulose Cellulose - metabolism Colonization Coniferous forests Corn Ecology Energy Enzymes Evolutionary Biology Fibers Forests Genomes Habitat hemicellulose Hymenoptera Insects Larva - microbiology Life Sciences Microbial Ecology Microbial Genetics and Genomics Microbiology Microorganisms Noctilio Nutrients Original original-article pH effects Plant biomass Sirex Stover Streptomyces Streptomyces - genetics Streptomyces - isolation & purification Streptomyces - metabolism Substrates Sugar Symbionts Trees Trees - microbiology Wasps - growth & development Wasps - microbiology Wood |
title | Cellulose-degrading bacteria associated with the invasive woodwasp Sirex noctilio |
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