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Neotropical termite microbiomes as sources of novel plant cell wall degrading enzymes
In this study, we used shotgun metagenomic sequencing to characterise the microbial metabolic potential for lignocellulose transformation in the gut of two colonies of Argentine higher termite species with different feeding habits, Cortaritermes fulviceps and Nasutitermes aquilinus . Our goal was to...
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Published in: | Scientific reports 2020-03, Vol.10 (1), p.3864-3864, Article 3864 |
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creator | Romero Victorica, Matias Soria, Marcelo A. Batista-García, Ramón Alberto Ceja-Navarro, Javier A. Vikram, Surendra Ortiz, Maximiliano Ontañon, Ornella Ghio, Silvina Martínez-Ávila, Liliana Quintero García, Omar Jasiel Etcheverry, Clara Campos, Eleonora Cowan, Donald Arneodo, Joel Talia, Paola M. |
description | In this study, we used shotgun metagenomic sequencing to characterise the microbial metabolic potential for lignocellulose transformation in the gut of two colonies of Argentine higher termite species with different feeding habits,
Cortaritermes fulviceps
and
Nasutitermes aquilinus
. Our goal was to assess the microbial community compositions and metabolic capacity, and to identify genes involved in lignocellulose degradation. Individuals from both termite species contained the same five dominant bacterial phyla (Spirochaetes, Firmicutes, Proteobacteria, Fibrobacteres and Bacteroidetes) although with different relative abundances. However, detected functional capacity varied, with
C. fulviceps
(a grass-wood-feeder) gut microbiome samples containing more genes related to amino acid metabolism, whereas
N. aquilinus
(a wood-feeder) gut microbiome samples were enriched in genes involved in carbohydrate metabolism and cellulose degradation. The
C. fulviceps
gut microbiome was enriched specifically in genes coding for debranching- and oligosaccharide-degrading enzymes. These findings suggest an association between the primary food source and the predicted categories of the enzymes present in the gut microbiomes of each species. To further investigate the termite microbiomes as sources of biotechnologically relevant glycosyl hydrolases, a putative GH10 endo-β-1,4-xylanase, Xyl10E, was cloned and expressed in
Escherichia coli
. Functional analysis of the recombinant metagenome-derived enzyme showed high specificity towards beechwood xylan (288.1 IU/mg), with the optimum activity at 50 °C and a pH-activity range from 5 to 10. These characteristics suggest that Xy110E may be a promising candidate for further development in lignocellulose deconstruction applications. |
doi_str_mv | 10.1038/s41598-020-60850-5 |
format | article |
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Cortaritermes fulviceps
and
Nasutitermes aquilinus
. Our goal was to assess the microbial community compositions and metabolic capacity, and to identify genes involved in lignocellulose degradation. Individuals from both termite species contained the same five dominant bacterial phyla (Spirochaetes, Firmicutes, Proteobacteria, Fibrobacteres and Bacteroidetes) although with different relative abundances. However, detected functional capacity varied, with
C. fulviceps
(a grass-wood-feeder) gut microbiome samples containing more genes related to amino acid metabolism, whereas
N. aquilinus
(a wood-feeder) gut microbiome samples were enriched in genes involved in carbohydrate metabolism and cellulose degradation. The
C. fulviceps
gut microbiome was enriched specifically in genes coding for debranching- and oligosaccharide-degrading enzymes. These findings suggest an association between the primary food source and the predicted categories of the enzymes present in the gut microbiomes of each species. To further investigate the termite microbiomes as sources of biotechnologically relevant glycosyl hydrolases, a putative GH10 endo-β-1,4-xylanase, Xyl10E, was cloned and expressed in
Escherichia coli
. Functional analysis of the recombinant metagenome-derived enzyme showed high specificity towards beechwood xylan (288.1 IU/mg), with the optimum activity at 50 °C and a pH-activity range from 5 to 10. These characteristics suggest that Xy110E may be a promising candidate for further development in lignocellulose deconstruction applications.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/s41598-020-60850-5</identifier><identifier>PMID: 32123275</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>38 ; 38/22 ; 38/77 ; 631/326/2565/2142 ; 631/61/514/2254 ; 82/80 ; 82/83 ; Amino acids ; Animals ; Bacteria - enzymology ; Bacteria - genetics ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; BASIC BIOLOGICAL SCIENCES ; Biodegradation ; Biotechnology ; Carbohydrate metabolism ; Cell Wall ; Cell walls ; Cellulose ; Cellulose - chemistry ; E coli ; Enzymes ; Food sources ; Gastrointestinal Microbiome - physiology ; Glycoside Hydrolases - genetics ; Glycoside Hydrolases - metabolism ; Glycosyl hydrolase ; Humanities and Social Sciences ; Intestinal microflora ; Isoptera - metabolism ; Isoptera - microbiology ; Lignocellulose ; Metabolism ; Metagenomics ; Microbiomes ; multidisciplinary ; Oligosaccharides ; Plant Cells ; Science ; Science (multidisciplinary) ; Species ; Species Specificity ; Termites ; Wood ; Xylan</subject><ispartof>Scientific reports, 2020-03, Vol.10 (1), p.3864-3864, Article 3864</ispartof><rights>The Author(s) 2020</rights><rights>This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>The Author(s) 2020. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c566t-894e9247a532cdf4f982a92f36dd57533dcdfa2c208f14813ad3ad77b1c8e48a3</citedby><cites>FETCH-LOGICAL-c566t-894e9247a532cdf4f982a92f36dd57533dcdfa2c208f14813ad3ad77b1c8e48a3</cites><orcidid>0000-0002-4481-7835 ; 0000-0001-8556-147X ; 0000-0002-2954-3477 ; 0000000244817835 ; 0000000229543477 ; 000000018556147X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2369855377/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2369855377?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32123275$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/servlets/purl/1615315$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Romero Victorica, Matias</creatorcontrib><creatorcontrib>Soria, Marcelo A.</creatorcontrib><creatorcontrib>Batista-García, Ramón Alberto</creatorcontrib><creatorcontrib>Ceja-Navarro, Javier A.</creatorcontrib><creatorcontrib>Vikram, Surendra</creatorcontrib><creatorcontrib>Ortiz, Maximiliano</creatorcontrib><creatorcontrib>Ontañon, Ornella</creatorcontrib><creatorcontrib>Ghio, Silvina</creatorcontrib><creatorcontrib>Martínez-Ávila, Liliana</creatorcontrib><creatorcontrib>Quintero García, Omar Jasiel</creatorcontrib><creatorcontrib>Etcheverry, Clara</creatorcontrib><creatorcontrib>Campos, Eleonora</creatorcontrib><creatorcontrib>Cowan, Donald</creatorcontrib><creatorcontrib>Arneodo, Joel</creatorcontrib><creatorcontrib>Talia, Paola M.</creatorcontrib><creatorcontrib>Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)</creatorcontrib><title>Neotropical termite microbiomes as sources of novel plant cell wall degrading enzymes</title><title>Scientific reports</title><addtitle>Sci Rep</addtitle><addtitle>Sci Rep</addtitle><description>In this study, we used shotgun metagenomic sequencing to characterise the microbial metabolic potential for lignocellulose transformation in the gut of two colonies of Argentine higher termite species with different feeding habits,
Cortaritermes fulviceps
and
Nasutitermes aquilinus
. Our goal was to assess the microbial community compositions and metabolic capacity, and to identify genes involved in lignocellulose degradation. Individuals from both termite species contained the same five dominant bacterial phyla (Spirochaetes, Firmicutes, Proteobacteria, Fibrobacteres and Bacteroidetes) although with different relative abundances. However, detected functional capacity varied, with
C. fulviceps
(a grass-wood-feeder) gut microbiome samples containing more genes related to amino acid metabolism, whereas
N. aquilinus
(a wood-feeder) gut microbiome samples were enriched in genes involved in carbohydrate metabolism and cellulose degradation. The
C. fulviceps
gut microbiome was enriched specifically in genes coding for debranching- and oligosaccharide-degrading enzymes. These findings suggest an association between the primary food source and the predicted categories of the enzymes present in the gut microbiomes of each species. To further investigate the termite microbiomes as sources of biotechnologically relevant glycosyl hydrolases, a putative GH10 endo-β-1,4-xylanase, Xyl10E, was cloned and expressed in
Escherichia coli
. Functional analysis of the recombinant metagenome-derived enzyme showed high specificity towards beechwood xylan (288.1 IU/mg), with the optimum activity at 50 °C and a pH-activity range from 5 to 10. These characteristics suggest that Xy110E may be a promising candidate for further development in lignocellulose deconstruction applications.</description><subject>38</subject><subject>38/22</subject><subject>38/77</subject><subject>631/326/2565/2142</subject><subject>631/61/514/2254</subject><subject>82/80</subject><subject>82/83</subject><subject>Amino acids</subject><subject>Animals</subject><subject>Bacteria - enzymology</subject><subject>Bacteria - genetics</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>Biodegradation</subject><subject>Biotechnology</subject><subject>Carbohydrate metabolism</subject><subject>Cell Wall</subject><subject>Cell walls</subject><subject>Cellulose</subject><subject>Cellulose - chemistry</subject><subject>E coli</subject><subject>Enzymes</subject><subject>Food sources</subject><subject>Gastrointestinal Microbiome - physiology</subject><subject>Glycoside Hydrolases - genetics</subject><subject>Glycoside Hydrolases - metabolism</subject><subject>Glycosyl hydrolase</subject><subject>Humanities and Social Sciences</subject><subject>Intestinal microflora</subject><subject>Isoptera - metabolism</subject><subject>Isoptera - microbiology</subject><subject>Lignocellulose</subject><subject>Metabolism</subject><subject>Metagenomics</subject><subject>Microbiomes</subject><subject>multidisciplinary</subject><subject>Oligosaccharides</subject><subject>Plant Cells</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Species</subject><subject>Species Specificity</subject><subject>Termites</subject><subject>Wood</subject><subject>Xylan</subject><issn>2045-2322</issn><issn>2045-2322</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><recordid>eNp9Ul1vFSEQJUZjm2v_gA-G6IsvqzDAAi8mpvEraepL-0y4LHtLswtX4Lapv16u2y99KJnAhDlzhhkOQq8p-UAJUx8Lp0KrjgDpeqIE6cQzdAiEiw4YwPNH_gE6KuWStCVAc6pfogMGtEWkOETnpz7VnLbB2QlXn-dQPZ6Dy2kd0uwLtgWXtMuuuWnEMV35CW8nGyt2fprwtW3b4DfZDiFusI-_b1rWK_RitFPxR7fnCp1__XJ2_L07-fntx_Hnk86Jvq-d0txr4NIKBm4Y-agVWA0j64dBSMHY0G4tOCBqpFxRZodmUq6pU54ry1bo08K73a1nPzgfa7aT2eYw23xjkg3m30gMF2aTroxss6CcN4K3C0EqNZjiWvfuwqUYvauG9lSwZiv0_rZKTr92vlQzh7Lv3kafdsUAk4RrDlo26Lv_oJdteLHNwIBkgjMKoJ9EsV4rIZjcc8GCap9RSvbjfV-UmL0GzKIB0zRg_mrA7N_65vFE7lPufrwB2AIoLRQ3Pj_UfoL2D--mvCA</recordid><startdate>20200302</startdate><enddate>20200302</enddate><creator>Romero Victorica, Matias</creator><creator>Soria, Marcelo A.</creator><creator>Batista-García, Ramón Alberto</creator><creator>Ceja-Navarro, Javier A.</creator><creator>Vikram, Surendra</creator><creator>Ortiz, Maximiliano</creator><creator>Ontañon, Ornella</creator><creator>Ghio, Silvina</creator><creator>Martínez-Ávila, Liliana</creator><creator>Quintero García, Omar Jasiel</creator><creator>Etcheverry, Clara</creator><creator>Campos, Eleonora</creator><creator>Cowan, Donald</creator><creator>Arneodo, Joel</creator><creator>Talia, Paola M.</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>C6C</scope><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>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</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>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>7X8</scope><scope>OIOZB</scope><scope>OTOTI</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-4481-7835</orcidid><orcidid>https://orcid.org/0000-0001-8556-147X</orcidid><orcidid>https://orcid.org/0000-0002-2954-3477</orcidid><orcidid>https://orcid.org/0000000244817835</orcidid><orcidid>https://orcid.org/0000000229543477</orcidid><orcidid>https://orcid.org/000000018556147X</orcidid></search><sort><creationdate>20200302</creationdate><title>Neotropical termite microbiomes as sources of novel plant cell wall degrading enzymes</title><author>Romero Victorica, Matias ; Soria, Marcelo A. ; Batista-García, Ramón Alberto ; Ceja-Navarro, Javier A. ; Vikram, Surendra ; Ortiz, Maximiliano ; Ontañon, Ornella ; Ghio, Silvina ; Martínez-Ávila, Liliana ; Quintero García, Omar Jasiel ; Etcheverry, Clara ; Campos, Eleonora ; Cowan, Donald ; Arneodo, Joel ; Talia, Paola M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c566t-894e9247a532cdf4f982a92f36dd57533dcdfa2c208f14813ad3ad77b1c8e48a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>38</topic><topic>38/22</topic><topic>38/77</topic><topic>631/326/2565/2142</topic><topic>631/61/514/2254</topic><topic>82/80</topic><topic>82/83</topic><topic>Amino acids</topic><topic>Animals</topic><topic>Bacteria - 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Academic</collection><collection>OSTI.GOV - Hybrid</collection><collection>OSTI.GOV</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Scientific reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Romero Victorica, Matias</au><au>Soria, Marcelo A.</au><au>Batista-García, Ramón Alberto</au><au>Ceja-Navarro, Javier A.</au><au>Vikram, Surendra</au><au>Ortiz, Maximiliano</au><au>Ontañon, Ornella</au><au>Ghio, Silvina</au><au>Martínez-Ávila, Liliana</au><au>Quintero García, Omar Jasiel</au><au>Etcheverry, Clara</au><au>Campos, Eleonora</au><au>Cowan, Donald</au><au>Arneodo, Joel</au><au>Talia, Paola M.</au><aucorp>Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Neotropical termite microbiomes as sources of novel plant cell wall degrading enzymes</atitle><jtitle>Scientific reports</jtitle><stitle>Sci Rep</stitle><addtitle>Sci Rep</addtitle><date>2020-03-02</date><risdate>2020</risdate><volume>10</volume><issue>1</issue><spage>3864</spage><epage>3864</epage><pages>3864-3864</pages><artnum>3864</artnum><issn>2045-2322</issn><eissn>2045-2322</eissn><abstract>In this study, we used shotgun metagenomic sequencing to characterise the microbial metabolic potential for lignocellulose transformation in the gut of two colonies of Argentine higher termite species with different feeding habits,
Cortaritermes fulviceps
and
Nasutitermes aquilinus
. Our goal was to assess the microbial community compositions and metabolic capacity, and to identify genes involved in lignocellulose degradation. Individuals from both termite species contained the same five dominant bacterial phyla (Spirochaetes, Firmicutes, Proteobacteria, Fibrobacteres and Bacteroidetes) although with different relative abundances. However, detected functional capacity varied, with
C. fulviceps
(a grass-wood-feeder) gut microbiome samples containing more genes related to amino acid metabolism, whereas
N. aquilinus
(a wood-feeder) gut microbiome samples were enriched in genes involved in carbohydrate metabolism and cellulose degradation. The
C. fulviceps
gut microbiome was enriched specifically in genes coding for debranching- and oligosaccharide-degrading enzymes. These findings suggest an association between the primary food source and the predicted categories of the enzymes present in the gut microbiomes of each species. To further investigate the termite microbiomes as sources of biotechnologically relevant glycosyl hydrolases, a putative GH10 endo-β-1,4-xylanase, Xyl10E, was cloned and expressed in
Escherichia coli
. Functional analysis of the recombinant metagenome-derived enzyme showed high specificity towards beechwood xylan (288.1 IU/mg), with the optimum activity at 50 °C and a pH-activity range from 5 to 10. These characteristics suggest that Xy110E may be a promising candidate for further development in lignocellulose deconstruction applications.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>32123275</pmid><doi>10.1038/s41598-020-60850-5</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-4481-7835</orcidid><orcidid>https://orcid.org/0000-0001-8556-147X</orcidid><orcidid>https://orcid.org/0000-0002-2954-3477</orcidid><orcidid>https://orcid.org/0000000244817835</orcidid><orcidid>https://orcid.org/0000000229543477</orcidid><orcidid>https://orcid.org/000000018556147X</orcidid><oa>free_for_read</oa></addata></record> |
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identifier | ISSN: 2045-2322 |
ispartof | Scientific reports, 2020-03, Vol.10 (1), p.3864-3864, Article 3864 |
issn | 2045-2322 2045-2322 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7052144 |
source | PubMed (Medline); Publicly Available Content Database; Free Full-Text Journals in Chemistry; Springer Nature - nature.com Journals - Fully Open Access |
subjects | 38 38/22 38/77 631/326/2565/2142 631/61/514/2254 82/80 82/83 Amino acids Animals Bacteria - enzymology Bacteria - genetics Bacterial Proteins - genetics Bacterial Proteins - metabolism BASIC BIOLOGICAL SCIENCES Biodegradation Biotechnology Carbohydrate metabolism Cell Wall Cell walls Cellulose Cellulose - chemistry E coli Enzymes Food sources Gastrointestinal Microbiome - physiology Glycoside Hydrolases - genetics Glycoside Hydrolases - metabolism Glycosyl hydrolase Humanities and Social Sciences Intestinal microflora Isoptera - metabolism Isoptera - microbiology Lignocellulose Metabolism Metagenomics Microbiomes multidisciplinary Oligosaccharides Plant Cells Science Science (multidisciplinary) Species Species Specificity Termites Wood Xylan |
title | Neotropical termite microbiomes as sources of novel plant cell wall degrading enzymes |
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