Broad phylogeny and functionality of cellulosomal components in the bovine rumen microbiome
Summary The cellulosome is an extracellular multi‐enzyme complex that is considered one of the most efficient plant cell wall‐degrading strategies devised by nature. Its unique modular architecture, achieved by high affinity and specific interaction between protein modules (cohesins and dockerins) e...
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creator | Bensoussan, Lizi Moraïs, Sarah Dassa, Bareket Friedman, Nir Henrissat, Bernard Lombard, Vincent Bayer, Edward A. Mizrahi, Itzhak |
description | Summary
The cellulosome is an extracellular multi‐enzyme complex that is considered one of the most efficient plant cell wall‐degrading strategies devised by nature. Its unique modular architecture, achieved by high affinity and specific interaction between protein modules (cohesins and dockerins) enables formation of various enzyme combinations. Extensive research has been dedicated to the mechanistic nature of the cellulosome complex. Nevertheless, little is known regarding its distribution and abundance among microbes in natural plant fibre‐rich environments. Here, we explored these questions in bovine rumen microbial communities, specialized in efficient degradation of lignocellulosic plant material. We bioinformatically screened for cellulosomal modules in this complex environment using a previously published ultra‐deep fibre‐adherent rumen metagenome. Intriguingly, a large portion of the functions of the dockerin‐containing proteins were related to alternative biological processes, and not necessarily to the classic fibre degradation function. Our analysis was experimentally validated by characterizing specific interactions between selected cohesins and dockerins and revealed that cellulosome is a more generalized strategy used by diverse bacteria, some of which were not previously associated with cellulosome production. Remarkably, our results provide additional proof of similarity among rumen microbial communities worldwide. This study suggests a broader and widespread role for the cellulosomal machinery in nature. |
doi_str_mv | 10.1111/1462-2920.13561 |
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The cellulosome is an extracellular multi‐enzyme complex that is considered one of the most efficient plant cell wall‐degrading strategies devised by nature. Its unique modular architecture, achieved by high affinity and specific interaction between protein modules (cohesins and dockerins) enables formation of various enzyme combinations. Extensive research has been dedicated to the mechanistic nature of the cellulosome complex. Nevertheless, little is known regarding its distribution and abundance among microbes in natural plant fibre‐rich environments. Here, we explored these questions in bovine rumen microbial communities, specialized in efficient degradation of lignocellulosic plant material. We bioinformatically screened for cellulosomal modules in this complex environment using a previously published ultra‐deep fibre‐adherent rumen metagenome. Intriguingly, a large portion of the functions of the dockerin‐containing proteins were related to alternative biological processes, and not necessarily to the classic fibre degradation function. Our analysis was experimentally validated by characterizing specific interactions between selected cohesins and dockerins and revealed that cellulosome is a more generalized strategy used by diverse bacteria, some of which were not previously associated with cellulosome production. Remarkably, our results provide additional proof of similarity among rumen microbial communities worldwide. This study suggests a broader and widespread role for the cellulosomal machinery in nature.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.13561</identifier><identifier>PMID: 27712009</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Animals ; Bacteria ; Bacteria - classification ; Bacteria - genetics ; Bacteria - isolation & purification ; Bacteria - metabolism ; Bacterial Proteins ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Biochemistry, Molecular Biology ; Biodiversity ; Cattle ; Cellulosomes ; Cellulosomes - enzymology ; Cellulosomes - genetics ; Enzymes ; Gastrointestinal Microbiome ; Life Sciences ; Metagenome ; Microbiology and Parasitology ; Multienzyme Complexes ; Multienzyme Complexes - genetics ; Multienzyme Complexes - metabolism ; Phylogeny ; Rumen ; Rumen - microbiology ; Systematics, Phylogenetics and taxonomy</subject><ispartof>Environmental microbiology, 2017-01, Vol.19 (1), p.185-197</ispartof><rights>2016 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd</rights><rights>2016 Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>2017 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c6001-16eba6e14ff1550a5b3fb1c045f3cd47e1afa035ebfbd21af21466b8eced24853</citedby><cites>FETCH-LOGICAL-c6001-16eba6e14ff1550a5b3fb1c045f3cd47e1afa035ebfbd21af21466b8eced24853</cites><orcidid>0000-0002-9684-7067</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2F1462-2920.13561$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.13561$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27712009$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01802735$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Bensoussan, Lizi</creatorcontrib><creatorcontrib>Moraïs, Sarah</creatorcontrib><creatorcontrib>Dassa, Bareket</creatorcontrib><creatorcontrib>Friedman, Nir</creatorcontrib><creatorcontrib>Henrissat, Bernard</creatorcontrib><creatorcontrib>Lombard, Vincent</creatorcontrib><creatorcontrib>Bayer, Edward A.</creatorcontrib><creatorcontrib>Mizrahi, Itzhak</creatorcontrib><title>Broad phylogeny and functionality of cellulosomal components in the bovine rumen microbiome</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
The cellulosome is an extracellular multi‐enzyme complex that is considered one of the most efficient plant cell wall‐degrading strategies devised by nature. Its unique modular architecture, achieved by high affinity and specific interaction between protein modules (cohesins and dockerins) enables formation of various enzyme combinations. Extensive research has been dedicated to the mechanistic nature of the cellulosome complex. Nevertheless, little is known regarding its distribution and abundance among microbes in natural plant fibre‐rich environments. Here, we explored these questions in bovine rumen microbial communities, specialized in efficient degradation of lignocellulosic plant material. We bioinformatically screened for cellulosomal modules in this complex environment using a previously published ultra‐deep fibre‐adherent rumen metagenome. Intriguingly, a large portion of the functions of the dockerin‐containing proteins were related to alternative biological processes, and not necessarily to the classic fibre degradation function. Our analysis was experimentally validated by characterizing specific interactions between selected cohesins and dockerins and revealed that cellulosome is a more generalized strategy used by diverse bacteria, some of which were not previously associated with cellulosome production. Remarkably, our results provide additional proof of similarity among rumen microbial communities worldwide. This study suggests a broader and widespread role for the cellulosomal machinery in nature.</description><subject>Animals</subject><subject>Bacteria</subject><subject>Bacteria - classification</subject><subject>Bacteria - genetics</subject><subject>Bacteria - isolation & purification</subject><subject>Bacteria - metabolism</subject><subject>Bacterial Proteins</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Biochemistry, Molecular Biology</subject><subject>Biodiversity</subject><subject>Cattle</subject><subject>Cellulosomes</subject><subject>Cellulosomes - enzymology</subject><subject>Cellulosomes - genetics</subject><subject>Enzymes</subject><subject>Gastrointestinal Microbiome</subject><subject>Life Sciences</subject><subject>Metagenome</subject><subject>Microbiology and Parasitology</subject><subject>Multienzyme Complexes</subject><subject>Multienzyme Complexes - genetics</subject><subject>Multienzyme Complexes - metabolism</subject><subject>Phylogeny</subject><subject>Rumen</subject><subject>Rumen - microbiology</subject><subject>Systematics, Phylogenetics and taxonomy</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNqNksFu1DAQhi0EomXhzA1Z4gKHpR47trMXpFIVWmkRFzhxsJxk3HWV2EucLMrb4zRlBb2AL_aMv_k9nhlCXgJ7B3mdQaH4mm94NoVU8IicHj2Pj2fgJ-RZSreMgRaaPSUnXGvgjG1OyfcPfbQN3e-mNt5gmKgNDXVjqAcfg239MNHoaI1tO7Yxxc62tI7dPgYMQ6I-0GGHtIoHH5D2Y4eBdr7uY-Vjh8_JE2fbhC_u9xX59vHy68XVevvl0_XF-XZdq5zSGhRWViEUzoGUzMpKuApqVkgn6qbQCNZZJiRWrmp4Nnj-l6pKrLHhRSnFirxfdPdj1WFT59R625p97zvbTyZab_6-CX5nbuLBqKLUG8WywNtFYPcg7Op8a2Yfg5JxLeQBMvvm_rE-_hgxDabzaa6PDRjHZKBUpWBaC_UfqJBCQ5m7siKvH6C3cexzA-4EQYgNgyJTZwuVK5xSj-6YLDAzz4OZO27m7pu7ecgRr_4szZH_PQAZkAvw07c4_UvPXH6-XoR_ATvrwB4</recordid><startdate>201701</startdate><enddate>201701</enddate><creator>Bensoussan, Lizi</creator><creator>Moraïs, Sarah</creator><creator>Dassa, Bareket</creator><creator>Friedman, Nir</creator><creator>Henrissat, Bernard</creator><creator>Lombard, Vincent</creator><creator>Bayer, Edward A.</creator><creator>Mizrahi, Itzhak</creator><general>Wiley Subscription Services, Inc</general><general>Society for Applied Microbiology and Wiley-Blackwell</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</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>7QH</scope><scope>7QL</scope><scope>7ST</scope><scope>7T7</scope><scope>7TN</scope><scope>7U9</scope><scope>7UA</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-9684-7067</orcidid></search><sort><creationdate>201701</creationdate><title>Broad phylogeny and functionality of cellulosomal components in the bovine rumen microbiome</title><author>Bensoussan, Lizi ; Moraïs, Sarah ; Dassa, Bareket ; Friedman, Nir ; Henrissat, Bernard ; Lombard, Vincent ; Bayer, Edward A. ; Mizrahi, Itzhak</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c6001-16eba6e14ff1550a5b3fb1c045f3cd47e1afa035ebfbd21af21466b8eced24853</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Animals</topic><topic>Bacteria</topic><topic>Bacteria - classification</topic><topic>Bacteria - genetics</topic><topic>Bacteria - isolation & purification</topic><topic>Bacteria - metabolism</topic><topic>Bacterial Proteins</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Biochemistry, Molecular Biology</topic><topic>Biodiversity</topic><topic>Cattle</topic><topic>Cellulosomes</topic><topic>Cellulosomes - enzymology</topic><topic>Cellulosomes - genetics</topic><topic>Enzymes</topic><topic>Gastrointestinal Microbiome</topic><topic>Life Sciences</topic><topic>Metagenome</topic><topic>Microbiology and Parasitology</topic><topic>Multienzyme Complexes</topic><topic>Multienzyme Complexes - genetics</topic><topic>Multienzyme Complexes - metabolism</topic><topic>Phylogeny</topic><topic>Rumen</topic><topic>Rumen - microbiology</topic><topic>Systematics, Phylogenetics and taxonomy</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bensoussan, Lizi</creatorcontrib><creatorcontrib>Moraïs, Sarah</creatorcontrib><creatorcontrib>Dassa, Bareket</creatorcontrib><creatorcontrib>Friedman, Nir</creatorcontrib><creatorcontrib>Henrissat, Bernard</creatorcontrib><creatorcontrib>Lombard, Vincent</creatorcontrib><creatorcontrib>Bayer, Edward A.</creatorcontrib><creatorcontrib>Mizrahi, Itzhak</creatorcontrib><collection>Wiley-Blackwell Open Access Titles</collection><collection>Wiley Free Content</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aqualine</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Oceanic Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Water Resources Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bensoussan, Lizi</au><au>Moraïs, Sarah</au><au>Dassa, Bareket</au><au>Friedman, Nir</au><au>Henrissat, Bernard</au><au>Lombard, Vincent</au><au>Bayer, Edward A.</au><au>Mizrahi, Itzhak</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Broad phylogeny and functionality of cellulosomal components in the bovine rumen microbiome</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2017-01</date><risdate>2017</risdate><volume>19</volume><issue>1</issue><spage>185</spage><epage>197</epage><pages>185-197</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
The cellulosome is an extracellular multi‐enzyme complex that is considered one of the most efficient plant cell wall‐degrading strategies devised by nature. Its unique modular architecture, achieved by high affinity and specific interaction between protein modules (cohesins and dockerins) enables formation of various enzyme combinations. Extensive research has been dedicated to the mechanistic nature of the cellulosome complex. Nevertheless, little is known regarding its distribution and abundance among microbes in natural plant fibre‐rich environments. Here, we explored these questions in bovine rumen microbial communities, specialized in efficient degradation of lignocellulosic plant material. We bioinformatically screened for cellulosomal modules in this complex environment using a previously published ultra‐deep fibre‐adherent rumen metagenome. Intriguingly, a large portion of the functions of the dockerin‐containing proteins were related to alternative biological processes, and not necessarily to the classic fibre degradation function. Our analysis was experimentally validated by characterizing specific interactions between selected cohesins and dockerins and revealed that cellulosome is a more generalized strategy used by diverse bacteria, some of which were not previously associated with cellulosome production. Remarkably, our results provide additional proof of similarity among rumen microbial communities worldwide. This study suggests a broader and widespread role for the cellulosomal machinery in nature.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>27712009</pmid><doi>10.1111/1462-2920.13561</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-9684-7067</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Bacteria Bacteria - classification Bacteria - genetics Bacteria - isolation & purification Bacteria - metabolism Bacterial Proteins Bacterial Proteins - genetics Bacterial Proteins - metabolism Biochemistry, Molecular Biology Biodiversity Cattle Cellulosomes Cellulosomes - enzymology Cellulosomes - genetics Enzymes Gastrointestinal Microbiome Life Sciences Metagenome Microbiology and Parasitology Multienzyme Complexes Multienzyme Complexes - genetics Multienzyme Complexes - metabolism Phylogeny Rumen Rumen - microbiology Systematics, Phylogenetics and taxonomy |
title | Broad phylogeny and functionality of cellulosomal components in the bovine rumen microbiome |
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