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Inference of phenotype-defining functional modules of protein families for microbial plant biomass degraders
BACKGROUND: Efficient industrial processes for converting plant lignocellulosic materials into biofuels are a key to global efforts to come up with alternative energy sources to fossil fuels. Novel cellulolytic enzymes have been discovered in microbial genomes and metagenomes of microbial communitie...
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Published in: | Biotechnology for biofuels 2014-09, Vol.7 (1), p.124-124, Article 124 |
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description | BACKGROUND: Efficient industrial processes for converting plant lignocellulosic materials into biofuels are a key to global efforts to come up with alternative energy sources to fossil fuels. Novel cellulolytic enzymes have been discovered in microbial genomes and metagenomes of microbial communities. However, the identification of relevant genes without known homologs, and the elucidation of the lignocellulolytic pathways and protein complexes for different microorganisms remain challenging. RESULTS: We describe a new computational method for the targeted discovery of functional modules of plant biomass-degrading protein families, based on their co-occurrence patterns across genomes and metagenome datasets, and the strength of association of these modules with the genomes of known degraders. From approximately 6.4 million family annotations for 2,884 microbial genomes, and 332 taxonomic bins from 18 metagenomes, we identified 5 functional modules that are distinctive for plant biomass degraders, which we term “plant biomass degradation modules” (PDMs). These modules incorporate protein families involved in the degradation of cellulose, hemicelluloses, and pectins, structural components of the cellulosome, and additional families with potential functions in plant biomass degradation. The PDMs were linked to 81 gene clusters in genomes of known lignocellulose degraders, including previously described clusters of lignocellulolytic genes. On average, 70% of the families of each PDM were found to map to gene clusters in known degraders, which served as an additional confirmation of their functional relationships. The presence of a PDM in a genome or taxonomic metagenome bin furthermore allowed us to accurately predict the ability of any particular organism to degrade plant biomass. For 15 draft genomes of a cow rumen metagenome, we used cross-referencing to confirmed cellulolytic enzymes to validate that the PDMs identified plant biomass degraders within a complex microbial community. CONCLUSIONS: Functional modules of protein families that are involved in different aspects of plant cell wall degradation can be inferred from co-occurrence patterns across (meta-)genomes with a probabilistic topic model. PDMs represent a new resource of protein families and candidate genes implicated in microbial plant biomass degradation. They can also be used to predict the plant biomass degradation ability for a genome or taxonomic bin. The method is also suitable for charact |
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Novel cellulolytic enzymes have been discovered in microbial genomes and metagenomes of microbial communities. However, the identification of relevant genes without known homologs, and the elucidation of the lignocellulolytic pathways and protein complexes for different microorganisms remain challenging. RESULTS: We describe a new computational method for the targeted discovery of functional modules of plant biomass-degrading protein families, based on their co-occurrence patterns across genomes and metagenome datasets, and the strength of association of these modules with the genomes of known degraders. From approximately 6.4 million family annotations for 2,884 microbial genomes, and 332 taxonomic bins from 18 metagenomes, we identified 5 functional modules that are distinctive for plant biomass degraders, which we term “plant biomass degradation modules” (PDMs). These modules incorporate protein families involved in the degradation of cellulose, hemicelluloses, and pectins, structural components of the cellulosome, and additional families with potential functions in plant biomass degradation. The PDMs were linked to 81 gene clusters in genomes of known lignocellulose degraders, including previously described clusters of lignocellulolytic genes. On average, 70% of the families of each PDM were found to map to gene clusters in known degraders, which served as an additional confirmation of their functional relationships. The presence of a PDM in a genome or taxonomic metagenome bin furthermore allowed us to accurately predict the ability of any particular organism to degrade plant biomass. For 15 draft genomes of a cow rumen metagenome, we used cross-referencing to confirmed cellulolytic enzymes to validate that the PDMs identified plant biomass degraders within a complex microbial community. CONCLUSIONS: Functional modules of protein families that are involved in different aspects of plant cell wall degradation can be inferred from co-occurrence patterns across (meta-)genomes with a probabilistic topic model. PDMs represent a new resource of protein families and candidate genes implicated in microbial plant biomass degradation. They can also be used to predict the plant biomass degradation ability for a genome or taxonomic bin. The method is also suitable for characterizing other microbial phenotypes.</description><identifier>ISSN: 1754-6834</identifier><identifier>EISSN: 1754-6834</identifier><identifier>DOI: 10.1186/s13068-014-0124-8</identifier><identifier>PMID: 25342967</identifier><language>eng</language><publisher>England: Springer-Verlag</publisher><subject>Bacteriology ; biofuels ; biomass ; Carbohydrates ; cell walls ; Cellulase ; Cellulose ; cellulosome ; cows ; data collection ; Enzymes ; fossil fuels ; Genes ; Genetic aspects ; Genomes ; Genotype & phenotype ; Glucose ; hemicellulose ; Lignin ; Lignocellulose ; metagenomics ; Methods ; microbial communities ; microorganisms ; multigene family ; Pectin ; pectins ; phenotype ; Proteins ; Rankings ; rumen</subject><ispartof>Biotechnology for biofuels, 2014-09, Vol.7 (1), p.124-124, Article 124</ispartof><rights>COPYRIGHT 2014 BioMed Central Ltd.</rights><rights>2014 Konietzny et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.</rights><rights>Konietzny et al.; licensee BioMed Central Ltd. 2014</rights><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-b651t-c1f196d22f30476019e1f094f343e084a7c562c7ff9352d5b35773a18ec9991a3</citedby><cites>FETCH-LOGICAL-b651t-c1f196d22f30476019e1f094f343e084a7c562c7ff9352d5b35773a18ec9991a3</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/PMC4189754/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1609282697?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,25731,27901,27902,36989,36990,44566,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25342967$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Konietzny, Sebastian GA</creatorcontrib><creatorcontrib>Pope, Phillip B</creatorcontrib><creatorcontrib>Weimann, Aaron</creatorcontrib><creatorcontrib>McHardy, Alice C</creatorcontrib><title>Inference of phenotype-defining functional modules of protein families for microbial plant biomass degraders</title><title>Biotechnology for biofuels</title><addtitle>Biotechnol Biofuels</addtitle><description>BACKGROUND: Efficient industrial processes for converting plant lignocellulosic materials into biofuels are a key to global efforts to come up with alternative energy sources to fossil fuels. Novel cellulolytic enzymes have been discovered in microbial genomes and metagenomes of microbial communities. However, the identification of relevant genes without known homologs, and the elucidation of the lignocellulolytic pathways and protein complexes for different microorganisms remain challenging. RESULTS: We describe a new computational method for the targeted discovery of functional modules of plant biomass-degrading protein families, based on their co-occurrence patterns across genomes and metagenome datasets, and the strength of association of these modules with the genomes of known degraders. From approximately 6.4 million family annotations for 2,884 microbial genomes, and 332 taxonomic bins from 18 metagenomes, we identified 5 functional modules that are distinctive for plant biomass degraders, which we term “plant biomass degradation modules” (PDMs). These modules incorporate protein families involved in the degradation of cellulose, hemicelluloses, and pectins, structural components of the cellulosome, and additional families with potential functions in plant biomass degradation. The PDMs were linked to 81 gene clusters in genomes of known lignocellulose degraders, including previously described clusters of lignocellulolytic genes. On average, 70% of the families of each PDM were found to map to gene clusters in known degraders, which served as an additional confirmation of their functional relationships. The presence of a PDM in a genome or taxonomic metagenome bin furthermore allowed us to accurately predict the ability of any particular organism to degrade plant biomass. For 15 draft genomes of a cow rumen metagenome, we used cross-referencing to confirmed cellulolytic enzymes to validate that the PDMs identified plant biomass degraders within a complex microbial community. CONCLUSIONS: Functional modules of protein families that are involved in different aspects of plant cell wall degradation can be inferred from co-occurrence patterns across (meta-)genomes with a probabilistic topic model. PDMs represent a new resource of protein families and candidate genes implicated in microbial plant biomass degradation. They can also be used to predict the plant biomass degradation ability for a genome or taxonomic bin. The method is also suitable for characterizing other microbial phenotypes.</description><subject>Bacteriology</subject><subject>biofuels</subject><subject>biomass</subject><subject>Carbohydrates</subject><subject>cell walls</subject><subject>Cellulase</subject><subject>Cellulose</subject><subject>cellulosome</subject><subject>cows</subject><subject>data collection</subject><subject>Enzymes</subject><subject>fossil fuels</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Genotype & phenotype</subject><subject>Glucose</subject><subject>hemicellulose</subject><subject>Lignin</subject><subject>Lignocellulose</subject><subject>metagenomics</subject><subject>Methods</subject><subject>microbial communities</subject><subject>microorganisms</subject><subject>multigene family</subject><subject>Pectin</subject><subject>pectins</subject><subject>phenotype</subject><subject>Proteins</subject><subject>Rankings</subject><subject>rumen</subject><issn>1754-6834</issn><issn>1754-6834</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><recordid>eNqNkl1r1jAYhosobk5_gCda8EQPOvPVfJwMxvwaDATnjkPe9EmX0SavSSvu35uuc-yVHYymNCRXLprnfqrqNUaHGEv-MWOKuGwQZuUlrJFPqn0sWtZwSdnTe_O96kXOVwhxLJB4Xu2RljKiuNivhtPgIEGwUEdXby8hxOl6C00Hzgcf-trNwU4-BjPUY-zmAfINmOIEPtTOjH7wZc3FVI_eprjxhdwOJkz1xsfR5Fx30CfTQcovq2fODBle3X4Pqosvn3-efGvOvn89PTk-aza8xVNjscOKd4Q4ipjgCCvADinmKKOAJDPCtpxY4ZyiLenaDW2FoAZLsEopbOhBdbR6t_NmhM5CmJIZ9Db50aRrHY3XuzvBX-o-_tYMS1VqVgSfVsFyhYcFuzs2jnpNQ5c09JKGlkXz_vY_Uvw1Q5706LOFoVQH4pw15pxyJATjj0AxZ5IwJR6DlsGQXKzv_kOv4pxKlguFFJGE3wgPV6o3A2gfXCx3suXpoEQaQ2mFsn7cFiUlrVi0H3YOFGaCP1Nv5pz16fmPXRavbOmNnBO4uypipJcufrBub-7nd3fiX9sW4O0KOBO16ZPP-uKcFANCxVgqSv8CxCv2KQ</recordid><startdate>20140909</startdate><enddate>20140909</enddate><creator>Konietzny, 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of phenotype-defining functional modules of protein families for microbial plant biomass degraders</title><author>Konietzny, Sebastian GA ; Pope, Phillip B ; Weimann, Aaron ; McHardy, Alice C</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-b651t-c1f196d22f30476019e1f094f343e084a7c562c7ff9352d5b35773a18ec9991a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Bacteriology</topic><topic>biofuels</topic><topic>biomass</topic><topic>Carbohydrates</topic><topic>cell walls</topic><topic>Cellulase</topic><topic>Cellulose</topic><topic>cellulosome</topic><topic>cows</topic><topic>data collection</topic><topic>Enzymes</topic><topic>fossil fuels</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Genomes</topic><topic>Genotype & phenotype</topic><topic>Glucose</topic><topic>hemicellulose</topic><topic>Lignin</topic><topic>Lignocellulose</topic><topic>metagenomics</topic><topic>Methods</topic><topic>microbial communities</topic><topic>microorganisms</topic><topic>multigene family</topic><topic>Pectin</topic><topic>pectins</topic><topic>phenotype</topic><topic>Proteins</topic><topic>Rankings</topic><topic>rumen</topic><toplevel>online_resources</toplevel><creatorcontrib>Konietzny, Sebastian GA</creatorcontrib><creatorcontrib>Pope, Phillip B</creatorcontrib><creatorcontrib>Weimann, Aaron</creatorcontrib><creatorcontrib>McHardy, Alice C</creatorcontrib><collection>AGRIS</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Science In Context</collection><collection>ProQuest Central (Corporate)</collection><collection>Biotechnology Research Abstracts</collection><collection>Electronics & Communications Abstracts</collection><collection>Environment 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biofuels</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Konietzny, Sebastian GA</au><au>Pope, Phillip B</au><au>Weimann, Aaron</au><au>McHardy, Alice C</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Inference of phenotype-defining functional modules of protein families for microbial plant biomass degraders</atitle><jtitle>Biotechnology for biofuels</jtitle><addtitle>Biotechnol Biofuels</addtitle><date>2014-09-09</date><risdate>2014</risdate><volume>7</volume><issue>1</issue><spage>124</spage><epage>124</epage><pages>124-124</pages><artnum>124</artnum><issn>1754-6834</issn><eissn>1754-6834</eissn><abstract>BACKGROUND: Efficient industrial processes for converting plant lignocellulosic materials into biofuels are a key to global efforts to come up with alternative energy sources to fossil fuels. Novel cellulolytic enzymes have been discovered in microbial genomes and metagenomes of microbial communities. However, the identification of relevant genes without known homologs, and the elucidation of the lignocellulolytic pathways and protein complexes for different microorganisms remain challenging. RESULTS: We describe a new computational method for the targeted discovery of functional modules of plant biomass-degrading protein families, based on their co-occurrence patterns across genomes and metagenome datasets, and the strength of association of these modules with the genomes of known degraders. From approximately 6.4 million family annotations for 2,884 microbial genomes, and 332 taxonomic bins from 18 metagenomes, we identified 5 functional modules that are distinctive for plant biomass degraders, which we term “plant biomass degradation modules” (PDMs). These modules incorporate protein families involved in the degradation of cellulose, hemicelluloses, and pectins, structural components of the cellulosome, and additional families with potential functions in plant biomass degradation. The PDMs were linked to 81 gene clusters in genomes of known lignocellulose degraders, including previously described clusters of lignocellulolytic genes. On average, 70% of the families of each PDM were found to map to gene clusters in known degraders, which served as an additional confirmation of their functional relationships. The presence of a PDM in a genome or taxonomic metagenome bin furthermore allowed us to accurately predict the ability of any particular organism to degrade plant biomass. For 15 draft genomes of a cow rumen metagenome, we used cross-referencing to confirmed cellulolytic enzymes to validate that the PDMs identified plant biomass degraders within a complex microbial community. CONCLUSIONS: Functional modules of protein families that are involved in different aspects of plant cell wall degradation can be inferred from co-occurrence patterns across (meta-)genomes with a probabilistic topic model. PDMs represent a new resource of protein families and candidate genes implicated in microbial plant biomass degradation. They can also be used to predict the plant biomass degradation ability for a genome or taxonomic bin. The method is also suitable for characterizing other microbial phenotypes.</abstract><cop>England</cop><pub>Springer-Verlag</pub><pmid>25342967</pmid><doi>10.1186/s13068-014-0124-8</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Bacteriology biofuels biomass Carbohydrates cell walls Cellulase Cellulose cellulosome cows data collection Enzymes fossil fuels Genes Genetic aspects Genomes Genotype & phenotype Glucose hemicellulose Lignin Lignocellulose metagenomics Methods microbial communities microorganisms multigene family Pectin pectins phenotype Proteins Rankings rumen |
title | Inference of phenotype-defining functional modules of protein families for microbial plant biomass degraders |
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