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Metagenomic and metaproteomic analyses of a corn stover-adapted microbial consortium EMSD5 reveal its taxonomic and enzymatic basis for degrading lignocellulose

BACKGROUND: Microbial consortia represent promising candidates for aiding in the development of plant biomass conversion strategies for biofuel production. However, the interaction between different community members and the dynamics of enzyme complements during the lignocellulose deconstruction pro...

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Autores principales: Zhu, Ning, Yang, Jinshui, Ji, Lei, Liu, Jiawen, Yang, Yi, Yuan, Hongli
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5103373/
https://www.ncbi.nlm.nih.gov/pubmed/27833656
http://dx.doi.org/10.1186/s13068-016-0658-z
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author Zhu, Ning
Yang, Jinshui
Ji, Lei
Liu, Jiawen
Yang, Yi
Yuan, Hongli
author_facet Zhu, Ning
Yang, Jinshui
Ji, Lei
Liu, Jiawen
Yang, Yi
Yuan, Hongli
author_sort Zhu, Ning
collection PubMed
description BACKGROUND: Microbial consortia represent promising candidates for aiding in the development of plant biomass conversion strategies for biofuel production. However, the interaction between different community members and the dynamics of enzyme complements during the lignocellulose deconstruction process remain poorly understood. We present here a comprehensive study on the community structure and enzyme systems of a lignocellulolytic microbial consortium EMSD5 during growth on corn stover, using metagenome sequencing in combination with quantitative metaproteomics. RESULTS: The taxonomic affiliation of the metagenomic data showed that EMSD5 was primarily composed of members from the phyla Proteobacteria, Firmicutes and Bacteroidetes. The carbohydrate-active enzyme (CAZyme) annotation revealed that representatives of Firmicutes encoded a broad array of enzymes responsible for hemicellulose and cellulose deconstruction. Extracellular metaproteome analysis further pinpointed the specific role and synergistic interaction of Firmicutes populations in plant polysaccharide breakdown. In particular, a wide range of xylan degradation-related enzymes, including xylanases, β-xylosidases, α-l-arabinofuranosidases, α-glucuronidases and acetyl xylan esterases, were secreted by diverse members from Firmicutes during growth on corn stover. Using label-free quantitative proteomics, we identified the differential secretion pattern of a core subset of enzymes, including xylanases and cellulases with multiple carbohydrate-binding modules (CBMs). In addition, analysis of the coordinate expression patterns indicated that transport proteins and hypothetical proteins may play a role in bacteria processing lignocellulose. Moreover, enzyme preparation from EMSD5 demonstrated synergistic activities in the hydrolysis of pretreated corn stover by commercial cellulases from Trichoderma reesei. CONCLUSIONS: These results demonstrate that the corn stover-adapted microbial consortium EMSD5 harbors a variety of lignocellulolytic anaerobic bacteria and degradative enzymes, especially those implicated in hemicellulose decomposition. The data in this study highlight the pivotal role and cooperative relationship of Firmicutes members in the biodegradation of plant lignocellulose by EMSD5. The differential expression patterns of enzymes reveal the strategy of sequential lignocellulose deconstruction by EMSD5. Our findings provide insights into the mechanism by which consortium members orchestrate their array of enzymes to degrade complex lignocellulosic biomass. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13068-016-0658-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-51033732016-11-10 Metagenomic and metaproteomic analyses of a corn stover-adapted microbial consortium EMSD5 reveal its taxonomic and enzymatic basis for degrading lignocellulose Zhu, Ning Yang, Jinshui Ji, Lei Liu, Jiawen Yang, Yi Yuan, Hongli Biotechnol Biofuels Research BACKGROUND: Microbial consortia represent promising candidates for aiding in the development of plant biomass conversion strategies for biofuel production. However, the interaction between different community members and the dynamics of enzyme complements during the lignocellulose deconstruction process remain poorly understood. We present here a comprehensive study on the community structure and enzyme systems of a lignocellulolytic microbial consortium EMSD5 during growth on corn stover, using metagenome sequencing in combination with quantitative metaproteomics. RESULTS: The taxonomic affiliation of the metagenomic data showed that EMSD5 was primarily composed of members from the phyla Proteobacteria, Firmicutes and Bacteroidetes. The carbohydrate-active enzyme (CAZyme) annotation revealed that representatives of Firmicutes encoded a broad array of enzymes responsible for hemicellulose and cellulose deconstruction. Extracellular metaproteome analysis further pinpointed the specific role and synergistic interaction of Firmicutes populations in plant polysaccharide breakdown. In particular, a wide range of xylan degradation-related enzymes, including xylanases, β-xylosidases, α-l-arabinofuranosidases, α-glucuronidases and acetyl xylan esterases, were secreted by diverse members from Firmicutes during growth on corn stover. Using label-free quantitative proteomics, we identified the differential secretion pattern of a core subset of enzymes, including xylanases and cellulases with multiple carbohydrate-binding modules (CBMs). In addition, analysis of the coordinate expression patterns indicated that transport proteins and hypothetical proteins may play a role in bacteria processing lignocellulose. Moreover, enzyme preparation from EMSD5 demonstrated synergistic activities in the hydrolysis of pretreated corn stover by commercial cellulases from Trichoderma reesei. CONCLUSIONS: These results demonstrate that the corn stover-adapted microbial consortium EMSD5 harbors a variety of lignocellulolytic anaerobic bacteria and degradative enzymes, especially those implicated in hemicellulose decomposition. The data in this study highlight the pivotal role and cooperative relationship of Firmicutes members in the biodegradation of plant lignocellulose by EMSD5. The differential expression patterns of enzymes reveal the strategy of sequential lignocellulose deconstruction by EMSD5. Our findings provide insights into the mechanism by which consortium members orchestrate their array of enzymes to degrade complex lignocellulosic biomass. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13068-016-0658-z) contains supplementary material, which is available to authorized users. BioMed Central 2016-11-09 /pmc/articles/PMC5103373/ /pubmed/27833656 http://dx.doi.org/10.1186/s13068-016-0658-z Text en © The Author(s) 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.
spellingShingle Research
Zhu, Ning
Yang, Jinshui
Ji, Lei
Liu, Jiawen
Yang, Yi
Yuan, Hongli
Metagenomic and metaproteomic analyses of a corn stover-adapted microbial consortium EMSD5 reveal its taxonomic and enzymatic basis for degrading lignocellulose
title Metagenomic and metaproteomic analyses of a corn stover-adapted microbial consortium EMSD5 reveal its taxonomic and enzymatic basis for degrading lignocellulose
title_full Metagenomic and metaproteomic analyses of a corn stover-adapted microbial consortium EMSD5 reveal its taxonomic and enzymatic basis for degrading lignocellulose
title_fullStr Metagenomic and metaproteomic analyses of a corn stover-adapted microbial consortium EMSD5 reveal its taxonomic and enzymatic basis for degrading lignocellulose
title_full_unstemmed Metagenomic and metaproteomic analyses of a corn stover-adapted microbial consortium EMSD5 reveal its taxonomic and enzymatic basis for degrading lignocellulose
title_short Metagenomic and metaproteomic analyses of a corn stover-adapted microbial consortium EMSD5 reveal its taxonomic and enzymatic basis for degrading lignocellulose
title_sort metagenomic and metaproteomic analyses of a corn stover-adapted microbial consortium emsd5 reveal its taxonomic and enzymatic basis for degrading lignocellulose
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5103373/
https://www.ncbi.nlm.nih.gov/pubmed/27833656
http://dx.doi.org/10.1186/s13068-016-0658-z
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