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Genomic and functional analyses of fungal and bacterial consortia that enable lignocellulose breakdown in goat gut microbiomes

The herbivore digestive tract is home to a complex community of anaerobic microbes that work together to break down lignocellulose. These microbiota are an untapped resource of strains, pathways and enzymes that could be applied to convert plant waste into sugar substrates for green biotechnology. W...

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Autores principales: Peng, Xuefeng, Wilken, St. Elmo, Lankiewicz, Thomas S., Gilmore, Sean P., Brown, Jennifer L., Henske, John K., Swift, Candice L., Salamov, Asaf, Barry, Kerrie, Grigoriev, Igor V., Theodorou, Michael K., Valentine, David L., O’Malley, Michelle A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8007473/
https://www.ncbi.nlm.nih.gov/pubmed/33526884
http://dx.doi.org/10.1038/s41564-020-00861-0
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author Peng, Xuefeng
Wilken, St. Elmo
Lankiewicz, Thomas S.
Gilmore, Sean P.
Brown, Jennifer L.
Henske, John K.
Swift, Candice L.
Salamov, Asaf
Barry, Kerrie
Grigoriev, Igor V.
Theodorou, Michael K.
Valentine, David L.
O’Malley, Michelle A.
author_facet Peng, Xuefeng
Wilken, St. Elmo
Lankiewicz, Thomas S.
Gilmore, Sean P.
Brown, Jennifer L.
Henske, John K.
Swift, Candice L.
Salamov, Asaf
Barry, Kerrie
Grigoriev, Igor V.
Theodorou, Michael K.
Valentine, David L.
O’Malley, Michelle A.
author_sort Peng, Xuefeng
collection PubMed
description The herbivore digestive tract is home to a complex community of anaerobic microbes that work together to break down lignocellulose. These microbiota are an untapped resource of strains, pathways and enzymes that could be applied to convert plant waste into sugar substrates for green biotechnology. We carried out more than 400 parallel enrichment experiments from goat faeces to determine how substrate and antibiotic selection influence membership, activity, stability and chemical productivity of herbivore gut communities. We assembled 719 high-quality metagenome-assembled genomes (MAGs) that are unique at the species level. More than 90% of these MAGs are from previously unidentified herbivore gut microorganisms. Microbial consortia dominated by anaerobic fungi outperformed bacterially dominated consortia in terms of both methane production and extent of cellulose degradation, which indicates that fungi have an important role in methane release. Metabolic pathway reconstructions from MAGs of 737 bacteria, archaea and fungi suggest that cross-domain partnerships between fungi and methanogens enabled production of acetate, formate and methane, whereas bacterially dominated consortia mainly produced short-chain fatty acids, including propionate and butyrate. Analyses of carbohydrate-active enzyme domains present in each anaerobic consortium suggest that anaerobic bacteria and fungi employ mostly complementary hydrolytic strategies. The division of labour among herbivore anaerobes to degrade plant biomass could be harnessed for industrial bioprocessing.
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spelling pubmed-80074732021-04-12 Genomic and functional analyses of fungal and bacterial consortia that enable lignocellulose breakdown in goat gut microbiomes Peng, Xuefeng Wilken, St. Elmo Lankiewicz, Thomas S. Gilmore, Sean P. Brown, Jennifer L. Henske, John K. Swift, Candice L. Salamov, Asaf Barry, Kerrie Grigoriev, Igor V. Theodorou, Michael K. Valentine, David L. O’Malley, Michelle A. Nat Microbiol Article The herbivore digestive tract is home to a complex community of anaerobic microbes that work together to break down lignocellulose. These microbiota are an untapped resource of strains, pathways and enzymes that could be applied to convert plant waste into sugar substrates for green biotechnology. We carried out more than 400 parallel enrichment experiments from goat faeces to determine how substrate and antibiotic selection influence membership, activity, stability and chemical productivity of herbivore gut communities. We assembled 719 high-quality metagenome-assembled genomes (MAGs) that are unique at the species level. More than 90% of these MAGs are from previously unidentified herbivore gut microorganisms. Microbial consortia dominated by anaerobic fungi outperformed bacterially dominated consortia in terms of both methane production and extent of cellulose degradation, which indicates that fungi have an important role in methane release. Metabolic pathway reconstructions from MAGs of 737 bacteria, archaea and fungi suggest that cross-domain partnerships between fungi and methanogens enabled production of acetate, formate and methane, whereas bacterially dominated consortia mainly produced short-chain fatty acids, including propionate and butyrate. Analyses of carbohydrate-active enzyme domains present in each anaerobic consortium suggest that anaerobic bacteria and fungi employ mostly complementary hydrolytic strategies. The division of labour among herbivore anaerobes to degrade plant biomass could be harnessed for industrial bioprocessing. Nature Publishing Group UK 2021-02-01 2021 /pmc/articles/PMC8007473/ /pubmed/33526884 http://dx.doi.org/10.1038/s41564-020-00861-0 Text en © The Author(s) 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Peng, Xuefeng
Wilken, St. Elmo
Lankiewicz, Thomas S.
Gilmore, Sean P.
Brown, Jennifer L.
Henske, John K.
Swift, Candice L.
Salamov, Asaf
Barry, Kerrie
Grigoriev, Igor V.
Theodorou, Michael K.
Valentine, David L.
O’Malley, Michelle A.
Genomic and functional analyses of fungal and bacterial consortia that enable lignocellulose breakdown in goat gut microbiomes
title Genomic and functional analyses of fungal and bacterial consortia that enable lignocellulose breakdown in goat gut microbiomes
title_full Genomic and functional analyses of fungal and bacterial consortia that enable lignocellulose breakdown in goat gut microbiomes
title_fullStr Genomic and functional analyses of fungal and bacterial consortia that enable lignocellulose breakdown in goat gut microbiomes
title_full_unstemmed Genomic and functional analyses of fungal and bacterial consortia that enable lignocellulose breakdown in goat gut microbiomes
title_short Genomic and functional analyses of fungal and bacterial consortia that enable lignocellulose breakdown in goat gut microbiomes
title_sort genomic and functional analyses of fungal and bacterial consortia that enable lignocellulose breakdown in goat gut microbiomes
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8007473/
https://www.ncbi.nlm.nih.gov/pubmed/33526884
http://dx.doi.org/10.1038/s41564-020-00861-0
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