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A catalog of microbial genes from the bovine rumen unveils a specialized and diverse biomass-degrading environment

BACKGROUND: The rumen microbiota provides essential services to its host and, through its role in ruminant production, contributes to human nutrition and food security. A thorough knowledge of the genetic potential of rumen microbes will provide opportunities for improving the sustainability of rumi...

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Autores principales: Li, Junhua, Zhong, Huanzi, Ramayo-Caldas, Yuliaxis, Terrapon, Nicolas, Lombard, Vincent, Potocki-Veronese, Gabrielle, Estellé, Jordi, Popova, Milka, Yang, Ziyi, Zhang, Hui, Li, Fang, Tang, Shanmei, Yang, Fangming, Chen, Weineng, Chen, Bing, Li, Jiyang, Guo, Jing, Martin, Cécile, Maguin, Emmanuelle, Xu, Xun, Yang, Huanming, Wang, Jian, Madsen, Lise, Kristiansen, Karsten, Henrissat, Bernard, Ehrlich, Stanislav D, Morgavi, Diego P
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7260996/
https://www.ncbi.nlm.nih.gov/pubmed/32473013
http://dx.doi.org/10.1093/gigascience/giaa057
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author Li, Junhua
Zhong, Huanzi
Ramayo-Caldas, Yuliaxis
Terrapon, Nicolas
Lombard, Vincent
Potocki-Veronese, Gabrielle
Estellé, Jordi
Popova, Milka
Yang, Ziyi
Zhang, Hui
Li, Fang
Tang, Shanmei
Yang, Fangming
Chen, Weineng
Chen, Bing
Li, Jiyang
Guo, Jing
Martin, Cécile
Maguin, Emmanuelle
Xu, Xun
Yang, Huanming
Wang, Jian
Madsen, Lise
Kristiansen, Karsten
Henrissat, Bernard
Ehrlich, Stanislav D
Morgavi, Diego P
author_facet Li, Junhua
Zhong, Huanzi
Ramayo-Caldas, Yuliaxis
Terrapon, Nicolas
Lombard, Vincent
Potocki-Veronese, Gabrielle
Estellé, Jordi
Popova, Milka
Yang, Ziyi
Zhang, Hui
Li, Fang
Tang, Shanmei
Yang, Fangming
Chen, Weineng
Chen, Bing
Li, Jiyang
Guo, Jing
Martin, Cécile
Maguin, Emmanuelle
Xu, Xun
Yang, Huanming
Wang, Jian
Madsen, Lise
Kristiansen, Karsten
Henrissat, Bernard
Ehrlich, Stanislav D
Morgavi, Diego P
author_sort Li, Junhua
collection PubMed
description BACKGROUND: The rumen microbiota provides essential services to its host and, through its role in ruminant production, contributes to human nutrition and food security. A thorough knowledge of the genetic potential of rumen microbes will provide opportunities for improving the sustainability of ruminant production systems. The availability of gene reference catalogs from gut microbiomes has advanced the understanding of the role of the microbiota in health and disease in humans and other mammals. In this work, we established a catalog of reference prokaryote genes from the bovine rumen. RESULTS: Using deep metagenome sequencing we identified 13,825,880 non-redundant prokaryote genes from the bovine rumen. Compared to human, pig, and mouse gut metagenome catalogs, the rumen is larger and richer in functions and microbial species associated with the degradation of plant cell wall material and production of methane. Genes encoding enzymes catalyzing the breakdown of plant polysaccharides showed a particularly high richness that is otherwise impossible to infer from available genomes or shallow metagenomics sequencing. The catalog expands the dataset of carbohydrate-degrading enzymes described in the rumen. Using an independent dataset from a group of 77 cattle fed 4 common dietary regimes, we found that only <0.1% of genes were shared by all animals, which contrast with a large overlap for functions, i.e., 63% for KEGG functions. Different diets induced differences in the relative abundance rather than the presence or absence of genes, which explains the great adaptability of cattle to rapidly adjust to dietary changes. CONCLUSIONS: These data bring new insights into functions, carbohydrate-degrading enzymes, and microbes of the rumen to complement the available information on microbial genomes. The catalog is a significant biological resource enabling deeper understanding of phenotypes and biological processes and will be expanded as new data are made available.
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spelling pubmed-72609962020-06-03 A catalog of microbial genes from the bovine rumen unveils a specialized and diverse biomass-degrading environment Li, Junhua Zhong, Huanzi Ramayo-Caldas, Yuliaxis Terrapon, Nicolas Lombard, Vincent Potocki-Veronese, Gabrielle Estellé, Jordi Popova, Milka Yang, Ziyi Zhang, Hui Li, Fang Tang, Shanmei Yang, Fangming Chen, Weineng Chen, Bing Li, Jiyang Guo, Jing Martin, Cécile Maguin, Emmanuelle Xu, Xun Yang, Huanming Wang, Jian Madsen, Lise Kristiansen, Karsten Henrissat, Bernard Ehrlich, Stanislav D Morgavi, Diego P Gigascience Research BACKGROUND: The rumen microbiota provides essential services to its host and, through its role in ruminant production, contributes to human nutrition and food security. A thorough knowledge of the genetic potential of rumen microbes will provide opportunities for improving the sustainability of ruminant production systems. The availability of gene reference catalogs from gut microbiomes has advanced the understanding of the role of the microbiota in health and disease in humans and other mammals. In this work, we established a catalog of reference prokaryote genes from the bovine rumen. RESULTS: Using deep metagenome sequencing we identified 13,825,880 non-redundant prokaryote genes from the bovine rumen. Compared to human, pig, and mouse gut metagenome catalogs, the rumen is larger and richer in functions and microbial species associated with the degradation of plant cell wall material and production of methane. Genes encoding enzymes catalyzing the breakdown of plant polysaccharides showed a particularly high richness that is otherwise impossible to infer from available genomes or shallow metagenomics sequencing. The catalog expands the dataset of carbohydrate-degrading enzymes described in the rumen. Using an independent dataset from a group of 77 cattle fed 4 common dietary regimes, we found that only <0.1% of genes were shared by all animals, which contrast with a large overlap for functions, i.e., 63% for KEGG functions. Different diets induced differences in the relative abundance rather than the presence or absence of genes, which explains the great adaptability of cattle to rapidly adjust to dietary changes. CONCLUSIONS: These data bring new insights into functions, carbohydrate-degrading enzymes, and microbes of the rumen to complement the available information on microbial genomes. The catalog is a significant biological resource enabling deeper understanding of phenotypes and biological processes and will be expanded as new data are made available. Oxford University Press 2020-05-30 /pmc/articles/PMC7260996/ /pubmed/32473013 http://dx.doi.org/10.1093/gigascience/giaa057 Text en © The Author(s) 2020. Published by Oxford University Press. http://creativecommons.org/licenses/by/4.0/ 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 reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Li, Junhua
Zhong, Huanzi
Ramayo-Caldas, Yuliaxis
Terrapon, Nicolas
Lombard, Vincent
Potocki-Veronese, Gabrielle
Estellé, Jordi
Popova, Milka
Yang, Ziyi
Zhang, Hui
Li, Fang
Tang, Shanmei
Yang, Fangming
Chen, Weineng
Chen, Bing
Li, Jiyang
Guo, Jing
Martin, Cécile
Maguin, Emmanuelle
Xu, Xun
Yang, Huanming
Wang, Jian
Madsen, Lise
Kristiansen, Karsten
Henrissat, Bernard
Ehrlich, Stanislav D
Morgavi, Diego P
A catalog of microbial genes from the bovine rumen unveils a specialized and diverse biomass-degrading environment
title A catalog of microbial genes from the bovine rumen unveils a specialized and diverse biomass-degrading environment
title_full A catalog of microbial genes from the bovine rumen unveils a specialized and diverse biomass-degrading environment
title_fullStr A catalog of microbial genes from the bovine rumen unveils a specialized and diverse biomass-degrading environment
title_full_unstemmed A catalog of microbial genes from the bovine rumen unveils a specialized and diverse biomass-degrading environment
title_short A catalog of microbial genes from the bovine rumen unveils a specialized and diverse biomass-degrading environment
title_sort catalog of microbial genes from the bovine rumen unveils a specialized and diverse biomass-degrading environment
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7260996/
https://www.ncbi.nlm.nih.gov/pubmed/32473013
http://dx.doi.org/10.1093/gigascience/giaa057
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