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New roles in hemicellulosic sugar fermentation for the uncultivated Bacteroidetes family BS11

Ruminants have co-evolved with their gastrointestinal microbial communities that digest plant materials to provide energy for the host. Some arctic and boreal ruminants have already shown to be vulnerable to dietary shifts caused by changing climate, yet we know little about the metabolic capacity o...

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Autores principales: Solden, Lindsey M, Hoyt, David W, Collins, William B, Plank, Johanna E, Daly, Rebecca A, Hildebrand, Erik, Beavers, Timothy J, Wolfe, Richard, Nicora, Carrie D, Purvine, Sam O, Carstensen, Michelle, Lipton, Mary S, Spalinger, Donald E, Firkins, Jeffrey L, Wolfe, Barbara A, Wrighton, Kelly C
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5322302/
https://www.ncbi.nlm.nih.gov/pubmed/27959345
http://dx.doi.org/10.1038/ismej.2016.150
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author Solden, Lindsey M
Hoyt, David W
Collins, William B
Plank, Johanna E
Daly, Rebecca A
Hildebrand, Erik
Beavers, Timothy J
Wolfe, Richard
Nicora, Carrie D
Purvine, Sam O
Carstensen, Michelle
Lipton, Mary S
Spalinger, Donald E
Firkins, Jeffrey L
Wolfe, Barbara A
Wrighton, Kelly C
author_facet Solden, Lindsey M
Hoyt, David W
Collins, William B
Plank, Johanna E
Daly, Rebecca A
Hildebrand, Erik
Beavers, Timothy J
Wolfe, Richard
Nicora, Carrie D
Purvine, Sam O
Carstensen, Michelle
Lipton, Mary S
Spalinger, Donald E
Firkins, Jeffrey L
Wolfe, Barbara A
Wrighton, Kelly C
author_sort Solden, Lindsey M
collection PubMed
description Ruminants have co-evolved with their gastrointestinal microbial communities that digest plant materials to provide energy for the host. Some arctic and boreal ruminants have already shown to be vulnerable to dietary shifts caused by changing climate, yet we know little about the metabolic capacity of the ruminant microbiome in these animals. Here, we use meta-omics approaches to sample rumen fluid microbial communities from Alaskan moose foraging along a seasonal lignocellulose gradient. Winter diets with increased hemicellulose and lignin strongly enriched for BS11, a Bacteroidetes family lacking cultivated or genomically sampled representatives. We show that BS11 are cosmopolitan host-associated bacteria prevalent in gastrointestinal tracts of ruminants and other mammals. Metagenomic reconstruction yielded the first four BS11 genomes; phylogenetically resolving two genera within this previously taxonomically undefined family. Genome-enabled metabolic analyses uncovered multiple pathways for fermenting hemicellulose monomeric sugars to short-chain fatty acids (SCFA), metabolites vital for ruminant energy. Active hemicellulosic sugar fermentation and SCFA production was validated by shotgun proteomics and rumen metabolites, illuminating the role BS11 have in carbon transformations within the rumen. Our results also highlight the currently unknown metabolic potential residing in the rumen that may be vital for sustaining host energy in response to a changing vegetative environment.
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spelling pubmed-53223022017-03-01 New roles in hemicellulosic sugar fermentation for the uncultivated Bacteroidetes family BS11 Solden, Lindsey M Hoyt, David W Collins, William B Plank, Johanna E Daly, Rebecca A Hildebrand, Erik Beavers, Timothy J Wolfe, Richard Nicora, Carrie D Purvine, Sam O Carstensen, Michelle Lipton, Mary S Spalinger, Donald E Firkins, Jeffrey L Wolfe, Barbara A Wrighton, Kelly C ISME J Original Article Ruminants have co-evolved with their gastrointestinal microbial communities that digest plant materials to provide energy for the host. Some arctic and boreal ruminants have already shown to be vulnerable to dietary shifts caused by changing climate, yet we know little about the metabolic capacity of the ruminant microbiome in these animals. Here, we use meta-omics approaches to sample rumen fluid microbial communities from Alaskan moose foraging along a seasonal lignocellulose gradient. Winter diets with increased hemicellulose and lignin strongly enriched for BS11, a Bacteroidetes family lacking cultivated or genomically sampled representatives. We show that BS11 are cosmopolitan host-associated bacteria prevalent in gastrointestinal tracts of ruminants and other mammals. Metagenomic reconstruction yielded the first four BS11 genomes; phylogenetically resolving two genera within this previously taxonomically undefined family. Genome-enabled metabolic analyses uncovered multiple pathways for fermenting hemicellulose monomeric sugars to short-chain fatty acids (SCFA), metabolites vital for ruminant energy. Active hemicellulosic sugar fermentation and SCFA production was validated by shotgun proteomics and rumen metabolites, illuminating the role BS11 have in carbon transformations within the rumen. Our results also highlight the currently unknown metabolic potential residing in the rumen that may be vital for sustaining host energy in response to a changing vegetative environment. Nature Publishing Group 2017-03 2016-12-13 /pmc/articles/PMC5322302/ /pubmed/27959345 http://dx.doi.org/10.1038/ismej.2016.150 Text en Copyright © 2017 International Society for Microbial Ecology http://creativecommons.org/licenses/by-nc-sa/4.0/ This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/4.0/
spellingShingle Original Article
Solden, Lindsey M
Hoyt, David W
Collins, William B
Plank, Johanna E
Daly, Rebecca A
Hildebrand, Erik
Beavers, Timothy J
Wolfe, Richard
Nicora, Carrie D
Purvine, Sam O
Carstensen, Michelle
Lipton, Mary S
Spalinger, Donald E
Firkins, Jeffrey L
Wolfe, Barbara A
Wrighton, Kelly C
New roles in hemicellulosic sugar fermentation for the uncultivated Bacteroidetes family BS11
title New roles in hemicellulosic sugar fermentation for the uncultivated Bacteroidetes family BS11
title_full New roles in hemicellulosic sugar fermentation for the uncultivated Bacteroidetes family BS11
title_fullStr New roles in hemicellulosic sugar fermentation for the uncultivated Bacteroidetes family BS11
title_full_unstemmed New roles in hemicellulosic sugar fermentation for the uncultivated Bacteroidetes family BS11
title_short New roles in hemicellulosic sugar fermentation for the uncultivated Bacteroidetes family BS11
title_sort new roles in hemicellulosic sugar fermentation for the uncultivated bacteroidetes family bs11
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5322302/
https://www.ncbi.nlm.nih.gov/pubmed/27959345
http://dx.doi.org/10.1038/ismej.2016.150
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