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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Published in:The ISME Journal
Main Authors: 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
Format: Text
Language:English
Published: Nature Publishing Group 2017
Subjects:
Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5322302/
http://www.ncbi.nlm.nih.gov/pubmed/27959345
https://doi.org/10.1038/ismej.2016.150
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spelling ftpubmed:oai:pubmedcentral.nih.gov:5322302 2023-05-15T15:07:30+02:00 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 2017-03 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5322302/ http://www.ncbi.nlm.nih.gov/pubmed/27959345 https://doi.org/10.1038/ismej.2016.150 en eng Nature Publishing Group http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5322302/ http://www.ncbi.nlm.nih.gov/pubmed/27959345 http://dx.doi.org/10.1038/ismej.2016.150 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/ CC-BY-NC-SA Original Article Text 2017 ftpubmed https://doi.org/10.1038/ismej.2016.150 2017-03-05T01:27:54Z 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. Text Arctic Moose PubMed Central (PMC) Arctic The ISME Journal 11 3 691 703
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Original Article
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
topic_facet Original Article
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.
format Text
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
title 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_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_sort new roles in hemicellulosic sugar fermentation for the uncultivated bacteroidetes family bs11
publisher Nature Publishing Group
publishDate 2017
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5322302/
http://www.ncbi.nlm.nih.gov/pubmed/27959345
https://doi.org/10.1038/ismej.2016.150
geographic Arctic
geographic_facet Arctic
genre Arctic
Moose
genre_facet Arctic
Moose
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5322302/
http://www.ncbi.nlm.nih.gov/pubmed/27959345
http://dx.doi.org/10.1038/ismej.2016.150
op_rights 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/
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op_doi https://doi.org/10.1038/ismej.2016.150
container_title The ISME Journal
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