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

Abstract 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 c...

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Bibliographic Details
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: Article in Journal/Newspaper
Language:English
Published: Oxford University Press (OUP) 2016
Subjects:
Arctic
Moose
Online Access:http://dx.doi.org/10.1038/ismej.2016.150
http://www.nature.com/articles/ismej2016150.pdf
http://www.nature.com/articles/ismej2016150
https://academic.oup.com/ismej/article-pdf/11/3/691/56140812/41396_2017_article_bfismej2016150.pdf
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Summary:Abstract 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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