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Title: Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla

Abstract

The adult human distal gut microbial community is typically dominated by 2 bacterial phyla (divisions), the Firmicutes and the Bacteroidetes. Little is known about the factors that govern the interactions between their members. Here, we examine the niches of representatives of both phyla in vivo. Finished genome sequences were generated from Eubacterium rectale and E. eligens, which belong to Clostridium Cluster XIVa, one of the most common gut Firmicute clades. Comparison of these and 25 other gut Firmicutes and Bacteroidetes indicated that the Firmicutes possess smaller genomes and a disproportionately smaller number of glycan-degrading enzymes. Germ-free mice were then colonized with E. rectale and/or a prominent human gut Bacteroidetes, Bacteroides thetaiotaomicron, followed by whole-genome transcriptional profiling, high-resolution proteomic analysis, and biochemical assays of microbial microbial and microbial host interactions. B. thetaiotaomicron adapts to E. rectale by up-regulating expression of a variety of polysaccharide utilization loci encoding numerous glycoside hydrolases, and by signaling the host to produce mucosal glycans that it, but not E. rectale, can access. E. rectale adapts to B. thetaiotaomicron by decreasing production of its glycan-degrading enzymes, increasing expression of selected amino acid and sugar transporters, and facilitating glycolysis by reducing levels of NADH, in part via generationmore » of butyrate from acetate, which in turn is used by the gut epithelium. This simplified model of the human gut microbiota illustrates niche specialization and functional redundancy within members of its major bacterial phyla, and the importance of host glycans as a nutrient foundation that ensures ecosystem stability.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [2];  [3];  [3];  [1];  [4];  [4];  [1]
  1. Washington University, St. Louis
  2. Centre National de la Recherche Scientifique, Unite Mixte de Recherche
  3. Universite d'Aix-Marseille I & II
  4. ORNL
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Laboratory Directed Research and Development (LDRD) Program
OSTI Identifier:
953189
DOE Contract Number:  
DE-AC05-00OR22725
Resource Type:
Journal Article
Journal Name:
Proceedings of the National Academy of Sciences
Additional Journal Information:
Journal Volume: 106; Journal Issue: 14; Journal ID: ISSN 0027-8424
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; ADULTS; AMINO ACIDS; CLOSTRIDIUM; ECOSYSTEMS; ENZYMES; EPITHELIUM; FUNCTIONALS; GLYCOLYSIS; GLYCOSIDES; HYDROLASES; IN VIVO; MICE; NUTRIENTS; POLYSACCHARIDES; REDUNDANCY; SACCHAROSE; STABILITY; human gut Firmicutes and Bacteroidetes; carbohydrate metabolism; gnotobiotic mice; gut microbiome; nutrient sharing

Citation Formats

Mahowald, Michael, Rey, Frederico E., Seedorf, Henning, Turnbaugh, Peter J., Fulton, Robert S., Wollam, Aye, Shah, Neha, Wang, Chunyan, Magrini, Vincent, Wilson, Richard K., Cantarel, Brandi L., Coutinho, Pedro M, Henrissat, Bernard, Crock, Lara W., Verberkmoes, Nathan C, Hettich, Robert, Erickson, Alison L, and Gordon, Jeffrey. Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. United States: N. p., 2009. Web. doi:10.1073/pnas.0901529106.
Mahowald, Michael, Rey, Frederico E., Seedorf, Henning, Turnbaugh, Peter J., Fulton, Robert S., Wollam, Aye, Shah, Neha, Wang, Chunyan, Magrini, Vincent, Wilson, Richard K., Cantarel, Brandi L., Coutinho, Pedro M, Henrissat, Bernard, Crock, Lara W., Verberkmoes, Nathan C, Hettich, Robert, Erickson, Alison L, & Gordon, Jeffrey. Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. United States. doi:10.1073/pnas.0901529106.
Mahowald, Michael, Rey, Frederico E., Seedorf, Henning, Turnbaugh, Peter J., Fulton, Robert S., Wollam, Aye, Shah, Neha, Wang, Chunyan, Magrini, Vincent, Wilson, Richard K., Cantarel, Brandi L., Coutinho, Pedro M, Henrissat, Bernard, Crock, Lara W., Verberkmoes, Nathan C, Hettich, Robert, Erickson, Alison L, and Gordon, Jeffrey. Thu . "Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla". United States. doi:10.1073/pnas.0901529106.
@article{osti_953189,
title = {Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla},
author = {Mahowald, Michael and Rey, Frederico E. and Seedorf, Henning and Turnbaugh, Peter J. and Fulton, Robert S. and Wollam, Aye and Shah, Neha and Wang, Chunyan and Magrini, Vincent and Wilson, Richard K. and Cantarel, Brandi L. and Coutinho, Pedro M and Henrissat, Bernard and Crock, Lara W. and Verberkmoes, Nathan C and Hettich, Robert and Erickson, Alison L and Gordon, Jeffrey},
abstractNote = {The adult human distal gut microbial community is typically dominated by 2 bacterial phyla (divisions), the Firmicutes and the Bacteroidetes. Little is known about the factors that govern the interactions between their members. Here, we examine the niches of representatives of both phyla in vivo. Finished genome sequences were generated from Eubacterium rectale and E. eligens, which belong to Clostridium Cluster XIVa, one of the most common gut Firmicute clades. Comparison of these and 25 other gut Firmicutes and Bacteroidetes indicated that the Firmicutes possess smaller genomes and a disproportionately smaller number of glycan-degrading enzymes. Germ-free mice were then colonized with E. rectale and/or a prominent human gut Bacteroidetes, Bacteroides thetaiotaomicron, followed by whole-genome transcriptional profiling, high-resolution proteomic analysis, and biochemical assays of microbial microbial and microbial host interactions. B. thetaiotaomicron adapts to E. rectale by up-regulating expression of a variety of polysaccharide utilization loci encoding numerous glycoside hydrolases, and by signaling the host to produce mucosal glycans that it, but not E. rectale, can access. E. rectale adapts to B. thetaiotaomicron by decreasing production of its glycan-degrading enzymes, increasing expression of selected amino acid and sugar transporters, and facilitating glycolysis by reducing levels of NADH, in part via generation of butyrate from acetate, which in turn is used by the gut epithelium. This simplified model of the human gut microbiota illustrates niche specialization and functional redundancy within members of its major bacterial phyla, and the importance of host glycans as a nutrient foundation that ensures ecosystem stability.},
doi = {10.1073/pnas.0901529106},
journal = {Proceedings of the National Academy of Sciences},
issn = {0027-8424},
number = 14,
volume = 106,
place = {United States},
year = {2009},
month = {1}
}