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

Michael A. Mahowald, Federico E. Rey, Henning Seedorf, Peter J. Turnbaugh, Robert S. Fulton, Aye Wollam, Neha Shah, Chunyan Wang, Vincent Magrini, Richard K. Wilson, Brandi L. Cantarel, Pedro M. Coutinho, Bernard Henrissat, Lara W. Crock, Alison Russell, Nathan C. Verberkmoes, Robert L. Hettich, Jeffrey I. Gordon

Research output: Contribution to journalArticle

366 Citations (Scopus)

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, oneofthe 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.

Original languageEnglish (US)
Pages (from-to)5859-5864
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume106
Issue number14
DOIs
StatePublished - Apr 7 2009

Fingerprint

Polysaccharides
Bacteroidetes
Genome
Microbial Interactions
Eubacterium
Amino Sugars
Amino Acid Transport Systems
Clostridium
Butyrates
Glycoside Hydrolases
Glycolysis
Enzymes
NAD
Proteomics
Ecosystem
Acetates
Epithelium
Gastrointestinal Microbiome
Food
Bacteroides thetaiotaomicron

Keywords

  • Carbohydrate metabolism gnotobiotic mice
  • Gut microbiome
  • Human gut Firmicutes and Bacteroidetes
  • Nutrient sharing

ASJC Scopus subject areas

  • General

Cite this

Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. / Mahowald, Michael A.; Rey, Federico 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.; Russell, Alison; Verberkmoes, Nathan C.; Hettich, Robert L.; Gordon, Jeffrey I.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 106, No. 14, 07.04.2009, p. 5859-5864.

Research output: Contribution to journalArticle

Mahowald, MA, Rey, FE, Seedorf, H, Turnbaugh, PJ, Fulton, RS, Wollam, A, Shah, N, Wang, C, Magrini, V, Wilson, RK, Cantarel, BL, Coutinho, PM, Henrissat, B, Crock, LW, Russell, A, Verberkmoes, NC, Hettich, RL & Gordon, JI 2009, 'Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla', Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 14, pp. 5859-5864. https://doi.org/10.1073/pnas.0901529106
Mahowald, Michael A. ; Rey, Federico 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. ; Russell, Alison ; Verberkmoes, Nathan C. ; Hettich, Robert L. ; Gordon, Jeffrey I. / Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. In: Proceedings of the National Academy of Sciences of the United States of America. 2009 ; Vol. 106, No. 14. pp. 5859-5864.
@article{0a059fca327b4d14baab65357c3a9fd0,
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, oneofthe 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.",
keywords = "Carbohydrate metabolism gnotobiotic mice, Gut microbiome, Human gut Firmicutes and Bacteroidetes, Nutrient sharing",
author = "Mahowald, {Michael A.} and Rey, {Federico E.} and Henning Seedorf and Turnbaugh, {Peter J.} and Fulton, {Robert S.} and Aye Wollam and Neha Shah and Chunyan Wang and Vincent Magrini and Wilson, {Richard K.} and Cantarel, {Brandi L.} and Coutinho, {Pedro M.} and Bernard Henrissat and Crock, {Lara W.} and Alison Russell and Verberkmoes, {Nathan C.} and Hettich, {Robert L.} and Gordon, {Jeffrey I.}",
year = "2009",
month = "4",
day = "7",
doi = "10.1073/pnas.0901529106",
language = "English (US)",
volume = "106",
pages = "5859--5864",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "14",

}

TY - JOUR

T1 - Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla

AU - Mahowald, Michael A.

AU - Rey, Federico E.

AU - Seedorf, Henning

AU - Turnbaugh, Peter J.

AU - Fulton, Robert S.

AU - Wollam, Aye

AU - Shah, Neha

AU - Wang, Chunyan

AU - Magrini, Vincent

AU - Wilson, Richard K.

AU - Cantarel, Brandi L.

AU - Coutinho, Pedro M.

AU - Henrissat, Bernard

AU - Crock, Lara W.

AU - Russell, Alison

AU - Verberkmoes, Nathan C.

AU - Hettich, Robert L.

AU - Gordon, Jeffrey I.

PY - 2009/4/7

Y1 - 2009/4/7

N2 - 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, oneofthe 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.

AB - 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, oneofthe 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.

KW - Carbohydrate metabolism gnotobiotic mice

KW - Gut microbiome

KW - Human gut Firmicutes and Bacteroidetes

KW - Nutrient sharing

UR - http://www.scopus.com/inward/record.url?scp=65249149643&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=65249149643&partnerID=8YFLogxK

U2 - 10.1073/pnas.0901529106

DO - 10.1073/pnas.0901529106

M3 - Article

C2 - 19321416

AN - SCOPUS:65249149643

VL - 106

SP - 5859

EP - 5864

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 14

ER -