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

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369 Scopus citations

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

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Keywords

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

ASJC Scopus subject areas

  • General

Cite this

Mahowald, M. A., Rey, F. E., Seedorf, H., Turnbaugh, P. J., Fulton, R. S., Wollam, A., Shah, N., Wang, C., Magrini, V., Wilson, R. K., Cantarel, B. L., Coutinho, P. M., Henrissat, B., Crock, L. W., Russell, A., Verberkmoes, N. C., Hettich, R. L., & Gordon, J. I. (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, 106(14), 5859-5864. https://doi.org/10.1073/pnas.0901529106