Cited by 380Gut microbiota and healthEvolution and Genetic DynamicsMicrobial Community Ecology and Physiology

Deciphering functional redundancy in the human microbiome

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Tian, Liang, Wang, Xu-Wen, Wu, Ang-Kun, Fan, Yuhang, Friedman, Jonathan, Dahlin, Amber, Waldor, Matthew K., Weinstock, George M. +2 more·2020·Nature Communications

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Abstract

Although the taxonomic composition of the human microbiome varies tremendously across individuals, its gene composition or functional capacity is highly conserved — implying an ecological property known as functional redundancy. Such functional redundancy has been hypothesized to underlie the stability and resilience of the human microbiome, but this hypothesis has never been quantitatively tested. The origin of functional redundancy is still elusive. Here, we investigate the basis for functional redundancy in the human microbiome by analyzing its genomic content network — a bipartite graph that links microbes to the genes in their genomes. We find that this network exhibits several topological features that favor high functional redundancy. Furthermore, we develop a simple genome evolution model to generate genomic content network, finding that moderate selection pressure and high horizontal gene transfer rate are necessary to generate genomic content networks with key topological features that favor high functional redundancy. Finally, we analyze data from two published studies of fecal microbiota transplantation (FMT), finding that high functional redundancy of the recipient’s pre-FMT microbiota raises barriers to donor microbiota engraftment. This work elucidates the potential ecological and evolutionary processes that create and maintain functional redundancy in the human microbiome and contribute to its resilience.

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  1. [4]Lawton, J. H. & Brown, V. K. In Biodiversity and Ecosystem Function (eds. Ernst-Detlef Schulze & Harold A. Mooney) 255–270 (Springer Berlin Heidelberg, 1994).
  2. [58]McCune, B., Grace, J. B. & Urban, D. L. Analysis of ecological communities. Vol. 28 (MjM software design Gleneden Beach, OR, 2002).

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Authors
Tian, L., Wang, X.-W., Wu, A.-K., Fan, Y., Friedman, J., Dahlin, A., Waldor, M. K., Weinstock, G. M., Weiss, S. T., & Liu, Y.-Y.
Affiliations
  • Brigham and Women's Hospital (US)
  • Rutgers, The State University of New Jersey (US)
  • Hebrew University of Jerusalem (IL)
  • The Jackson Laboratory for Genomic Medicine (US)
Corresponding author
Liu, Yang-Yu
Venue
Nature Communications
Published
2020-12-04
Volume
11
Issue
1
Pages
6217-6217
ISSN
2041-1723 (ISSN-L)
OpenAlex
W3015439700
Cited by
380
References
67
Citations by year
2026: 68 · 2025: 87 · 2024: 73 · 2023: 64 · 2022: 42 · 2021: 34 · 2020: 10 · 2019: 1 · 2018: 1
FWCI
12.41
Type
journal article
Language
en
Open access
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • The Mouseion at the JAXlibrary (Jackson Laboratory) (submittedVersion, cc-by)
  • APS
Funders
  • U.S. Department of Health & Human Services | NIH | NIH Office of the Director (UH3OD023268)
  • U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases (U19AI095219)
  • U.S. Department of Health & Human Services | NIH | National Heart, Lung, and Blood Institute (U01HL089856)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Keywords
functional redundancy, human microbiome, horizontal gene transfer, selection pressure, fecal microbiota transplantation, microbiome resilience
MeSH terms
Gastrointestinal Microbiome, Algorithms, Bacteria, Feces, Humans, Models, Genetic, Gene Transfer, Horizontal, Gastrointestinal Tract, Gene Regulatory Networks, Metagenome, Metagenomics, Microbiota

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