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Deciphering functional redundancy in the human microbiome

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  • Liang Tian

    (Brigham and Women’s Hospital and Harvard Medical School
    Hong Kong Baptist University
    Hong Kong Baptist University
    Hong Kong Baptist University)

  • Xu-Wen Wang

    (Brigham and Women’s Hospital and Harvard Medical School)

  • Ang-Kun Wu

    (Brigham and Women’s Hospital and Harvard Medical School
    Rutgers University)

  • Yuhang Fan

    (Brigham and Women’s Hospital and Harvard Medical School
    Stanford University)

  • Jonathan Friedman

    (The Hebrew University of Jerusalem)

  • Amber Dahlin

    (Brigham and Women’s Hospital and Harvard Medical School)

  • Matthew K. Waldor

    (Brigham and Women’s Hospital and Harvard Medical School
    Howard Hughes Medical Institute)

  • George M. Weinstock

    (The Jackson Laboratory for Genomic Medicine)

  • Scott T. Weiss

    (Brigham and Women’s Hospital and Harvard Medical School)

  • Yang-Yu Liu

    (Brigham and Women’s Hospital and Harvard Medical School)

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.

Suggested Citation

  • Liang Tian & Xu-Wen Wang & Ang-Kun Wu & Yuhang Fan & Jonathan Friedman & Amber Dahlin & Matthew K. Waldor & George M. Weinstock & Scott T. Weiss & Yang-Yu Liu, 2020. "Deciphering functional redundancy in the human microbiome," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-19940-1
    DOI: 10.1038/s41467-020-19940-1
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    Cited by:

    1. Vanessa R. Marcelino & Caitlin Welsh & Christian Diener & Emily L. Gulliver & Emily L. Rutten & Remy B. Young & Edward M. Giles & Sean M. Gibbons & Chris Greening & Samuel C. Forster, 2023. "Disease-specific loss of microbial cross-feeding interactions in the human gut," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    2. Leyuan Li & Tong Wang & Zhibin Ning & Xu Zhang & James Butcher & Joeselle M. Serrana & Caitlin M. A. Simopoulos & Janice Mayne & Alain Stintzi & David R. Mack & Yang-Yu Liu & Daniel Figeys, 2023. "Revealing proteome-level functional redundancy in the human gut microbiome using ultra-deep metaproteomics," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Benjamin H. Good & Layton B. Rosenfeld, 2023. "Eco-evolutionary feedbacks in the human gut microbiome," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    4. Xu-Wen Wang & Yang Hu & Giulia Menichetti & Francine Grodstein & Shilpa N. Bhupathiraju & Qi Sun & Xuehong Zhang & Frank B. Hu & Scott T. Weiss & Yang-Yu Liu, 2023. "Nutritional redundancy in the human diet and its application in phenotype association studies," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Ziheng Peng & Xun Qian & Yu Liu & Xiaomeng Li & Hang Gao & Yining An & Jiejun Qi & Lan Jiang & Yiran Zhang & Shi Chen & Haibo Pan & Beibei Chen & Chunling Liang & Marcel G. A. Heijden & Gehong Wei & S, 2024. "Land conversion to agriculture induces taxonomic homogenization of soil microbial communities globally," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

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