Universal gut microbial relationships in the gut microbiome of wild baboons

  1. Kimberly E Roche
  2. Johannes R Bjork
  3. Mauna R Dasari
  4. Laura Grieneisen
  5. David AWAM Jansen
  6. Trevor J Gould
  7. Laurence R Gesquiere
  8. Luis B Barreiro
  9. Susan C Alberts
  10. Ran Blekhman
  11. Jack A Gilbert
  12. Jenny Tung
  13. Sayan Mukherjee
  14. Elizabeth A Archie  Is a corresponding author
  1. Duke University, United States
  2. University of Groningen, Netherlands
  3. University of Pittsburgh, United States
  4. University of Notre Dame, United States
  5. University of British Columbia, Canada
  6. University of Chicago, United States
  7. University of California, San Diego, United States

Abstract

Ecological relationships between bacteria mediate the services that gut microbiomes provide to their hosts. Knowing the overall direction and strength of these relationships is essential to learn how ecology scales up to affect microbiome assembly, dynamics, and host health. However, whether bacterial relationships are generalizable across hosts or personalized to individual hosts is debated. Several eco-evolutionary processes could personalize microbiome community ecology, but the few studies that have tested this idea find that bacterial interactions are largely consistent (i.e., 'universal') across hosts. Here we apply a robust, multinomial logistic-normal modeling framework to extensive time series data (5,534 samples from 56 wild baboons over 13 years) to infer thousands of correlations in bacterial abundance in individual hosts and test the degree to which bacterial abundance correlations are 'universal'. We also compare these patterns to two human data sets. We find that, in baboons, most bacterial correlations are weak, negative, and universal across hosts, such that shared correlation patterns dominate over host-specific correlations by almost 2-fold. Further, taxon pairs that had inconsistent correlation signs (either positive or negative) in different hosts always had weak correlations within hosts. From the host perspective, host pairs with the most similar bacterial correlation patterns also had similar microbiome taxonomic compositions and tended to be genetic relatives. Compared to humans, universality in baboons was similar to that in human infants, and stronger than one data set from human adults. Bacterial families that showed universal correlations in human infants also tended to show universal correlations in baboons. Together, our work contributes new tools for analyzing the universality of bacterial associations across hosts, with implications for microbiome personalization, community assembly and stability, and for designing microbiome interventions to improve host health.

Data availability

16S rRNA gene sequences are available on EBI-ENA (project 590 ERP119849) and Qiita (study 12949). Analyzed data and code are available on GitHub at: https://github.com/kimberlyroche/rulesoflife

The following previously published data sets were used

Article and author information

Author details

  1. Kimberly E Roche

    Program in Computational Biology and Bioinformatics, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
  2. Johannes R Bjork

    Department of Gastroenterology and Hepatology, University of Groningen, Groningen, Netherlands
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9768-1946
  3. Mauna R Dasari

    Department of Biological Sciences, University of Pittsburgh, Pittsburgh, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1956-2500
  4. Laura Grieneisen

    Department of Biology, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
  5. David AWAM Jansen

    Department of Biological Sciences, University of Notre Dame, Notre Dame, United States
    Competing interests
    No competing interests declared.
  6. Trevor J Gould

    Department of Biology, University of British Columbia, Kelowna, Canada
    Competing interests
    No competing interests declared.
  7. Laurence R Gesquiere

    Department of Biology, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
  8. Luis B Barreiro

    Committee on Genetics, Genomics, and Systems Biology, University of Chicago, Chicago, United States
    Competing interests
    No competing interests declared.
  9. Susan C Alberts

    Department of Biology, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1313-488X
  10. Ran Blekhman

    Department of Medicine, University of Chicago, Chicago, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3218-613X
  11. Jack A Gilbert

    Department of Pediatrics, University of California, San Diego, San Diego, United States
    Competing interests
    No competing interests declared.
  12. Jenny Tung

    Department of Biology, Duke University, Durham, United States
    Competing interests
    Jenny Tung, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0416-2958
  13. Sayan Mukherjee

    Program in Computational Biology and Bioinformatics, Duke University, Durham, United States
    Competing interests
    No competing interests declared.
  14. Elizabeth A Archie

    Department of Biological Sciences, University of Notre Dame, Notre Dame, United States
    For correspondence
    earchie@nd.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1187-0998

Funding

National Science Foundation (DEB1840223)

  • Jack A Gilbert
  • Elizabeth A Archie

National Institute on Aging (R01AG071684)

  • Elizabeth A Archie

National Institute on Aging (R21AG055777)

  • Ran Blekhman
  • Elizabeth A Archie

National Institute on Aging (R01AG053330)

  • Elizabeth A Archie

National Institute of General Medical Sciences (R35GM128716)

  • Ran Blekhman

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Dario Riccardo Valenzano, Leibniz Institute on Aging, Germany

Publication history

  1. Received: September 1, 2022
  2. Accepted: May 8, 2023
  3. Accepted Manuscript published: May 9, 2023 (version 1)

Copyright

© 2023, Roche et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Kimberly E Roche
  2. Johannes R Bjork
  3. Mauna R Dasari
  4. Laura Grieneisen
  5. David AWAM Jansen
  6. Trevor J Gould
  7. Laurence R Gesquiere
  8. Luis B Barreiro
  9. Susan C Alberts
  10. Ran Blekhman
  11. Jack A Gilbert
  12. Jenny Tung
  13. Sayan Mukherjee
  14. Elizabeth A Archie
(2023)
Universal gut microbial relationships in the gut microbiome of wild baboons
eLife 12:e83152.
https://doi.org/10.7554/eLife.83152

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