Does diversity beget diversity in microbiomes?

  1. Naïma Jesse Madi
  2. Michiel Vos
  3. Carmen Lia Murall
  4. Pierre Legendre
  5. B. Jesse Shapiro  Is a corresponding author
  1. University of Montreal, Canada
  2. University of Exeter, United Kingdom
  3. McGill University, Canada

Abstract

Microbes are embedded in complex communities where they engage in a wide array of intra- and inter-specific interactions. The extent to which these interactions drive or impede microbiome diversity is not well understood. Historically, two contrasting hypotheses have been suggested to explain how species interactions could influence diversity. 'Ecological Controls' (EC) predicts a negative relationship, where the evolution or migration of novel types is constrained as niches become filled. In contrast, 'Diversity Begets Diversity' (DBD) predicts a positive relationship, with existing diversity promoting the accumulation of further diversity via niche construction and other interactions. Using high-throughput amplicon sequencing data from the Earth Microbiome Project, we provide evidence that DBD is strongest in low-diversity biomes, but weaker in more diverse biomes, consistent with biotic interactions initially favoring the accumulation of diversity (as predicted by DBD). However, as niches become increasingly filled, diversity hits a plateau (as predicted by EC).

Data availability

All data is available from the Earth Microbiome Project (ftp.microbio.me), as detailed in the Methods. All computer code used for analysis are available at https://github.com/Naima16/dbd.git.

The following previously published data sets were used
    1. Thompson LR et al
    (2017) Earth Microbiome Project
    ftp://ftp.microbio.me/emp/release1/otu_distributions/otu_summary.emp_deblur_90bp.subset_2k.rare_5000.tsv.

Article and author information

Author details

  1. Naïma Jesse Madi

    Sciences Biologiques, University of Montreal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  2. Michiel Vos

    European Centre for Environment and Human Health, University of Exeter, Exeter, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Carmen Lia Murall

    Sciences Biologiques, University of Montreal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1543-4501
  4. Pierre Legendre

    Sciences Biologiques, University of Montreal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. B. Jesse Shapiro

    Microbiology and Immunology, McGill University, Montreal, Canada
    For correspondence
    jesse.shapiro@mcgill.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6819-8699

Funding

Natural Sciences and Engineering Research Council of Canada

  • B. Jesse Shapiro

Canada Research Chairs

  • B. Jesse Shapiro

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

Reviewing Editor

  1. Detlef Weigel, Max Planck Institute for Developmental Biology, Germany

Version history

  1. Received: May 18, 2020
  2. Accepted: November 19, 2020
  3. Accepted Manuscript published: November 20, 2020 (version 1)
  4. Version of Record published: December 22, 2020 (version 2)
  5. Version of Record updated: December 24, 2020 (version 3)

Copyright

© 2020, Madi 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. Naïma Jesse Madi
  2. Michiel Vos
  3. Carmen Lia Murall
  4. Pierre Legendre
  5. B. Jesse Shapiro
(2020)
Does diversity beget diversity in microbiomes?
eLife 9:e58999.
https://doi.org/10.7554/eLife.58999

Share this article

https://doi.org/10.7554/eLife.58999

Further reading

    1. Ecology
    2. Evolutionary Biology
    Naïma Madi, Daisy Chen ... Nandita R Garud
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    How the ecological process of community assembly interacts with intra-species diversity and evolutionary change is a longstanding question. Two contrasting hypotheses have been proposed: Diversity Begets Diversity (DBD), in which taxa tend to become more diverse in already diverse communities, and Ecological Controls (EC), in which higher community diversity impedes diversification. Previously, using 16S rRNA gene amplicon data across a range of microbiomes, we showed a generally positive relationship between taxa diversity and community diversity at higher taxonomic levels, consistent with the predictions of DBD (Madi et al., 2020). However, this positive 'diversity slope' plateaus at high levels of community diversity. Here we show that this general pattern holds at much finer genetic resolution, by analyzing intra-species strain and nucleotide variation in static and temporally sampled metagenomes from the human gut microbiome. Consistent with DBD, both intra-species polymorphism and strain number were positively correlated with community Shannon diversity. Shannon diversity is also predictive of increases in polymorphism over time scales up to ~4-6 months, after which the diversity slope flattens and becomes negative – consistent with DBD eventually giving way to EC. Finally, we show that higher community diversity predicts gene loss at a future time point. This observation is broadly consistent with the Black Queen Hypothesis, which posits that genes with functions provided by the community are less likely to be retained in a focal species' genome. Together, our results show that a mixture of DBD, EC, and Black Queen may operate simultaneously in the human gut microbiome, adding to a growing body of evidence that these eco-evolutionary processes are key drivers of biodiversity and ecosystem function.

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