1. Ecology
  2. Evolutionary Biology

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
https://doi.org/10.7554/eLife.58999
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS

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.
    https://cdn.elifesciences.org/articles/58999/ftp.microbio.me

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

Publication 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.

Metrics

  • 3,970
    Page views
  • 526
    Downloads
  • 14
    Citations

Article citation count generated by polling the highest count across the following sources: PubMed Central, Crossref, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Categories and tags

Further reading

    1. Ecology
    2. Evolutionary Biology

    Community diversity is associated with intra-species genetic diversity and gene loss in the human gut microbiome

    Naïma Madi, Daisy Chen ... Nandita R Garud
    Research Advance Updated

    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.

    1. Ecology
    2. Evolutionary Biology

    The deep-rooted origin of disulfide-rich spider venom toxins

    Naeem Yusuf Shaikh, Kartik Sunagar
    Research Article Updated

    Spider venoms are a complex concoction of enzymes, polyamines, inorganic salts, and disulfide-rich peptides (DRPs). Although DRPs are widely distributed and abundant, their bevolutionary origin has remained elusive. This knowledge gap stems from the extensive molecular divergence of DRPs and a lack of sequence and structural data from diverse lineages. By evaluating DRPs under a comprehensive phylogenetic, structural and evolutionary framework, we have not only identified 78 novel spider toxin superfamilies but also provided the first evidence for their common origin. We trace the origin of these toxin superfamilies to a primordial knot – which we name ‘Adi Shakti’, after the creator of the Universe according to Hindu mythology – 375 MYA in the common ancestor of Araneomorphae and Mygalomorphae. As the lineages under evaluation constitute nearly 60% of extant spiders, our findings provide fascinating insights into the early evolution and diversification of the spider venom arsenal. Reliance on a single molecular toxin scaffold by nearly all spiders is in complete contrast to most other venomous animals that have recruited into their venoms diverse toxins with independent origins. By comparatively evaluating the molecular evolutionary histories of araneomorph and mygalomorph spider venom toxins, we highlight their contrasting evolutionary diversification rates. Our results also suggest that venom deployment (e.g. prey capture or self-defense) influences evolutionary diversification of DRP toxin superfamilies.

    1. Ecology
    2. Epidemiology and Global Health

    Antibiotic Resistance: A mobile target

    Carolina Oliveira de Santana, Pieter Spealman, Gabriel G Perron
    Insight

    The global spread of antibiotic resistance could be due to a number of factors, and not just the overuse of antibiotics in agriculture and medicine as previously thought.