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

  1. Naïma Jesse Madi
  2. Daisy Chen
  3. Richard Wolff
  4. B Jesse Shapiro  Is a corresponding author
  5. Nandita R Garud  Is a corresponding author
  1. University of Montreal, Canada
  2. University of California, Los Angeles, United States
  3. McGill University, Canada

Abstract

The human gut microbiome contains a diversity of microbial species that varies in composition over time and across individuals. These species (and strains within species) can migrate across hosts and evolve by mutation and recombination within hosts. 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 based on ecological observations and theory: 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 within taxa. Previously, using 16S rRNA gene amplicon data across a range of environments, 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' reaches a plateau 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 shotgun-sequenced fecal metagenomes from cohorts of healthy human hosts. We find that both intra-species polymorphism and strain number are positively correlated with community Shannon diversity. This trend is consistent with DBD, although we cannot exclude abiotic drivers of 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 then becomes negative-consistent with DBD eventually giving way to EC. Also supporting a complex mixture of DBD and EC, the number of strains per focal species is positively associated with Shannon diversity but negatively associated with richness. Finally, we show that higher community diversity predicts gene loss in a focal species 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.

Data availability

The raw sequencing reads for the metagenomic samples used in this study were downloaded from Human Microbiome Project Consortium 2012 and Lloyd-Price et al. (2017) (URL: https://aws.amazon.com/datasets/human-microbiome-project/); and Poyet et al. 2019 (NCBI accession number PRJNA544527). All computer code for this paper is available at https://github.com/Naima16/DBD_in_gut_microbiome.

The following previously published data sets were used

Article and author information

Author details

  1. Naïma Jesse Madi

    Département de Sciences Biologiques, University of Montreal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  2. Daisy Chen

    Computational and Systems Biology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6516-7029
  3. Richard Wolff

    Department of Ecology and Evolutionary Biology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. B Jesse Shapiro

    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
  5. Nandita R Garud

    Department of Ecology and Evolutionary Biology, University of California, Los Angeles, Los Angeles, United States
    For correspondence
    ngarud@ucla.edu
    Competing interests
    The authors declare that no competing interests exist.

Funding

Paul Allen Frontiers Group

  • Nandita R Garud

Research Corporation for Science Advancement

  • Nandita R Garud

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.

Ethics

Human subjects: All human-derived samples used in this study were previously published. We include no additional identifiable or sensitive information.

Reviewing Editor

  1. Sara Mitri, University of Lausanne, Switzerland

Version history

  1. Preprint posted: March 8, 2022 (view preprint)
  2. Received: March 16, 2022
  3. Accepted: February 8, 2023
  4. Accepted Manuscript published: February 9, 2023 (version 1)
  5. Version of Record published: February 28, 2023 (version 2)

Copyright

© 2023, 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

  • 1,476
    Page views
  • 212
    Downloads
  • 7
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, 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. Daisy Chen
  3. Richard Wolff
  4. B Jesse Shapiro
  5. Nandita R Garud
(2023)
Community diversity is associated with intra-species genetic diversity and gene loss in the human gut microbiome
eLife 12:e78530.
https://doi.org/10.7554/eLife.78530

Share this article

https://doi.org/10.7554/eLife.78530

Further reading

    1. Ecology
    2. Plant Biology
    Jamie Mitchel Waterman, Tristan Michael Cofer ... Matthias Erb
    Research Article

    Volatiles emitted by herbivore-attacked plants (senders) can enhance defenses in neighboring plants (receivers), however, the temporal dynamics of this phenomenon remain poorly studied. Using a custom-built, high-throughput proton transfer reaction time-of-flight mass spectrometry (PTR-ToF-MS) system, we explored temporal patterns of volatile transfer and responses between herbivore-attacked and undamaged maize plants. We found that continuous exposure to natural blends of herbivore-induced volatiles results in clocked temporal response patterns in neighboring plants, characterized by an induced terpene burst at the onset of the second day of exposure. This delayed burst is not explained by terpene accumulation during the night, but coincides with delayed jasmonate accumulation in receiver plants. The delayed burst occurs independent of day:night light transitions and cannot be fully explained by sender volatile dynamics. Instead, it is the result of a stress memory from volatile exposure during the first day and secondary exposure to bioactive volatiles on the second day. Our study reveals that prolonged exposure to natural blends of stress-induced volatiles results in a response that integrates priming and direct induction into a distinct and predictable temporal response pattern. This provides an answer to the long-standing question of whether stress volatiles predominantly induce or prime plant defenses in neighboring plants, by revealing that they can do both in sequence.

    1. Ecology
    Congnan Sun, Yoel Hassin ... Yossi Yovel
    Research Article

    Covid-19 lockdowns provided ecologists with a rare opportunity to examine how animals behave when humans are absent. Indeed many studies reported various effects of lockdowns on animal activity, especially in urban areas and other human-dominated habitats. We explored how Covid-19 lockdowns in Israel have influenced bird activity in an urban environment by using continuous acoustic recordings to monitor three common bird species that differ in their level of adaptation to the urban ecosystem: (1) the hooded crow, an urban exploiter, which depends heavily on anthropogenic resources; (2) the rose-ringed parakeet, an invasive alien species that has adapted to exploit human resources; and (3) the graceful prinia, an urban adapter, which is relatively shy of humans and can be found in urban habitats with shrubs and prairies. Acoustic recordings provided continuous monitoring of bird activity without an effect of the observer on the animal. We performed dense sampling of a 1.3 square km area in northern Tel-Aviv by placing 17 recorders for more than a month in different micro-habitats within this region including roads, residential areas and urban parks. We monitored both lockdown and no-lockdown periods. We portray a complex dynamic system where the activity of specific bird species depended on many environmental parameters and decreases or increases in a habitat-dependent manner during lockdown. Specifically, urban exploiter species decreased their activity in most urban habitats during lockdown, while human adapter species increased their activity during lockdown especially in parks where humans were absent. Our results also demonstrate the value of different habitats within urban environments for animal activity, specifically highlighting the importance of urban parks. These species- and habitat-specific changes in activity might explain the contradicting results reported by others who have not performed a habitat specific analysis.