Interactions between strains govern the eco-evolutionary dynamics of microbial communities

  1. Akshit Goyal
  2. Leonora S Bittleston
  3. Gabriel E Leventhal
  4. Lu Lu
  5. Otto Cordero  Is a corresponding author
  1. Massachusetts Institute of Technology, United States

Abstract

Genomic data has revealed that genotypic variants of the same species, i.e., strains, coexist and are abundant in natural microbial communities. However, it is not clear if strains are ecologically equivalent, and at what characteristic genetic distance they might exhibit distinct interactions and dynamics. Here, we address this problem by tracking 10 taxonomically diverse microbial communities from the pitcher plant Sarracenia purpurea in the laboratory for more than 300 generations. Using metagenomic sequencing, we reconstruct their dynamics over time and across scales, from distant phyla to closely related genotypes. We find that most strains are not ecologically equivalent and exhibit distinct dynamical patterns, often being significantly more correlated with strains from another species than their own. Although even a single mutation can affect laboratory strains, on average, natural strains typically decouple in their dynamics beyond a genetic distance of 100 base pairs. Using mathematical consumer-resource models, we show that these taxonomic patterns emerge naturally from ecological interactions between community members, but only if the interactions are coarse-grained at the level of strains, not species. Finally, by analyzing genomic differences between strains, we identify major functional hubs such as transporters, regulators, and carbohydrate-catabolizing enzymes, which might be the basis for strain-specific interactions. Our work suggests that fine-scale genetic differences in natural communities could be created and stabilized via the rapid diversification of ecological interactions between strains.

Data availability

Raw sequencing reads are available in the NCBI Sequence Read Archive (BioSample SAMN17005333). Assembled genomes have been deposited in the NCBI GenBank database (BioProject PRJNA682646). Genome metadata and accession numbers are provided in Supplementary Table S1.

The following data sets were generated

Article and author information

Author details

  1. Akshit Goyal

    Department of Physics, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Leonora S Bittleston

    Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Gabriel E Leventhal

    Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Lu Lu

    Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Otto Cordero

    Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    ottox@mit.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2695-270X

Funding

Gordon and Betty Moore Foundation (GBMF4513)

  • Akshit Goyal

Human Frontiers Science Program (LT000643/2016-L)

  • Gabriel E Leventhal

James S. McDonnell Foundation (220020477)

  • Leonora S Bittleston

National Science Foundation (1655983)

  • Otto Cordero

Simons Foundation (542395)

  • Otto Cordero

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 Biology Tübingen, Germany

Publication history

  1. Preprint posted: January 4, 2021 (view preprint)
  2. Received: October 25, 2021
  3. Accepted: February 3, 2022
  4. Accepted Manuscript published: February 4, 2022 (version 1)
  5. Version of Record published: February 28, 2022 (version 2)

Copyright

© 2022, Goyal 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. Akshit Goyal
  2. Leonora S Bittleston
  3. Gabriel E Leventhal
  4. Lu Lu
  5. Otto Cordero
(2022)
Interactions between strains govern the eco-evolutionary dynamics of microbial communities
eLife 11:e74987.
https://doi.org/10.7554/eLife.74987

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