Selection on plastic adherence leads to hyper-multicellular strains and incidental virulence in the budding yeast

Abstract

Many disease-causing microbes are not obligate pathogens; rather, they are environmental microbes taking advantage of an ecological opportunity. The existence of microbes whose life cycle does not require a host and are not normally pathogenic, yet are well-suited to host exploitation, is an evolutionary puzzle. One hypothesis posits that selection in the environment may favor traits that incidentally lead to pathogenicity and virulence, or serve as pre-adaptations for survival in a host. An example of such a trait is surface adherence. To experimentally test the idea of 'accidental virulence', replicate populations of Saccharomyces cerevisiae were evolved to attach to a plastic bead for hundreds of generations. Along with plastic adherence, two multicellular phenotypes- biofilm formation and flor formation- increased; another phenotype, pseudohyphal growth, responded to the nutrient limitation. Thus, experimental selection led to the evolution of highly-adherent, hyper-multicellular strains. Wax moth larvae injected with evolved hyper-multicellular strains were significantly more likely to die than those injected with evolved non-multicellular strains. Hence, selection on plastic adherence incidentally led to the evolution of enhanced multicellularity and increased virulence. Our results support the idea that selection for a trait beneficial in the open environment can inadvertently generate opportunistic, 'accidental' pathogens.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for Figures 1, 2, and 5.

Article and author information

Author details

  1. Luke I Ekdahl

    Department of Biology, College of William and Mary, Williamsburg, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Juliana A Salcedo

    Department of Biology, College of William and Mary, Williamsburg, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Matthew M Dungan

    Department of Biology, College of William and Mary, Williamsburg, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Despina V Mason

    Department of Biology, College of William and Mary, Williamsburg, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Dulguun Myagmarsuren

    Department of Biology, College of William and Mary, Williamsburg, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Helen A Murphy

    Department of Biology, College of William and Mary, Williamsburg, United States
    For correspondence
    hamurphy@wm.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4363-4543

Funding

National Institutes of Health (R15-GM122032)

  • Helen A Murphy

National Science Foundation (DEB-1839555)

  • Helen A Murphy

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

Reviewing Editor

  1. Diane M Harper, University of Michigan, United States

Version history

  1. Preprint posted: June 4, 2022 (view preprint)
  2. Received: June 14, 2022
  3. Accepted: November 1, 2023
  4. Accepted Manuscript published: November 2, 2023 (version 1)

Copyright

© 2023, Ekdahl 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. Luke I Ekdahl
  2. Juliana A Salcedo
  3. Matthew M Dungan
  4. Despina V Mason
  5. Dulguun Myagmarsuren
  6. Helen A Murphy
(2023)
Selection on plastic adherence leads to hyper-multicellular strains and incidental virulence in the budding yeast
eLife 12:e81056.
https://doi.org/10.7554/eLife.81056

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