Abstract

Most bacteria exist and interact within polymicrobial communities. These interactions produce unique compounds, increase virulence and augment antibiotic resistance. One community associated with negative healthcare outcomes consists of Pseudomonas aeruginosa and Staphylococcus aureus. When co-cultured, virulence factors secreted by P. aeruginosa reduce metabolism and growth in S. aureus. When grown in vitro, this allows P. aeruginosa to drive S. aureus toward extinction. However, when found in vivo, both species can co-exist. Previous work has noted that this may be due to altered gene expression or mutations. However, little is known about how the growth environment could influence the co-existence of both species. Using a combination of mathematical modeling and experimentation, we show that changes to bacterial growth and metabolism caused by differences in the growth environment can determine the final population composition. We found that changing the carbon source in growth media affects the ratio of ATP to growth rate for both species, a metric we call absolute growth. We found that as a growth environment increases the absolute growth for one species, that species will increasingly dominate the co-culture. This is due to interactions between growth, metabolism, and metabolism-altering virulence factors produced by P. aeruginosa. Finally, we show that the relationship between absolute growth and the final population composition can be perturbed by altering the spatial structure in the community. Our results demonstrate that differences in growth environment can account for conflicting observations regarding the co-existence of these bacterial species in the literature, provides support for the intermediate disturbance hypothesis, and may offer a novel mechanism to manipulate polymicrobial populations.

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All raw experimental data is currently deposited in Dryad and will be publicly available upon publication.

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Article and author information

Author details

  1. Camryn Pajon

    Department of Biological Sciences, Nova Southeastern University, Fort Lauderdale, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Marla C Fortoul

    Department of Biological Sciences, Nova Southeastern University, Fort Lauderdale, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Gabriela Diaz-Tang

    Department of Biological Sciences, Nova Southeastern University, Fort Lauderdale, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Estefania Marin Meneses

    Department of Biological Sciences, Nova Southeastern University, Fort Lauderdale, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Ariane R Kalifa

    Department of Biological Sciences, Nova Southeastern University, Fort Lauderdale, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Elinor Sevy

    Department of Biological Sciences, Nova Southeastern University, Fort Lauderdale, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Taniya Mariah

    Department of Biological Sciences, Nova Southeastern University, Fort Lauderdale, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Brandon M Toscan

    Department of Biological Sciences, Nova Southeastern University, Fort Lauderdale, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Maili Marcelin

    Department of Biological Sciences, Nova Southeastern University, Fort Lauderdale, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Daniella M Hernandez

    Department of Biological Sciences, Nova Southeastern University, Fort Lauderdale, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Melissa M Marzouk

    Department of Biological Sciences, Nova Southeastern University, Fort Lauderdale, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Allison J Lopatkin

    Department of Biology, Barnard College, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Omar Tonsi Eldakar

    Department of Biological Sciences, Nova Southeastern University, Fort Lauderdale, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. Robert P Smith

    Department of Biological Sciences, Nova Southeastern University, Fort Lauderdale, United States
    For correspondence
    rsmith@nova.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2744-7390

Funding

Army Research Office (W911NF-18-1-0443)

  • Camryn Pajon
  • Marla C Fortoul
  • Gabriela Diaz-Tang
  • Estefania Marin Meneses
  • Ariane R Kalifa
  • Elinor Sevy
  • Taniya Mariah
  • Brandon M Toscan
  • Maili Marcelin
  • Daniella M Hernandez
  • Melissa M Marzouk
  • Allison J Lopatkin
  • Omar Tonsi Eldakar
  • Robert P Smith

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

Reviewing Editor

  1. Vaughn S Cooper, University of Pittsburgh, United States

Version history

  1. Preprint posted: September 14, 2022 (view preprint)
  2. Received: September 23, 2022
  3. Accepted: April 18, 2023
  4. Accepted Manuscript published: April 20, 2023 (version 1)
  5. Version of Record published: May 11, 2023 (version 2)
  6. Version of Record updated: May 16, 2023 (version 3)

Copyright

© 2023, Pajon 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. Camryn Pajon
  2. Marla C Fortoul
  3. Gabriela Diaz-Tang
  4. Estefania Marin Meneses
  5. Ariane R Kalifa
  6. Elinor Sevy
  7. Taniya Mariah
  8. Brandon M Toscan
  9. Maili Marcelin
  10. Daniella M Hernandez
  11. Melissa M Marzouk
  12. Allison J Lopatkin
  13. Omar Tonsi Eldakar
  14. Robert P Smith
(2023)
Interactions between metabolism and growth can determine the co-existence of Staphylococcus aureus and Pseudomonas aeruginosa
eLife 12:e83664.
https://doi.org/10.7554/eLife.83664

Share this article

https://doi.org/10.7554/eLife.83664

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