Interactions between metabolism and growth can determine the co-existence of Staphylococcus aureus and Pseudomonas aeruginosa
- Nova Southeastern University, United States
- Barnard College, United States
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.
Data availability
All raw experimental data is currently deposited in Dryad and will be publicly available upon publication.
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Interactions between metabolism and growth can determine the co-existence of Staphylococcus aureus and Pseudomonas aeruginosaDryad Digital Repository, doi:10.5061/dryad.fn2z34tz3.
Article and author information
Author details
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
- Vaughn S Cooper, University of Pittsburgh, United States
Version history
- Preprint posted: September 14, 2022 (view preprint)
- Received: September 23, 2022
- Accepted: April 18, 2023
- Accepted Manuscript published: April 20, 2023 (version 1)
- Version of Record published: May 11, 2023 (version 2)
- 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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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
Further reading
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