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Within-host competition causes pathogen molecular evolution and perpetual microbiota dysbiosis.

Stevens, Emily J.; Li, Jingdi D.; Hector, Tobias E.; Drew, Georgia C.; Hoang, Kim; Greenrod, Samuel T.E.; Paterson, Steve; King, Kayla C.

Authors

Jingdi D. Li

Tobias E. Hector

Georgia C. Drew

Kim Hoang

Samuel T.E. Greenrod

Steve Paterson

Kayla C. King



Abstract

Pathogens newly invading a host must compete with resident microbiota. This within-host microbial warfare could lead to more severe disease outcomes or constrain the evolution of virulence. By passaging a widespread pathogen (Staphylococcus aureus) and a native microbiota community across populations of nematode hosts, we show that the pathogen displaced microbiota and reduced species richness, but maintained its virulence across generations. Conversely, pathogen populations and microbiota passaged in isolation caused more host harm relative to their respective no-host controls. For the evolved pathogens, this increase in virulence was partly mediated by enhanced biofilm formation and expression of the global virulence regulator agr. Whole genome sequencing revealed shifts in the mode of selection from directional (on pathogens evolving in isolation) to fluctuating (on pathogens evolving in host microbiota). This approach also revealed that competitive interactions with the microbiota drove early pathogen genomic diversification. Metagenome sequencing of the passaged microbiota shows that evolution in pathogen-infected hosts caused a significant reduction in community stability (dysbiosis), along with restrictions on the co-existence of some species based on nutrient competition. Our study reveals how microbial competition during novel infection could determine the patterns and processes of evolution with major consequences for host health.

Citation

Stevens, E. J., Li, J. D., Hector, T. E., Drew, G. C., Hoang, K., Greenrod, S. T., Paterson, S., & King, K. C. (2025). Within-host competition causes pathogen molecular evolution and perpetual microbiota dysbiosis. ISME Journal, Article wraf071. https://doi.org/10.1093/ismejo/wraf071

Journal Article Type Article
Acceptance Date Apr 11, 2025
Online Publication Date Apr 17, 2025
Publication Date Apr 17, 2025
Deposit Date Apr 22, 2025
Publicly Available Date Apr 22, 2025
Journal The ISME Journal
Print ISSN 1751-7362
Electronic ISSN 1751-7370
Publisher Nature Publishing Group
Peer Reviewed Peer Reviewed
Article Number wraf071
DOI https://doi.org/10.1093/ismejo/wraf071
Keywords host-pathogen interactions, pathogenesis, microbiota, bacterial evolution, molecular evolution, virulence
Public URL https://keele-repository.worktribe.com/output/1198320
Publisher URL https://academic.oup.com/ismej/advance-article/doi/10.1093/ismejo/wraf071/8115470

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25-4-11 Main Manuscript (196 Kb)
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Licence
https://creativecommons.org/licenses/by/4.0/

Publisher Licence URL
https://creativecommons.org/licenses/by/4.0/

Copyright Statement
Accepted manuscripts are PDF versions of the author’s final manuscript, as accepted for publication by the journal but prior to copyediting or typesetting. They can be cited using the author(s), article title, journal title, year of online publication, and DOI. They will be replaced by the final typeset articles, which may therefore contain changes. The DOI will remain the same throughout.

© The Author(s) 2025. Published by Oxford University Press on behalf of the International Society for Microbial Ecology

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.






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