Competition between lysogenic and sensitive bacteria is determined by the fitness costs of the different emerging phage-resistance strategies

Abstract

Many bacterial genomes carry prophages whose induction can eliminate competitors. In response, bacteria may become resistant by modifying surface receptors, by lysogenization, or by other poorly known processes. All these mechanisms affect bacterial fitness and population dynamics. To understand the evolution of phage resistance, we co-cultivated a phage-sensitive strain (BJ1) and a poly-lysogenic Klebsiella pneumoniae strain (ST14) under different phage pressures. The population yield remained stable after 30 days. Surprisingly, the initially sensitive strain remained in all populations and its frequency was highest when phage pressure was strongest. Resistance to phages in these populations emerged initially through mutations preventing capsule biosynthesis. Protection through lysogeny was rarely observed because the lysogens have increased death rates due to prophage induction. Unexpectedly, the adaptation process changed at longer time scales the frequency of capsulated cells in BJ1 populations increased again, because the production of capsule was fine-tuned, reducing the ability of phage to absorb. Contrary to the lysogens, these capsulated resistant clones are pan-resistant to a large panel of phages. Intriguingly, some clones exhibited transient non-genetic resistance to phages, suggesting an important role of phenotypic resistance in coevolving populations. Our results show that interactions between lysogens and sensitive strains are shaped by antagonistic co-evolution between phages and bacteria. These processes may involve key physiological traits, such as the capsule, and depend on the time frame of the evolutionary process. At short time scales, simple and costly inactivating mutations are adaptive, but in the long-term, changes drawing more favorable trade-offs between resistance to phages and cell fitness become prevalent.

Data availability

All raw data is available on figshare.com; 10.6084/m9.figshare.22101998

The following data sets were generated

Article and author information

Author details

  1. Olaya Rendueles

    Institut Pasteur, Paris, France
    For correspondence
    olaya.rendueles-garcia@pasteur.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6648-1594
  2. Jorge AM Moura de Sousa

    Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Eduardo PC Rocha

    Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.

Funding

Agence Nationale de la Recherche (ANR 18 CE12 0001 01 ENCAPSULATION)

  • Olaya Rendueles

Agence Nationale de la Recherche (ANR-10-LABX-62-IBEID)

  • Eduardo PC Rocha

Fondation pour la Recherche Médicale (EQU201903007835)

  • Eduardo PC Rocha

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

Reviewing Editor

  1. Samuel L Díaz-Muñoz, University of California, Davis, United States

Version history

  1. Preprint posted: July 12, 2022 (view preprint)
  2. Received: September 15, 2022
  3. Accepted: March 16, 2023
  4. Accepted Manuscript published: March 28, 2023 (version 1)
  5. Version of Record published: April 5, 2023 (version 2)
  6. Version of Record updated: April 6, 2023 (version 3)

Copyright

© 2023, Rendueles 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. Olaya Rendueles
  2. Jorge AM Moura de Sousa
  3. Eduardo PC Rocha
(2023)
Competition between lysogenic and sensitive bacteria is determined by the fitness costs of the different emerging phage-resistance strategies
eLife 12:e83479.
https://doi.org/10.7554/eLife.83479

Share this article

https://doi.org/10.7554/eLife.83479

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