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Pneumococcal competence is a populational health sensor driving multilevel heterogeneity in response to antibiotics

Author

Listed:
  • Marc Prudhomme

    (Centre Nationale de la Recherche Scientifique (CNRS)
    Université Paul Sabatier (Toulouse III))

  • Calum H. G. Johnston

    (Centre Nationale de la Recherche Scientifique (CNRS)
    Université Paul Sabatier (Toulouse III))

  • Anne-Lise Soulet

    (Centre Nationale de la Recherche Scientifique (CNRS)
    Université Paul Sabatier (Toulouse III))

  • Anne Boyeldieu

    (Centre Nationale de la Recherche Scientifique (CNRS)
    Université Paul Sabatier (Toulouse III))

  • David Lemos

    (Centre Nationale de la Recherche Scientifique (CNRS)
    Université Paul Sabatier (Toulouse III))

  • Nathalie Campo

    (Centre Nationale de la Recherche Scientifique (CNRS)
    Université Paul Sabatier (Toulouse III))

  • Patrice Polard

    (Centre Nationale de la Recherche Scientifique (CNRS)
    Université Paul Sabatier (Toulouse III))

Abstract

Competence for natural transformation is a central driver of genetic diversity in bacteria. In the human pathogen Streptococcus pneumoniae, competence exhibits a populational character mediated by the stress-induced ComABCDE quorum-sensing (QS) system. Here, we explore how this cell-to-cell communication mechanism proceeds and the functional properties acquired by competent cells grown under lethal stress. We show that populational competence development depends on self-induced cells stochastically emerging in response to stresses, including antibiotics. Competence then propagates through the population from a low threshold density of self-induced cells, defining a biphasic Self-Induction and Propagation (SI&P) QS mechanism. We also reveal that a competent population displays either increased sensitivity or improved tolerance to lethal doses of antibiotics, dependent in the latter case on the competence-induced ComM division inhibitor. Remarkably, these surviving competent cells also display an altered transformation potential. Thus, the unveiled SI&P QS mechanism shapes pneumococcal competence as a health sensor of the clonal population, promoting a bet-hedging strategy that both responds to and drives cells towards heterogeneity.

Suggested Citation

  • Marc Prudhomme & Calum H. G. Johnston & Anne-Lise Soulet & Anne Boyeldieu & David Lemos & Nathalie Campo & Patrice Polard, 2024. "Pneumococcal competence is a populational health sensor driving multilevel heterogeneity in response to antibiotics," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49853-2
    DOI: 10.1038/s41467-024-49853-2
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    References listed on IDEAS

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    1. Léa Marie & Chiara Rapisarda & Violette Morales & Mathieu Bergé & Thomas Perry & Anne-Lise Soulet & Clémence Gruget & Han Remaut & Rémi Fronzes & Patrice Polard, 2017. "Bacterial RadA is a DnaB-type helicase interacting with RecA to promote bidirectional D-loop extension," Nature Communications, Nature, vol. 8(1), pages 1-14, August.
    2. Gürol M. Süel & Jordi Garcia-Ojalvo & Louisa M. Liberman & Michael B. Elowitz, 2006. "An excitable gene regulatory circuit induces transient cellular differentiation," Nature, Nature, vol. 440(7083), pages 545-550, March.
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