Substrate stiffness impacts early biofilm formation by modulating Pseudomonas aeruginosa twitching motility

  1. Sofia Gomez
  2. Lionel Bureau
  3. Karin John
  4. Elise-Noëlle Chêne
  5. Delphine Débarre  Is a corresponding author
  6. Sigolene Lecuyer  Is a corresponding author
  1. Université Grenoble Alpes, CNRS, France
  2. ENS de Lyon, CNRS, France
  3. ENS de Lyon,CNRS, France

Abstract

Surface-associated lifestyles dominate in the bacterial world. Large multicellular assemblies, called biofilms, are essential to the survival of bacteria in harsh environments, and are closely linked to antibiotic resistance in pathogenic strains. Biofilms stem from the surface colonization of a wide variety of substrates encountered by bacteria, from living tissues to inert materials. Here, we demonstrate experimentally that the promiscuous opportunistic pathogen Pseudomonas aeruginosa explores substrates differently based on their rigidity, leading to striking variations in biofilm structure, exopolysaccharides (EPS) distribution, strain mixing during co-colonization and phenotypic expression. Using simple kinetic models, we show that these phenotypes arise through a mechanical interaction between the elasticity of the substrate and the type IV pilus (T4P) machinery, that mediates the surface-based motility called twitching. Together, our findings reveal a new role for substrate softness in the spatial organization of bacteria in complex microenvironments, with far-reaching consequences on efficient biofilm formation.

Data availability

Figure 2 - Source Data and Figure 3 - Source Data contain the numerical data used to generate the figures.

Article and author information

Author details

  1. Sofia Gomez

    Université Grenoble Alpes, CNRS, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Lionel Bureau

    Université Grenoble Alpes, CNRS, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Karin John

    Université Grenoble Alpes, CNRS, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1678-6880
  4. Elise-Noëlle Chêne

    Laboratoire de Physique, ENS de Lyon, CNRS, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Delphine Débarre

    Université Grenoble Alpes, CNRS, Grenoble, France
    For correspondence
    delphine.debarre@univ-grenoble-alpes.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0513-6172
  6. Sigolene Lecuyer

    Laboratoire de Physique, ENS de Lyon,CNRS, Lyon, France
    For correspondence
    sigolene.lecuyer@ens-lyon.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7393-2667

Funding

Agence Nationale de la Recherche (ANR-19-CE42-0010)

  • Delphine Débarre

Labex Tec21 (ANR-11-LABX-0030)

  • Lionel Bureau
  • Karin John
  • Delphine Débarre
  • Sigolene Lecuyer

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

Reviewing Editor

  1. Tâm Mignot, CNRS-Aix Marseille University, France

Version history

  1. Preprint posted: February 19, 2022 (view preprint)
  2. Received: June 15, 2022
  3. Accepted: May 5, 2023
  4. Accepted Manuscript published: May 9, 2023 (version 1)
  5. Version of Record published: June 9, 2023 (version 2)

Copyright

© 2023, Gomez 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. Sofia Gomez
  2. Lionel Bureau
  3. Karin John
  4. Elise-Noëlle Chêne
  5. Delphine Débarre
  6. Sigolene Lecuyer
(2023)
Substrate stiffness impacts early biofilm formation by modulating Pseudomonas aeruginosa twitching motility
eLife 12:e81112.
https://doi.org/10.7554/eLife.81112

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https://doi.org/10.7554/eLife.81112

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