Biofilms deform soft surfaces and disrupt epithelia

  1. Alice Cont
  2. Tamara Rossy
  3. Zainebe Al-Mayyah
  4. Alexandre Persat  Is a corresponding author
  1. Ecole Polytechnique Fédérale de Lausanne, Switzerland

Abstract

During chronic infections and in microbiota, bacteria predominantly colonize their hosts as multicellular structures called biofilms. A common assumption is that biofilms exclusively interact with their hosts biochemically. However, the contributions of mechanics, while being central to the process of biofilm formation, have been overlooked as a factor influencing host physiology. Specifically, how biofilms form on soft, tissue-like materials remains unknown. Here we show that biofilms of the pathogens Vibrio cholerae and Pseudomonas aeruginosa can induce large deformations of soft synthetic hydrogels. Biofilms buildup internal mechanical stress as single cells grow within the elastic matrix. By combining mechanical measurements and mutations in matrix components, we found that biofilms deform by buckling, and that adhesion transmits these forces to their substrates. Finally, we demonstrate that V. cholerae biofilms can generate sufficient mechanical stress to deform and even disrupt soft epithelial cell monolayers, suggesting a mechanical mode of infection.

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Article and author information

Author details

  1. Alice Cont

    Institute for Bioengineering and Global Health Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Tamara Rossy

    Institute for Bioengineering and Global Health Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Zainebe Al-Mayyah

    Institute for Bioengineering and Global Health Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  4. Alexandre Persat

    Institute for Bioengineering and Global Health Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
    For correspondence
    alexandre.persat@epfl.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8426-8255

Funding

Swiss National Science Foundation

  • Alice Cont
  • Tamara Rossy
  • Zainebe Al-Mayyah
  • Alexandre Persat

Cavaglieri Foundation

  • Alice Cont
  • Tamara Rossy
  • Zainebe Al-Mayyah
  • Alexandre Persat

Fondation Beytout

  • Alice Cont
  • Tamara Rossy
  • Zainebe Al-Mayyah
  • Alexandre Persat

Gebert Rüf Stiftung

  • Alice Cont
  • Tamara Rossy
  • Zainebe Al-Mayyah
  • Alexandre Persat

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

Reviewing Editor

  1. Petra Anne Levin, Washington University in St. Louis, United States

Publication history

  1. Received: March 2, 2020
  2. Accepted: August 23, 2020
  3. Accepted Manuscript published: October 7, 2020 (version 1)
  4. Version of Record published: October 14, 2020 (version 2)

Copyright

© 2020, Cont 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. Alice Cont
  2. Tamara Rossy
  3. Zainebe Al-Mayyah
  4. Alexandre Persat
(2020)
Biofilms deform soft surfaces and disrupt epithelia
eLife 9:e56533.
https://doi.org/10.7554/eLife.56533
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