1. Physics of Living Systems
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Mechanical instability and interfacial energy drive biofilm morphogenesis

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Cite this article as: eLife 2019;8:e43920 doi: 10.7554/eLife.43920

Abstract

Surface-attached bacterial communities called biofilms display a diversity of morphologies. Although structural and regulatory components required for biofilm formation are known, it is not understood how these essential constituents promote biofilm surface morphology. Here, using Vibrio cholerae as our model system, we combine mechanical measurements, theory and simulation, quantitative image analyses, surface energy characterizations, and mutagenesis to show that mechanical instabilities, including wrinkling and delamination, underlie the morphogenesis program of growing biofilms. We also identify interfacial energy as a key driving force for mechanomorphogenesis because it dictates the generation/annihilation of new/existing interfaces. Finally, we discover feedback between mechanomorphogenesis and biofilm expansion, which shapes the overall biofilm contour. The morphogenesis principles we discover in bacterial biofilms, relying on mechanical instabilities and interfacial energies, should be generally applicable to morphogenesis processes in tissues in higher organisms.

Article and author information

Author details

  1. Jing Yan

    Department of Mechanical and Aerospace Engineering, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Chenyi Fei

    Department of Molecular Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8287-4347
  3. Sheng Mao

    Department of Mechanical and Aerospace Engineering, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Alexis Moreau

    Department of Mechanical and Aerospace Engineering, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Ned S Wingreen

    Department of Molecular Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7384-2821
  6. Andrej Košmrlj

    Department of Mechanical and Aerospace Engineering, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6137-9200
  7. Howard A Stone

    Department of Mechanical and Aerospace Engineering, Princeton University, Princeton, United States
    For correspondence
    hastone@princeton.edu
    Competing interests
    The authors declare that no competing interests exist.
  8. Bonnie L Bassler

    Department of Molecular Biology, Princeton University, Princeton, United States
    For correspondence
    bbassler@princeton.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0043-746X

Funding

Howard Hughes Medical Institute

  • Bonnie L Bassler

National Science Foundation

  • Ned S Wingreen
  • Howard A Stone
  • Bonnie L Bassler

National Institutes of Health

  • Bonnie L Bassler

Max Planck Society-Alexander von Humboldt Foundation

  • Bonnie L Bassler

Burroughs Wellcome Fund

  • Jing Yan

National Science Foundation (DMR-1420541)

  • Andrej Košmrlj
  • Howard A Stone

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

Reviewing Editor

  1. Michael T Laub, Massachusetts Institute of Technology, United States

Publication history

  1. Received: November 26, 2018
  2. Accepted: March 6, 2019
  3. Accepted Manuscript published: March 8, 2019 (version 1)

Copyright

© 2019, Yan 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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