1. Ecology
  2. Microbiology and Infectious Disease
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Flow environment and matrix structure interact to determine spatial competition in Pseudomonas aeruginosa biofilms

  1. Carey D Nadell
  2. Deirdre Ricaurte
  3. Jing Yan
  4. Knut Drescher
  5. Bonnie Bassler  Is a corresponding author
  1. Max Planck Institute for Terrestrial Microbiology, Germany
  2. Princeton University, United States
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Cite as: eLife 2017;6:e21855 doi: 10.7554/eLife.21855

Abstract

Bacteria often live in biofilms, which are microbial communities surrounded by a secreted extracellular matrix. Here, we demonstrate that hydrodynamic flow and matrix organization interact to shape competitive dynamics in Pseudomonas aeruginosa biofilms. Irrespective of initial frequency, in competition with matrix mutants, wild type cells always increase in relative abundance in planar microfluidic devices under simple flow regimes. By contrast, in microenvironments with complex, irregular flow profiles - which are common in natural environments - wild type matrix-producing and isogenic non-producing strains can coexist. This result stems from local obstruction of flow by wild-type matrix producers, which generates regions of near-zero shear that allow matrix mutants to locally accumulate. Our findings connect the evolutionary stability of matrix production with the hydrodynamics and spatial structure of the surrounding environment, providing a potential explanation for the variation in biofilm matrix secretion observed among bacteria in natural environments.

Article and author information

Author details

  1. Carey D Nadell

    Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Deirdre Ricaurte

    Department of Molecular Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jing Yan

    Department of Molecular Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Knut Drescher

    Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Bonnie 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 0000-0002-0043-746X

Funding

Alexander von Humboldt Stiftung

  • Carey D Nadell
  • Bonnie Bassler

Human Frontier Science Program

  • Knut Drescher

Max-Planck-Gesellschaft

  • Knut Drescher
  • Bonnie Bassler

Howard Hughes Medical Institute

  • Bonnie Bassler

National Institutes of Health

  • Bonnie Bassler

National Science Foundation

  • Bonnie Bassler

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

Reviewing Editor

  1. Sara Mitri, University of Lausanne, Switzerland

Publication history

  1. Received: September 25, 2016
  2. Accepted: January 11, 2017
  3. Accepted Manuscript published: January 13, 2017 (version 1)
  4. Version of Record published: January 31, 2017 (version 2)

Copyright

© 2017, Nadell 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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