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Matrix-trapped viruses can prevent invasion of bacterial biofilms by colonizing cells

  1. Matthew C Bond
  2. Lucia Vidakovic
  3. Praveen K Singh
  4. Knut Drescher
  5. Carey D Nadell  Is a corresponding author
  1. Dartmouth, United States
  2. Max Planck Institute for Terrestrial Microbiology, Germany
  3. University of Basel, Switzerland
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Cite this article as: eLife 2021;10:e65355 doi: 10.7554/eLife.65355

Abstract

Bacteriophages can be trapped in the matrix of bacterial biofilms, such that the cells inside them are protected. It is not known whether these phages are still infectious and whether they pose a threat to newly arriving bacteria. Here we address these questions using Escherichia coli and its lytic phage T7. Prior work has demonstrated that T7 phages are bound in the outermost curli polymer layers of the E. coli biofilm matrix. We show that these phages do remain viable and can kill colonizing cells that are T7-susceptible. If cells colonize a resident biofilm before phages do, we find that they can still be killed by phage exposure if it occurs soon thereafter. However, if colonizing cells are present on the biofilm long enough before phage exposure, they gain phage protection via envelopment within curli-producing clusters of the resident biofilm cells.

Data availability

Raw data for the entire study has been provided in the source data file with the re-submission

Article and author information

Author details

  1. Matthew C Bond

    Biological Sciences, Dartmouth, Hanover, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Lucia Vidakovic

    Systems and Synthetic Biology, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5289-5163
  3. Praveen K Singh

    Systems and Synthetic Biology, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0254-7400
  4. Knut Drescher

    University of Basel, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7340-2444
  5. Carey D Nadell

    Biological Sciences, Dartmouth, Hanover, United States
    For correspondence
    carey.d.nadell@dartmouth.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1751-4895

Funding

National Science Foundation (MCB 1817342)

  • Carey D Nadell

National Science Foundation (IOS 2017879)

  • Carey D Nadell

National Institutes of Health (P30-DK117469)

  • Carey D Nadell

National Institutes of Health (2R01AI081838)

  • Carey D Nadell

Cystic Fibrosis Foundation (STANTO15RO)

  • Carey D Nadell

National Institutes of Health (P20-GM113132)

  • Carey D Nadell

Human Frontier Science Program (RGY0077/2020)

  • Carey D Nadell

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

Reviewing Editor

  1. Wenying Shou, University College London, United Kingdom

Publication history

  1. Received: December 1, 2020
  2. Accepted: July 8, 2021
  3. Accepted Manuscript published: July 9, 2021 (version 1)
  4. Version of Record published: August 6, 2021 (version 2)

Copyright

© 2021, Bond 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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