eDNA-stimulated cell dispersion from Caulobacter crescentus biofilms upon oxygen limitation is dependent on a toxin-antitoxin system

  1. Cecile Berne
  2. Sebastien Zappa
  3. Yves V Brun  Is a corresponding author
  1. University of Montreal, Canada

Abstract

In their natural environment, most bacteria preferentially live as complex surface-attached multicellular colonies called biofilms. Biofilms begin with a few cells adhering to a surface, where they multiply to form a mature colony. When conditions deteriorate, cells can leave the biofilm. This dispersion is thought to be an important process that modifies the overall biofilm architecture and that promotes colonization of new environments. In Caulobacter crescentus biofilms, extracellular DNA (eDNA) is released upon cell death and prevents newborn cells from joining the established biofilm. Thus, eDNA promotes the dispersal of newborn cells and the subsequent colonization of new environments. These observations suggest that eDNA is a cue for sensing detrimental environmental conditions in the biofilm. Here we show that the toxin-antitoxin system (TAS) ParDE4 stimulates cell death in areas of a biofilm with decreased O2 availability. In conditions where O2 availability is low, eDNA concentration is correlated with cell death. Cell dispersal away from biofilms is decreased when parDE4 is deleted, probably due to the lower local eDNA concentration. Expression of parDE4 is positively regulated by O2 and the expression of this operon is decreased in biofilms where O2 availability is low. Thus, a programmed cell death mechanism using an O2-regulated TAS stimulates dispersal away from areas of a biofilm with decreased O2 availability and favors colonization of a new, more hospitable environment.

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Author details

  1. Cecile Berne

    Département de Microbiologie, Infectiologie et Immunologie, University of Montreal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3731-9317
  2. Sebastien Zappa

    Département de Microbiologie, Infectiologie et Immunologie, University of Montreal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3190-9199
  3. Yves V Brun

    Département de Microbiologie, Infectiologie et Immunologie, University of Montreal, Montreal, Canada
    For correspondence
    yves.brun@umontreal.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9289-1909

Funding

Canada Research Chairs

  • Yves V Brun

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

Reviewing Editor

  1. Vaughn S Cooper, University of Pittsburgh, United States

Version history

  1. Received: June 6, 2022
  2. Preprint posted: June 17, 2022 (view preprint)
  3. Accepted: December 2, 2022
  4. Accepted Manuscript published: December 7, 2022 (version 1)
  5. Version of Record published: January 19, 2023 (version 2)

Copyright

© 2022, Berne 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. Cecile Berne
  2. Sebastien Zappa
  3. Yves V Brun
(2022)
eDNA-stimulated cell dispersion from Caulobacter crescentus biofilms upon oxygen limitation is dependent on a toxin-antitoxin system
eLife 11:e80808.
https://doi.org/10.7554/eLife.80808

Share this article

https://doi.org/10.7554/eLife.80808

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