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

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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.

Data availability

All data generated or analyzed during this study are available on Dryad

The following data sets were generated

1. Berne C
2. Zappa S
3. Brun Y
(2022) Data from: eDNA-stimulated cell dispersion from Caulobacter crescentus biofilms upon oxygen limitation is dependent on a toxin-antitoxin system
Dryad Digital Repository, doi:10.5061/dryad.4j0zpc8fc.

https://dx.doi.org/10.5061/dryad.4j0zpc8fc

Article and author information

Author details

Cecile Berne

Département de Microbiologie, Infectiologie et Immunologie, University of Montreal, Montreal, Canada

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-3731-9317
Sebastien Zappa

Département de Microbiologie, Infectiologie et Immunologie, University of Montreal, Montreal, Canada

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-3190-9199
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.

"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.

Copyright

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.