Mechanical instability and interfacial energy drive biofilm morphogenesis

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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.

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All data generated or analyzed during this study are included in the manuscript and supporting files. Source data files have been provided for all figures, tables and SI figures.

Article and author information

Author details

Jing Yan

Department of Mechanical and Aerospace Engineering, Princeton University, Princeton, United States

Competing interests
The authors declare that no competing interests exist.
Chenyi Fei

Department of Molecular Biology, Princeton University, Princeton, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-8287-4347
Sheng Mao

Department of Mechanical and Aerospace Engineering, Princeton University, Princeton, United States

Competing interests
The authors declare that no competing interests exist.
Alexis Moreau

Department of Mechanical and Aerospace Engineering, Princeton University, Princeton, United States

Competing interests
The authors declare that no competing interests exist.
Ned S Wingreen

Department of Molecular Biology, Princeton University, Princeton, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-7384-2821
Andrej Košmrlj

Department of Mechanical and Aerospace Engineering, Princeton University, Princeton, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-6137-9200
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.
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.

"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.

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.