Mechanical instability and interfacial energy drive biofilm morphogenesis
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.
Data availability
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
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.
Reviewing Editor
- Michael T Laub, Massachusetts Institute of Technology, United States
Version history
- Received: November 26, 2018
- Accepted: March 6, 2019
- Accepted Manuscript published: March 8, 2019 (version 1)
- Version of Record published: April 8, 2019 (version 2)
Copyright
© 2019, Yan 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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