Mechanical instability and interfacial energy drive biofilm morphogenesis

Jing Yan; Chenyi Fei; Sheng Mao; Alexis Moreau; Ned S. Wingreen; Andrej Kosmrlj; Howard A. Stone; Bonnie Lynn Bassler

doi:10.7554/eLife.43920

Mechanical instability and interfacial energy drive biofilm morphogenesis

Jing Yan, Chenyi Fei, Sheng Mao, Alexis Moreau, Ned S. Wingreen, Andrej Kosmrlj, Howard A. Stone, Bonnie Lynn Bassler

Princeton University

Research output: Contribution to journal › Article › peer-review

15 Scopus citations

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 of new and the annihilation of existing interfaces. Finally, we discover feedback between mechanomorphogenesis and biofilm expansion, which shapes the overall biofilm contour. The morphogenesis principles that we discover in bacterial biofilms, which rely on mechanical instabilities and interfacial energies, should be generally applicable to morphogenesis processes in tissues in higher organisms.

Original language	American English
Article number	e43920
Journal	eLife
Volume	8
DOIs	https://doi.org/10.7554/eLife.43920
State	Published - Mar 2019

ASJC Scopus subject areas

General Immunology and Microbiology
General Biochemistry, Genetics and Molecular Biology
General Neuroscience

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10.7554/eLife.43920

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title = "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 of new and the annihilation of existing interfaces. Finally, we discover feedback between mechanomorphogenesis and biofilm expansion, which shapes the overall biofilm contour. The morphogenesis principles that we discover in bacterial biofilms, which rely on mechanical instabilities and interfacial energies, should be generally applicable to morphogenesis processes in tissues in higher organisms.",

author = "Jing Yan and Chenyi Fei and Sheng Mao and Alexis Moreau and Wingreen, {Ned S.} and Andrej Kosmrlj and Stone, {Howard A.} and Bassler, {Bonnie Lynn}",

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T1 - Mechanical instability and interfacial energy drive biofilm morphogenesis

AU - Yan, Jing

AU - Fei, Chenyi

AU - Mao, Sheng

AU - Moreau, Alexis

AU - Wingreen, Ned S.

AU - Kosmrlj, Andrej

AU - Stone, Howard A.

AU - Bassler, Bonnie Lynn

PY - 2019/3

Y1 - 2019/3

N2 - 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 of new and the annihilation of existing interfaces. Finally, we discover feedback between mechanomorphogenesis and biofilm expansion, which shapes the overall biofilm contour. The morphogenesis principles that we discover in bacterial biofilms, which rely on mechanical instabilities and interfacial energies, should be generally applicable to morphogenesis processes in tissues in higher organisms.

AB - 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 of new and the annihilation of existing interfaces. Finally, we discover feedback between mechanomorphogenesis and biofilm expansion, which shapes the overall biofilm contour. The morphogenesis principles that we discover in bacterial biofilms, which rely on mechanical instabilities and interfacial energies, should be generally applicable to morphogenesis processes in tissues in higher organisms.

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Mechanical instability and interfacial energy drive biofilm morphogenesis

Abstract

ASJC Scopus subject areas

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