Mechanical instability and interfacial energy drive biofilm morphogenesis
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...
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eLife Sciences Publications Ltd
2019-03-01
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| Online Access: | https://elifesciences.org/articles/43920 |
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doaj-9366cb6a76c54ceab589bd6c5d0b97832021-05-05T17:27:39ZengeLife Sciences Publications LtdeLife2050-084X2019-03-01810.7554/eLife.43920Mechanical instability and interfacial energy drive biofilm morphogenesisJing Yan0https://orcid.org/0000-0003-2773-0348Chenyi Fei1https://orcid.org/0000-0002-8287-4347Sheng Mao2https://orcid.org/0000-0001-9468-5095Alexis Moreau3Ned S Wingreen4https://orcid.org/0000-0001-7384-2821Andrej Košmrlj5https://orcid.org/0000-0001-6137-9200Howard A Stone6https://orcid.org/0000-0002-9670-0639Bonnie L Bassler7https://orcid.org/0000-0002-0043-746XDepartment of Mechanical and Aerospace Engineering, Princeton University, Princeton, United States; Department of Molecular Biology, Princeton University, Princeton, United StatesDepartment of Molecular Biology, Princeton University, Princeton, United StatesDepartment of Mechanical and Aerospace Engineering, Princeton University, Princeton, United StatesDepartment of Mechanical and Aerospace Engineering, Princeton University, Princeton, United StatesDepartment of Molecular Biology, Princeton University, Princeton, United StatesDepartment of Mechanical and Aerospace Engineering, Princeton University, Princeton, United StatesDepartment of Mechanical and Aerospace Engineering, Princeton University, Princeton, United StatesDepartment of Molecular Biology, Princeton University, Princeton, United States; The Howard Hughes Medical Institute, Chevy Chase, United StatesSurface-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.https://elifesciences.org/articles/43920biofilmsmechanobiologyV. choleraemorphogenesisbiomaterialdevelopment |
| collection |
DOAJ |
| language |
English |
| format |
Article |
| sources |
DOAJ |
| author |
Jing Yan Chenyi Fei Sheng Mao Alexis Moreau Ned S Wingreen Andrej Košmrlj Howard A Stone Bonnie L Bassler |
| spellingShingle |
Jing Yan Chenyi Fei Sheng Mao Alexis Moreau Ned S Wingreen Andrej Košmrlj Howard A Stone Bonnie L Bassler Mechanical instability and interfacial energy drive biofilm morphogenesis eLife biofilms mechanobiology V. cholerae morphogenesis biomaterial development |
| author_facet |
Jing Yan Chenyi Fei Sheng Mao Alexis Moreau Ned S Wingreen Andrej Košmrlj Howard A Stone Bonnie L Bassler |
| author_sort |
Jing Yan |
| title |
Mechanical instability and interfacial energy drive biofilm morphogenesis |
| title_short |
Mechanical instability and interfacial energy drive biofilm morphogenesis |
| title_full |
Mechanical instability and interfacial energy drive biofilm morphogenesis |
| title_fullStr |
Mechanical instability and interfacial energy drive biofilm morphogenesis |
| title_full_unstemmed |
Mechanical instability and interfacial energy drive biofilm morphogenesis |
| title_sort |
mechanical instability and interfacial energy drive biofilm morphogenesis |
| publisher |
eLife Sciences Publications Ltd |
| series |
eLife |
| issn |
2050-084X |
| publishDate |
2019-03-01 |
| description |
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. |
| topic |
biofilms mechanobiology V. cholerae morphogenesis biomaterial development |
| url |
https://elifesciences.org/articles/43920 |
| work_keys_str_mv |
AT jingyan mechanicalinstabilityandinterfacialenergydrivebiofilmmorphogenesis AT chenyifei mechanicalinstabilityandinterfacialenergydrivebiofilmmorphogenesis AT shengmao mechanicalinstabilityandinterfacialenergydrivebiofilmmorphogenesis AT alexismoreau mechanicalinstabilityandinterfacialenergydrivebiofilmmorphogenesis AT nedswingreen mechanicalinstabilityandinterfacialenergydrivebiofilmmorphogenesis AT andrejkosmrlj mechanicalinstabilityandinterfacialenergydrivebiofilmmorphogenesis AT howardastone mechanicalinstabilityandinterfacialenergydrivebiofilmmorphogenesis AT bonnielbassler mechanicalinstabilityandinterfacialenergydrivebiofilmmorphogenesis |
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