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Flow-induced symmetry breaking in growing bacterial biofilms

View ORCID ProfilePhilip Pearce, Boya Song, Dominic J. Skinner, Rachel Mok, Raimo Hartmann, Praveen K. Singh, Hannah Jeckel, Jeffrey S. Oishi, View ORCID ProfileKnut Drescher, View ORCID ProfileJörn Dunkel
doi: https://doi.org/10.1101/627208
Philip Pearce
1Department of Mathematics, Massachusetts Institute of Technology, Cambridge MA 02139-4307, USA
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  • For correspondence: ppearce@mit.edu
Boya Song
1Department of Mathematics, Massachusetts Institute of Technology, Cambridge MA 02139-4307, USA
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Dominic J. Skinner
1Department of Mathematics, Massachusetts Institute of Technology, Cambridge MA 02139-4307, USA
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Rachel Mok
1Department of Mathematics, Massachusetts Institute of Technology, Cambridge MA 02139-4307, USA
2Department of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139-4307, USA
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Raimo Hartmann
3Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, Germany
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Praveen K. Singh
3Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, Germany
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Hannah Jeckel
3Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, Germany
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Jeffrey S. Oishi
1Department of Mathematics, Massachusetts Institute of Technology, Cambridge MA 02139-4307, USA
4Department of Physics, Bates College, Lewiston, ME 04240, USA
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Knut Drescher
3Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, Germany
5Department of Physics, Philipps-Universität Marburg, 35043 Marburg, Germany
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Jörn Dunkel
1Department of Mathematics, Massachusetts Institute of Technology, Cambridge MA 02139-4307, USA
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Abstract

Bacterial biofilms represent a major form of microbial life on Earth and serve as a model active nematic system, in which activity results from growth of the rod-shaped bacterial cells. In their natural environments, ranging from human organs to industrial pipelines, biofilms have evolved to grow robustly under significant fluid shear. Despite intense practical and theoretical interest, it is unclear how strong fluid flow alters the local and global architectures of biofilms. Here, we combine highly time-resolved single-cell live imaging with 3D multi-scale modeling to investigate the mechanisms by which flow affects the dynamics of all individual cells in growing biofilms. Our experiments and cell-based simulations reveal three quantitatively different growth phases in strong external flow, and the transitions between them. In the initial stages of biofilm development, flow induces a downstream gradient in cell orientation, causing asymmetrical droplet-like biofilm shapes. In the later developmental stages, when the majority of cells are sheltered from the flow by the surrounding extracellular matrix, buckling-induced cell verticalization in the biofilm core restores radially symmetric biofilm growth, in agreement with predictions of a 3D continuum model.

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Posted August 15, 2019.
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Flow-induced symmetry breaking in growing bacterial biofilms
Philip Pearce, Boya Song, Dominic J. Skinner, Rachel Mok, Raimo Hartmann, Praveen K. Singh, Hannah Jeckel, Jeffrey S. Oishi, Knut Drescher, Jörn Dunkel
bioRxiv 627208; doi: https://doi.org/10.1101/627208
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Flow-induced symmetry breaking in growing bacterial biofilms
Philip Pearce, Boya Song, Dominic J. Skinner, Rachel Mok, Raimo Hartmann, Praveen K. Singh, Hannah Jeckel, Jeffrey S. Oishi, Knut Drescher, Jörn Dunkel
bioRxiv 627208; doi: https://doi.org/10.1101/627208

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