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Vibrio cholerae biofilm dispersal regulator causes cell release from matrix through type IV pilus retraction

View ORCID ProfilePraveen K. Singh, View ORCID ProfileDaniel K.H. Rode, View ORCID ProfilePauline Buffard, View ORCID ProfileKazuki Nosho, View ORCID ProfileMiriam Bayer, View ORCID ProfileHannah Jeckel, View ORCID ProfileEric Jelli, View ORCID ProfileKonstantin Neuhaus, View ORCID ProfileEva Jiménez-Siebert, View ORCID ProfileNikolai Peschek, View ORCID ProfileTimo Glatter, View ORCID ProfileKai Papenfort, View ORCID ProfileKnut Drescher
doi: https://doi.org/10.1101/2021.05.02.442311
Praveen K. Singh
1Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Str. 16, 35043 Marburg, Germany
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  • ORCID record for Praveen K. Singh
Daniel K.H. Rode
1Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Str. 16, 35043 Marburg, Germany
2Department of Physics, Philipps-Universität Marburg, Karl-von-Frisch-Str. 16, 35043 Marburg, Germany
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Pauline Buffard
1Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Str. 16, 35043 Marburg, Germany
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Kazuki Nosho
1Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Str. 16, 35043 Marburg, Germany
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Miriam Bayer
1Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Str. 16, 35043 Marburg, Germany
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Hannah Jeckel
1Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Str. 16, 35043 Marburg, Germany
2Department of Physics, Philipps-Universität Marburg, Karl-von-Frisch-Str. 16, 35043 Marburg, Germany
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Eric Jelli
1Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Str. 16, 35043 Marburg, Germany
2Department of Physics, Philipps-Universität Marburg, Karl-von-Frisch-Str. 16, 35043 Marburg, Germany
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Konstantin Neuhaus
1Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Str. 16, 35043 Marburg, Germany
2Department of Physics, Philipps-Universität Marburg, Karl-von-Frisch-Str. 16, 35043 Marburg, Germany
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Eva Jiménez-Siebert
1Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Str. 16, 35043 Marburg, Germany
2Department of Physics, Philipps-Universität Marburg, Karl-von-Frisch-Str. 16, 35043 Marburg, Germany
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Nikolai Peschek
3Institute of Microbiology, Friedrich Schiller University, 07745 Jena, Germany
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Timo Glatter
1Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Str. 16, 35043 Marburg, Germany
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Kai Papenfort
3Institute of Microbiology, Friedrich Schiller University, 07745 Jena, Germany
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Knut Drescher
1Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Str. 16, 35043 Marburg, Germany
2Department of Physics, Philipps-Universität Marburg, Karl-von-Frisch-Str. 16, 35043 Marburg, Germany
4Biozentrum, University of Basel, Spitalstrasse 41, 4056 Basel, Switzerland
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  • For correspondence: knut.drescher@unibas.ch
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Abstract

The extracellular matrix is a defining feature of bacterial biofilms and provides structural stability to the community by binding cells to the surface and to each other. Transitions between bacterial biofilm initiation, growth, and dispersion require different regulatory programs, all of which result in modifications to the extracellular matrix composition, abundance, or functionality. However, the mechanisms by which individual cells in biofilms disengage from the matrix to enable their departure during biofilm dispersal are unclear. Here, we investigated active biofilm dispersal of Vibrio cholerae during nutrient starvation, resulting in the discovery of the conserved Vibrio biofilm dispersal regulator VbdR. We show that VbdR triggers biofilm dispersal by controlling cellular release from the biofilm matrix, which is achieved by inducing the retraction of the mannose-sensitive hemagglutinin (MSHA) type IV pili and the expression of a matrix protease IvaP. We further show that MSHA pili have numerous binding partners in the matrix and that the joint effect of MSHA pilus retraction and IvaP activity is necessary and sufficient for causing biofilm dispersal. These results highlight the crucial role of type IV pilus dynamics during biofilm dispersal and provide a new target for controlling V. cholerae biofilm abundance through the induction and manipulation of biofilm dispersal.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted May 02, 2021.
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Vibrio cholerae biofilm dispersal regulator causes cell release from matrix through type IV pilus retraction
Praveen K. Singh, Daniel K.H. Rode, Pauline Buffard, Kazuki Nosho, Miriam Bayer, Hannah Jeckel, Eric Jelli, Konstantin Neuhaus, Eva Jiménez-Siebert, Nikolai Peschek, Timo Glatter, Kai Papenfort, Knut Drescher
bioRxiv 2021.05.02.442311; doi: https://doi.org/10.1101/2021.05.02.442311
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Vibrio cholerae biofilm dispersal regulator causes cell release from matrix through type IV pilus retraction
Praveen K. Singh, Daniel K.H. Rode, Pauline Buffard, Kazuki Nosho, Miriam Bayer, Hannah Jeckel, Eric Jelli, Konstantin Neuhaus, Eva Jiménez-Siebert, Nikolai Peschek, Timo Glatter, Kai Papenfort, Knut Drescher
bioRxiv 2021.05.02.442311; doi: https://doi.org/10.1101/2021.05.02.442311

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