Surface remodeling and inversion of cell-matrix interactions underlie community recognition and dispersal in Vibrio cholerae biofilms

A Alexis Moreau (CNRS, Centre Interdisciplinaire de Nanoscience de Marseille, Turing Centre for Living Systems, Aix Marseille Université) D Danh T. Nguyen A Alexander J. Hinbest (Department of Molecular Biology and Biochemistry, Molecular Biophysics Program, Wesleyan University) A Anthony Zamora R Ranjuna Weerasekera K Katherine Matej X Xuening Zhou (Department of Molecular Biosciences, The University of Texas at Austin) S Sandra Sanchez I Ignacio Rodriguez Brenes J Jung-Shen Benny Tai C Carey D. Nadell (Department of Biological Sciences, Dartmouth) W Wai-Leung Ng V Vernita Gordon (Interdisciplinary Life Sciences Graduate Programs, The University of Texas at Austin) N Natalia L. Komarova R Rich Olson (Department of Molecular Biology and Biochemistry, Molecular Biophysics Program, Wesleyan University) Y Ying Li J Jing Yan

Abstract

Abstract Biofilms are ubiquitous surface-associated bacterial communities embedded in an extracellular matrix. It is commonly assumed that biofilm cells are glued together by the matrix; however, how the specific biochemistry of matrix components affects the cell-matrix interactions and how these interactions vary during biofilm growth remain unclear. Here, we investigate cell-matrix interactions in Vibrio cholerae, the causative agent of cholera. We combine genetics, microscopy, simulations, and biochemical analyses to show that V. cholerae cells are not attracted to the main matrix component (Vibrio polysaccharide, VPS), but can be attached to each other and to the VPS network through surface-associated VPS and crosslinks formed by the protein Bap1. Downregulation of VPS production and surface trimming by the polysaccharide lyase RbmB cause surface remodeling as biofilms age, shifting the nature of cell-matrix interactions from attractive to repulsive and facilitating cell dispersal as aggregated groups. Our results shed light on the dynamics of diverse cell-matrix interactions as drivers of biofilm development.

Article Details

Volume / Issue Vol. 16, Issue 1
Published January 02, 2025
ISSN 2041-1723
Publisher Nature Portfolio

Journal Info

Nature Communications

Nature Portfolio

ISSN: 2041-1723 Open Access Life Sciences

Authors (17)

A

Alexis Moreau

CNRS, Centre Interdisciplinaire de Nanoscience de Marseille, Turing Centre for Living Systems, Aix Marseille Université

D

Danh T. Nguyen

A

Alexander J. Hinbest

Department of Molecular Biology and Biochemistry, Molecular Biophysics Program, Wesleyan University

A

Anthony Zamora

R

Ranjuna Weerasekera

K

Katherine Matej

X

Xuening Zhou

Department of Molecular Biosciences, The University of Texas at Austin

S

Sandra Sanchez

I

Ignacio Rodriguez Brenes

J

Jung-Shen Benny Tai

C

Carey D. Nadell

Department of Biological Sciences, Dartmouth

W

Wai-Leung Ng

V

Vernita Gordon

Interdisciplinary Life Sciences Graduate Programs, The University of Texas at Austin

N

Natalia L. Komarova

R

Rich Olson

Department of Molecular Biology and Biochemistry, Molecular Biophysics Program, Wesleyan University

Y

Ying Li

J

Jing Yan