Surface remodeling and inversion of cell-matrix interaction underlies community recognition and dispersal in biofilms

Biofilms are ubiquitous surface-associated bacterial communities embedded in an extracellular matrix. While it is commonly assumed that biofilm-dwelling cells are glued together by the matrix, this simplistic view fails to explain many observations, including the ability of biofilms to exclude other species and non-matrix-producing clonemates and the swift dispersion to a planktonic state upon starvation. Here, we investigated cell-matrix interactions in Vibrio cholerae (Vc), the causative agent of cholera. We combine genetics, microscopy, simulation, and biochemical tools to show that native Vc cell surfaces are repulsive to Vibrio polysaccharide (VPS), the main matrix component, leading to spontaneous depletion-aggregation during growth. Downregulation of VPS and surface trimming by a polysaccharide lyase cause surface remodeling as biofilms age, shifting the nature of cell-matrix interactions from attractive to repulsive and facilitating cell dispersal as aggregated groups. We experimentally show that this concept may generalize to certain other biofilm-forming species and exopolysaccharides. Our results suggest a new conceptual model in understanding the intricate cell-matrix interaction as the major driver for biofilm development and a potential drug target.