Spatially localized adhesin sharing confers ecological stability in V. cholerae biofilms

Biofilm is an important life form of bacteria. Central to the evolutionary advantage of biofilm formation is the adhesion of biofilm to surfaces, which endows biofilm-dwelling cells with fitness advantages such as access to nutrient sources in their natural habitats and colonization in hosts. Adhesion is achieved by biofilm-specific adhesins secreted into the extracellular space, raising the question of whether the adhesins are exploitable public goods and how sharing and exploitation of adhesins may shape the ecology of biofilms. In this work, using Vibrio cholerae as the model biofilm-former, we show that biofilm adhesins are indeed susceptible to cheater exploitation, and the evolutionary stability of adhesin production depends on the spatial structure of biofilms and the flow conditions in the environment. We further show that exploitation of adhesins is localized within a well-defined spatial range around adhesin producers, which depends critically on the diffusion and advection of adhesin molecules. Based on the exploitation range and the spatial distancing between biofilm clusters, we construct a spatial model of exploitation and relate the Hamilton’s relatedness coefficient to these two length scales. Our results show that adhesin production is favored under conditions consistent with their natural habitats and host environments. Compared to other diffusive public goods in bacterial biofilms, adhesin production presents distinct ecological dynamics. We expect the mechanisms revealed in this study to be relevant to other matrix components as cooperative public goods in biofilm-forming microbes, and the concept of spatial range and the associated analysis tools to be generally applicable to other ecological traits.