Social evolution of shared biofilm matrix components

Biofilm formation is an important and ubiquitous mode of growth among
bacteria. Central to the evolutionary advantage of biofilm formation is
cell-cell and cell-surface adhesion achieved by a variety of factors, some
of which are diffusible compounds that may operate as classical public
goods – factors that are costly to produce but may benefit other cells. An
outstanding question is how diffusible matrix production, in general, can
be stable over evolutionary timescales. In this work, using Vibrio
cholerae as a model, we show that shared diffusible biofilm matrix
proteins are indeed susceptible to cheater exploitation, and that the
evolutionary stability of producing these matrix components fundamentally
depends on biofilm spatial structure, intrinsic sharing mechanisms of
these components, and flow conditions in the environment. We further show
that exploitation of diffusible adhesion proteins is localized within a
well-defined spatial range around cell clusters that produce them. Based
on this exploitation range and the spatial distribution of cell clusters,
we construct a model of costly diffusible matrix production and relate
these length scales to the relatedness coefficient in social evolution
theory. Our results show that production of diffusible biofilm matrix
components is evolutionarily stable under conditions consistent with
natural biofilm habitats and host environments. We expect the mechanisms
revealed in this study to be relevant to other secreted factors that
operate as cooperative public goods in bacterial communities, and the
concept of exploitation range and the associated analysis tools to be
generally applicable.