Social evolution underlies the divergence of bacterial communication

Microbial communication by ‘quorum sensing’ (QS) systems, where microbes produce and respond to a signaling molecule, enable cells to sense their local density and coordinate a cooperative response to their environment. Many QS systems show intraspecific divergence in terms of specificity, where a signaling molecule from one strain activates its cognate receptor but fails to activate those of other strains in the same species. It is unclear how can a signaling molecule and its receptor co-evolve and what evolutionary forces maintain this divergence. In this lecture I will present a mathematical model and experimental results that explain how such divergence can occur based on social grounds. Briefly, if QS regulates the secretion of public goods, which benefit the community at a cost to the producer, then divergent QS receptor mutants will invade their ancestral population by exploitation, but will subsequently be invaded by a fully divergent signal-receptor mutant through social manipulation. Experimentally, we utilized both natural and synthetic QS-dependent social traits to establish a social selection system in the QS-divergent model bacterium Bacillus subtilis. Using competition assays we find that the predicted scheme of divergence is verified in both well mixed and structured environments. These results demonstrate the complexity of social interactions and their evolutionary outcomes in the simplest organisms.