Cheating on Cheaters Stabilizes Cooperation in Pseudomonas aeruginosa

Abstract

Bacterial cooperation can be disrupted by non-producers that can profit from public goods without paying their production cost. A cheater can increase in frequency, exhausting the public good and causing a population collapse. Here, we investigate how interactions among two cheaters for distinct social traits influence the short- and long-term dynamics of polymorphic populations. Using as a model Pseudomonas aeruginosa and its extensively studied social traits, production of the siderophore pyoverdine, and the quorum-sensing regulated elastase, we analyzed the social dynamics of polymorphic populations under conditions where the two traits are required for optimal growth. We show that cheaters for either trait compete with both the wild-type and each other and that mutants for pyoverdine production can prevent a drastic population collapse caused by quorum-sensing cheaters. A simple mathematical model suggests that the observed social dynamics are determined by the ratio of the costs of each social trait, such that the mutant, which avoids paying the highest cost, dominates the population; in contrast, mean fitness of the population is determined by the difference between the benefits and the costs of the social traits. Finally, we demonstrate how quorum-sensing regulation can avoid the full loss of cooperation.