Cooperation and Conflict in Quorum-Sensing Populations of Streptococcus mutans

Quorum sensing (QS) is a mechanism in which bacteria communicate with each other by releasing and sensing small diffusible signal molecules, enabling the cells to coordinate their cooperative activities by population-wide adaptive response. However, evolutionary theory predicts that individuals that cooperate can be exploited by so called the ‘cheaters'. Objective: To understand this conflict, we examined the interactions and fitness of QS populations of Streptococcus mutans that has a signaling peptide-mediated quorum-sensing system. Methods: A S. mutans wild type strain and its isogenic mutants that were defective in signal producing (SMdC), signal sensing (SMdD/E) or both (SMdCDE) were examined for their growth rates, yields and QS-dependent bacteriocin production. A growth competitive assay was performed to examine the cooperation and competition between the populations by growing mutant SMdCDE together with the parent. A competitive index analysis was performed to estimate the fitness consequence of QS populations. Results: The QS mutants were defective in the bacteriocin production, and had similar growth rates but the higher growth yields than the parent, suggesting that the QS-dependent cooperation is metabolically costly. In a mixed culture inoculated with 1:50 ratio of SMdCDE to the parent, SMdCDE population slowly increased and reached to 1:10 ratio in the culture, suggesting that the mutant population exploited the benefits from the parent. We then added the culture with S. sanguinis SK108, which had a competitive growth rate but was sensitive to the bacteriocins produced by the S. mutans. We found that all three populations co-existed with a 1:4.5 ratio of the SMdCDE to the parent, confirming that the size of the mutant population continued increasing in the presence of a competitor. Conclusion: This work suggests that social cooperation in the QS populations of S. mutans could be limited by the cost and by invasion of the ‘cheaters' in the community.