Quorum sensing protects bacterial co-operation from exploitation by cheats

Abstract

Quorum sensing (QS) is a cell–cell communication system found in many bacterial species, commonly controlling secreted co-operative traits, including extracellular digestive enzymes. We show that the canonical QS regulatory architecture allows bacteria to sense the genotypic composition of high-density populations, and limit co-operative investments to social environments enriched for co-operators. Using high-density populations of the opportunistic pathogen Pseudomonas aeruginosa we map per-capita signal and co-operative enzyme investment in the wild type as a function of the frequency of non-responder cheats. We demonstrate mathematically and experimentally that the observed response rule of ‘co-operate when surrounded by co-operators' allows bacteria to match their investment in co-operation to the composition of the group, therefore allowing the maintenance of co-operation at lower levels of population structuring (that is, lower relatedness). Similar behavioural responses have been described in vertebrates under the banner of ‘generalised reciprocity'. Our results suggest that mechanisms of reciprocity are not confined to taxa with advanced cognition, and can be implemented at the cellular level via positive feedback circuits.

Bacterial Quorum Sensing Stabilizes Cooperation by Optimizing Growth Strategies

“…The delay observed in activating cooperation by QS regulation in the WT strain is consistent with proposed forms of restraint such as metabolic prudence and generalized reciprocity, in which investment in the expression of cooperative traits is tuned to be more economical for the producing organism (18,33,63). In our case, the cost is lowered for the WT strain during early growth, when signal density is too low to induce QS.…”

“…Although it has recently been shown that QS can serve to modulate investment in cooperative goods, our study demonstrates that QS allows cooperators to match the fitness of defectors even in well-mixed environments, in the absence of any apparent spatial structure or policing by cooperators (33). More specifically, while previous studies suggested the value of functional QS in comparison to a modeled or simulated constitutive producer (33,37), this is the first study to explicitly and definitively show by experimental analysis the vastness of the difference between QS producers and UC producers.…”

“…More specifically, while previous studies suggested the value of functional QS in comparison to a modeled or simulated constitutive producer (33,37), this is the first study to explicitly and definitively show by experimental analysis the vastness of the difference between QS producers and UC producers. Moreover, comparing QS Pseudomonas aeruginosa and a simulated constitutive cooperator, Allen et al concluded that there are environments in which all forms of cooperation are disfavored (33). However, our experimental results demonstrate this is not the case in V. harveyi.…”

“…QS has been proposed as a mechanism to stabilize cooperation, but only modest experimental evidence exists to support this proposition (4,16,(33)(34)(35)(36). Because nonproducing defectors do not pay the cost to produce PG but can still reap the resulting benefits, a fundamental question is how QS systems, and the cooperative behaviors they regulate, are stably maintained in bacterial populations.…”

The path to re-evolve cooperation is constrained in Pseudomonas aeruginosa

“…only expressed at high cell density). This could mean that rare co-operators cannot invade because they do not reach the quorum, and thus no public good is produced and no benefit generated [39,40]. Important to note here is, that while we focussed on the re-evolution of cooperation via mutations, an alternative scenario under natural conditions is that cheats may revert to cooperators through horizontal gene transfer [41,42].…”