Microbial Communication, Cooperation and Cheating: Quorum Sensing Drives the Evolution of Cooperation in Bacteria

Tamás Czárán,Rolf F Hoekstra

doi:10.1371/journal.pone.0006655

Abstract

An increasing body of empirical evidence suggests that cooperation among clone-mates is common in bacteria. Bacterial cooperation may take the form of the excretion of “public goods”: exoproducts such as virulence factors, exoenzymes or components of the matrix in biofilms, to yield significant benefit for individuals joining in the common effort of producing them. Supposedly in order to spare unnecessary costs when the population is too sparse to supply the sufficient exoproduct level, many bacteria have evolved a simple chemical communication system called quorum sensing (QS), to “measure” the population density of clone-mates in their close neighborhood. Cooperation genes are expressed only above a threshold rate of QS signal molecule re-capture, i.e., above the local quorum of cooperators. The cooperative population is exposed to exploitation by cheaters, i.e., mutants who contribute less or nil to the effort but fully enjoy the benefits of cooperation. The communication system is also vulnerable to a different type of cheaters (“Liars”) who may produce the QS signal but not the exoproduct, thus ruining the reliability of the signal. Since there is no reason to assume that such cheaters cannot evolve and invade the populations of honestly signaling cooperators, the empirical fact of the existence of both bacterial cooperation and the associated QS communication system seems puzzling. Using a stochastic cellular automaton approach and allowing mutations in an initially non-cooperating, non-communicating strain we show that both cooperation and the associated communication system can evolve, spread and remain persistent. The QS genes help cooperative behavior to invade the population, and vice versa; cooperation and communication might have evolved synergistically in bacteria. Moreover, in good agreement with the empirical data recently available, this synergism opens up a remarkably rich repertoire of social interactions in which cheating and exploitation are commonplace.

Highlights

Cooperation – behavior that benefits other individuals – is not easy to explain from an evolutionary perspective, because of its potential vulnerability to selfish cheating
With a low quorum threshold there is much scope for non-cooperators to parasitize, because sufficiently often they can enjoy the benefit from cooperative neighbors without paying the cost of cooperation themselves; with nq = 2 and nq = 3, only a minority of the population will consist of cooperator genotypes
Cooperation often takes the form of a coordinated production and excretion of molecules like enzymes, toxins and virulence factors. This cooperative behavior is typically regulated by quorum sensing (QS), a chemical communication system in which cells produce diffusible molecules and can assess the cell density by sensing the local concentration of these signaling molecules [11,12,22,23]

Summary

Introduction

Cooperation – behavior that benefits other individuals – is not easy to explain from an evolutionary perspective, because of its potential vulnerability to selfish cheating. A commons pasture is used by many herders, and the best strategy for an individual herder is to add as many cattle as possible, even if this eventually causes degradation of the pasture. The unfortunate outcome follows from the fact that the division of the costs and benefits of adding additional animals is unequal: the individual herder gains all of the advantage, but the disadvantage is shared among all herders using the pasture. Cooperation (involving restraint in the input of animals) among the herders would yield the highest benefit for them as a group, each individual herder will be tempted to cheat by adding additional animals, causing the cooperation to break down. By helping a close relative reproduce, an individual is indirectly passing copies of its genes on to the generation

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Conclusion