Locality versus globality in bacterial signalling: can local communication stabilize bacterial communities?

BACKGROUND: Microbial consortia are a major form of life; however their stability conditions are poorly understood and are often explained in terms of species-specific defence mechanisms (secretion of extracellular matrix, antimicrobial compounds, siderophores, etc.). Here we propose a hypothesis that the primarily local nature of intercellular signalling can be a general mechanism underlying the stability of many forms of microbial communities. PRESENTATION OF THE HYPOTHESIS: We propose that a large microbial community can be pictured as a theatre of spontaneously emerging, partially overlapping, locally recruited microcommunities whose members interact primarily among themselves, via secreted (signalling) molecules or cell-cell contacts. We hypothesize that stability in an open environment relies on a predominantly local steady state of intercellular communication which ensures that i) deleterious mutants or strains can be excluded by a localized collapse, while ii) microcommunities harbouring useful traits can persist and/or spread even in the absence of specific protection mechanisms. TESTING THE HYPOTHESIS: Some elements of this model can be tested experimentally by analyzing the behaviour of synthetic consortia composed of strains having well-defined communication systems and devoid of specific defence mechanisms. Supporting evidence can be obtained by in silico simulations. IMPLICATIONS OF THE HYPOTHESIS: The hypothesis provides a framework for a systematic comparison of bacterial community behavior in open and closed environments. The model predicts that local signalling may enable multispecies communities to colonize open, structured environments. On the other hand, a confined niche or a host may be more likely to be colonized by a bacterial mono-species community, and local communication here provides a control against spontaneously arising cheaters, provided that survival depends on cooperation. REVIEWERS: This article was reviewed by G. Jékely, L. Aravind and E. Szathmáry (nominated by F. Eisenhaber)