Quorum sensing and social networking in the microbial world

Abstract

For many years, bacterial cells were considered primarily as selfish individuals, but, in recent years, it has become evident that, far from operating in isolation, they coordinate collective behaviour in response to environmental challenges using sophisticated intercellular communication networks. Cell-to-cell communication between bacteria is mediated by small diffusible signal molecules that trigger changes in gene expression in response to fluctuations in population density. This process, generally referred to as quorum sensing (QS), controls diverse phenotypes in numerous Gram-positive and Gram-negative bacteria. Recent advances have revealed that bacteria are not limited to communication within their own species but are capable of 'listening in' and 'broadcasting to' unrelated species to intercept messages and coerce cohabitants into behavioural modifications, either for the good of the population or for the benefit of one species over another. It is also evident that QS is not limited to the bacterial kingdom. The study of two-way intercellular signalling networks between bacteria and both uni- and multicellular eukaryotes as well as between eukaryotes is just beginning to unveil a rich diversity of communication pathways.

Figure 1.

The structures of some common QS signal molecules.

Figure 2.

The autoregulated QS circuits of Y. pseudotuberculosis, capable of producing up to eight AHLs at physiological concentrations, control flagella-mediated motility by regulating the expression of the motility master regulator flhDC and the alternative sigma factor fliA (adapted from Atkinson et al. 2008).

Figure 3.

Xanthomonas campestris DSF autoinduction. RpfC inhibits the activity of the DSF synthase RpfF at low cell density. As the cell density increases and basal DSF production allows for signal accumulation, an RpfC conformational change mediated by DSF promotes the release of RpfF to synthesize more DSF and also to initiate phosphorelay from RpfC to RpfG, which will trigger the expression of target genes in the DSF regulon (adapted from He & Zhang 2008).

Figure 4.

QS in V. cholerae. Two QS signals AI-2 and CAI-1 work synergistically to regulate virulence factor expression and biofilm development. At low population density in the absence of signal molecules, the absence of HapR triggers the expression of genes such as vps, ctx and tcp, which are normally repressed by HapR. As the cell density and therefore the signal molecule concentration increases HapR represses the expression of the genes responsible for colonization and promotes detachment from the intestinal epithelium to enable the organism to exit the host (adapted from Kaper & Sperandio 2005).

Figure 5.

AIP-mediated QS in S. aureus. (a) The AIP activates the transmembrane receptor histidine kinase AgrC to trigger autophosphorylation and phosphotransfer to AgrA, which in turn drives the transcription of the agrP2 and agrP3 promoters. This triggers rightward and leftward transcription of the agr locus and RNAIII-dependent and -independent genes. (b)(i) Structures of AIP-1 and (ii) the linear sequences of the four S. aureus AIPs which constitute four different agr specificity groups.