Look who's talking: communication and quorum sensing in the bacterial world

Abstract

For many years bacteria were considered primarily as autonomous unicellular organisms with little capacity for collective behaviour. However, we now appreciate that bacterial cells are in fact, highly communicative. The generic term 'quorum sensing' has been adopted to describe the bacterial cell-to-cell communication mechanisms which co-ordinate gene expression usually, but not always, when the population has reached a high cell density. Quorum sensing depends on the synthesis of small molecules (often referred to as pheromones or autoinducers) that diffuse in and out of bacterial cells. As the bacterial population density increases, so does the synthesis of quorum sensing signal molecules, and consequently, their concentration in the external environment rises. Once a critical threshold concentration has been reached, a target sensor kinase or response regulator is activated (or repressed) so facilitating the expression of quorum sensing-dependent genes. Quorum sensing enables a bacterial population to mount a co-operative response that improves access to nutrients or specific environmental niches, promotes collective defence against other competitor prokaryotes or eukaryotic defence mechanisms and facilitates survival through differentiation into morphological forms better able to combat environmental threats. Quorum sensing also crosses the prokaryotic-eukaryotic boundary since quorum sensing-dependent signalling can be exploited or inactivated by both plants and mammals.

Figure 1

Structures of some representative quorum sensing signalling molecules. 3-oxo-AHL, N-(3-oxoacyl)homoserine lactone; 3-hydroxy-AHL, N-(3-hydoxyacyl)homoserine lactone and AHL, N-acylhomoserine lactone where R ranges from C1 to C15. The acyl side chains may also contain one or more double bonds: A-factor, 2-isocapryloyl-3-hydroxymethyl-γ-butyrolactone; AI-2, autoinducer-2, furanosyl borate ester form; PQS, Pseudomonas quinolone signal, 2-heptyl-3-hydroxy-4(1H)-quinolone; DSF, ‘diffusible factor’, methyl dodecenoic acid; PAME, hydroxyl-palmitic acid methyl ester.

Figure 2

Chemical structures of the quorum sensing signal molecules: (a) nisin from L. lactis; (b) (top) autoinducing peptide-1 (AIP-1) from S. aureus and (bottom) schematic structures of characterized staphylococcal AIPs; (c) ComX from B. subtilis RO-E-2; (d) AIP from Lactobacillus plantarum; and (e) 28-membered AIP from E. faecalis.

Figure 3

LuxR/AHL-driven quorum sensing module where LuxR is the AHL receptor and signal transducer and LuxI is the AHL signal synthase. Many bacteria possess multiple LuxR/LuxI/AHL modules.

Figure 4

Integration of the P. aeruginosa AHL and PQS quorum sensing systems with other regulatory elements operating at the transcriptional and post-transcriptional levels to facilitate environmental adaptation at both population and single cell levels.

Figure 5

The activated methyl cycle (AMC) drives the formation of methionine and its subsequent conversion to S-adenosylmethionine (SAM) which is primarily used for the methylation of DNA, RNA, proteins and certain metabolites. Donation of the SAM methyl group leads to formation of the toxic metabolite S-adenosylhomocysteine (SAH). SAH is removed by one of two mechanisms involving either one (SAHh) or two enzymes (Pfs and LuxS) to generate homocysteine and complete the AMC cycle. The Pfs/LuxS pathway also leads to the generation of DPD which spontaneously cyclizes to generate the furanones which constitute AI-2.