A quorum-sensing system in the free-living photosynthetic bacterium Rhodobacter sphaeroides

Abstract

Rhodobacter sphaeroides is a free-living, photoheterotrophic bacterium known for its genomic and metabolic complexity. We have discovered that this purple photosynthetic organism possesses a quorum-sensing system. Quorum sensing occurs in a number of eukaryotic host-associated gram-negative bacteria. In these bacteria there are two genes required for quorum sensing, the luxR and luxI homologs, and there is an acylhomoserine lactone signal molecule synthesized by the product of the luxI homolog. In R. sphaeroides, synthesis of a novel homoserine lactone signal, 7,8-cis-N-(tetradecenoyl)homoserine lactone, is directed by a luxI homolog termed cerI. Two open reading frames immediately upstream of cerI are proposed to be components of the quorumsensing system. The first of these is a luxR homolog termed cerR, and the second is a small open reading frame of 159 bp. Inactivation of cerI in R. sphaeroides results in mucoid colony formation on agar and formation of large aggregates of cells in liquid cultures. Clumping of CerI mutants in liquid culture is reversible upon addition of the acylhomoserine lactone signal and represents a phenotype unlike those controlled by quorum sensing in other bacteria.Rhodobacter sphaeroides 2.4.1 is a free-living, photoheterotrophic member of the ␣-3 subdivision of the Proteobacteria and has been widely studied due to its remarkable genomic and physiologic complexity. It has a unique genome architecture, possessing both a large (chromosome I, 3.0 Mbp) and a smaller (chromosome II, 0.9 Mbp) circular chromosome (42, 43) in addition to five other endogenous replicons (15). It can grow aerobically as a chemoheterotroph, and it can grow anaerobically by using photosynthetic electron transport (8, 24) or anaerobic respiration (13).We report that R. sphaeroides produces an acylhomoserine lactone. N-Acylhomoserine lactones (commonly called autoinducers) are produced by many gram-negative bacteria and serve as intercellular signals that facilitate a phenomenon termed quorum sensing (17,18,34,40). Quorum sensing allows a bacterial species to monitor its population density and activate specific sets of genes at sufficiently high cell numbers. Regulation of luminescence in Vibrio fischeri was the first reported example of N-acylhomoserine lactone-mediated quorum sensing (9, 25) and continues to serve as a model system (17, 18). In V. fischeri, the luxI gene encodes an autoinducer synthase that catalyzes the production of N-(3-oxohexanoyl) homoserine lactone (9). The luxR gene encodes a transcriptional regulator that activates expression of the luminescence genes in the presence of a sufficient concentration of N-(3-oxohexanoyl)homoserine lactone (11).This type of regulation is involved in the expression of genes encoding extracellular virulence factors in Pseudomonas aeruginosa (27,28), conjugal transfer in Agrobacterium tumefaciens (16,30,46), and antibiotic synthesis and extracellular enzyme and exopolysaccharide production in Erwinia species (2, 31) to name a few. In these quorum-sensing system...

Biofilm dispersal inXanthomonas campestrisis controlled by cell–cell signaling and is required for full virulence to plants

“…Disruption of a hierarchical quorum-sensing system in Y. pseudotuberculosis by mutation of ypsR leads to the formation of clumps in liquid media (24). In R. sphaeroides, mutation of cerI, which directs synthesis of N- (7,8-cis-tetradecenoyl)-HSL, leads to the formation of large aggregates of bacteria in liquid culture (25). This aggregated phenotype in R. sphaeroides can be reversed by addition of the N-AHL signaling molecule.…”

“…Cell-cell signaling mediated by diffusible molecules is known to play a large role in regulating diverse physiological processes, including the formation and dispersal of biofilms, across distant genera of bacteria. Quorum sensing mediated by N-acylhomoserine lactones (N-AHLs) has been implicated in the regulation of biofilm formation or aggregation in a number of bacteria (21)(22)(23)(24)(25)(26), although it appears to have divergent regulatory roles in different bacteria. In Pseudomonas aeruginosa, N-(3-oxododecanoyl)- .…”

Heteroorganic molecules and bacterial biofilms: Controlling biodeterioration of cultural heritage

“…Lee, Li and Bowden 111 showed that a surface protein releasing enzyme mediates the release of cells from S. mutans biofilms, while Boyd and Chakrabarty 112 showed that degradation of the exopolysaccharide alginate in P. aeruginosa through the over expression of alginate lyase induces increased detachment. Cell-signalling through the release of autoinducers has also been found to be negatively correlated with cell aggregation, 113 the reduction of biofilm biomass and a loss of EPS. 107 In order to detach efficiently, the morphology of the cells must also change.…”

Quorum Sensing within the Gut Ecosystem

“…Linked with colonisation is the dispersal of bacteria from colonized areas. A role for quorum sensing in the induction of motility through liquids or along surfaces has now been shown in a number of organisms (88)(89)(90)(91). In considering a role for quorum sensing in colonisation it is important to emphasize that the gut is not a sterile environment, it is already colonized and so in many respects is different to a laboratory monoculture or an initially sterile site of infection.…”