Quorum sensing, virulence and secondary metabolite production in plant soft-rotting bacteria

Abstract

Quorum sensing describes the ability of bacteria to sense their population density and respond by modulating gene expression. In the plant soft-rotting bacteria, such as Erwinia, an arsenal of plant cell wall-degrading enzymes is produced in a cell density-dependent manner, which causes maceration of plant tissue. However, quorum sensing is central not only to controlling the production of such destructive enzymes, but also to the control of a number of other virulence determinants and secondary metabolites. Erwinia synthesizes both N-acylhomoserine lactone (AHL) and autoinducer-2 types of quorum sensing signal, which both play a role in regulating gene expression in the phytopathogen. We review the models for AHL-based regulation of carbapenem antibiotic production in Erwinia. We also discuss the importance of quorum sensing in the production and secretion of virulence determinants by Erwinia, and its interplay with other regulatory systems.

Figure 1

The regulation of carbapenem antibiotic production in Erwinia carotovora ssp. carotovora. The organization of the car biosynthetic locus is shown. carA–E encode the Car biosynthetic enzymes and carF–G encode the Car resistance mechanism. The carH product is of unknown function. carA–H are expressed from a single, quorum sensing-dependent promoter located upstream of carA (P_carA). There is also a weak, constitutive promoter located within carD (P_int), which causes expression of carEFGH, and hence primes the Car-resistance mechanism, in the absence of quorum sensing-dependent production of the Car antibiotic. Quorum sensing depends on a diffusible signalling molecule, N-(3-oxohexanoyl)-l-homoserine lactone (3-oxo-C6-HSL), produced by the CarI synthase. 3-Oxo-C6-HSL binds to and activates the response regulator CarR, which is encoded immediately upstream of the carA gene. CarR/3-oxo-C6-HSL binds to the carA promoter and activates transcription of carA–H. Car production is also controlled by the hor gene product. Various environmental factors such as temperature, pH of the culture medium, carbon source and anaerobiosis also influence expression of carA–H. Pointed arrows or (+) symbols indicate a positive effect, while blunted arrows indicate a negative effect. The (?) symbols indicate a possible effect.

Figure 2

Models for quorum sensing-dependent control of Car production in (a,b) Erwinia carotovora ssp. carotovora strain ATCC 39048 and (c,d) Serratia sp. strain ATCC 39006. At low cell densities, carA–H are not expressed in both Erwinia and Serratia (a,c); in Erwinia, this is because transcription of carA–H is not activated (a). However, in Serratia, the SmaR repressor adds an extra layer of control by preventing transcription of carA–H and carR in the absence of quorum sensing signal (c). At high cell densities in Erwinia, the 3-oxo-C6-HSL quorum sensing signal binds and activates CarR, which promotes carA–H transcription and hence activates Car production (b). In Serratia, Car production is derepressed at high cell densities due to the AHL quorum sensing signal which inactivates the SmaR repressor. The Serratia CarR protein is then able to activate carA–H transcription in a ligand-independent manner (d).

Figure 3

Structures and abbreviations of AHL quorum sensing signalling molecules commonly produced by erwiniae and related species.