Decoding the genetic and functional diversity of the DSF quorum-sensing system in Stenotrophomonas maltophilia.

Pol Huedo,Daniel Yero,Àngels Ruyra,Isidre Gibert,Sònia Martinez-Servat,Xavier Daura,Nerea Roher

doi:10.3389/fmicb.2015.00761

Abstract

Stenotrophomonas maltophilia uses the Diffusible Signal Factor (DSF) quorum sensing (QS) system to mediate intra- and inter-specific signaling and regulate virulence-related processes. The components of this system are encoded by the rpf cluster, with genes rpfF and rpfC encoding for the DSF synthase RpfF and sensor RpfC, respectively. Recently, we have shown that there exist two variants of the rpf cluster (rpf-1 and rpf-2), distinguishing two groups of S. maltophilia strains. Surprisingly, only rpf-1 strains produce detectable DSF, correlating with their ability to control biofilm formation, swarming motility and virulence. The evolutive advantage of acquiring two different rpf clusters, the phylogenetic time point and mechanism of this acquisition and the conditions that activate DSF production in rpf-2 strains, are however not known. Examination of this cluster in various species suggests that its variability originated most probably by genetic exchange between rhizosphere bacteria. We propose that rpf-2 variant strains make use of a strategy recently termed as “social cheating.” Analysis of cellular and extracellular fatty acids (FAs) of strains E77 (rpf-1) and M30 (rpf-2) suggests that their RpfFs have also a thioesterase activity that facilitates the release of unspecific FAs to the medium in addition to DSF. Production of DSF in rpf-1 strains appears in fact to be modulated by some of these extracellular FAs in addition to other factors such as temperature and nutrients, while in rpf-2 strains DSF biosynthesis is derepressed only upon detection of DSF itself, suggesting that they require cohabitation with DSF-producer bacteria to activate their DSF regulatory machinery. Finally, we show that the mixed rpf-1/rpf-2 population presents synergism in DSF production and virulence capacity in an in vivo infection model. Recovery and quantification of DSF from co-infected animals correlates with the observed mortality rate.

Highlights

Quorum Sensing (QS) refers to bacterial communication processes that allow populations to synchronize gene expression when reaching a critical cellular density
The Two rpf Cluster Variants in S. maltophilia May Have Originated by Horizontal Exchange To infer the origin of the two rpf cluster variants in S. maltophilia the diversity of this cluster among Xanthomonadales species was studied
A phylogenetic tree based on the rpfC and rpfF concatenated sequences (Figure 1) suggests that the origin of the two rpf variants in S. maltophilia may be explained by horizontal gene transfer

Summary

Introduction

Quorum Sensing (QS) refers to bacterial communication processes that allow populations to synchronize gene expression when reaching a critical cellular density. The QS system described for the nosocomial pathogen Stenotrophomonas maltophilia is based on the fatty acid (FA) signal DSF (cis-11-methyl-2dodecenoic acid) (Fouhy et al, 2007; Huang and Lee Wong, 2007; Huedo et al, 2014b). This cell-cell communication system was described for the first time in the phytopathogen Xanthomonas campestris pv. Little is known about the mechanisms participating in the synthesis and perception of DSF molecules by S. maltophilia

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