Stenotrophomonas maltophilia responds to exogenous AHL signals through the LuxR solo SmoR (Smlt1839).

Paula Martã­Nez,Daniel Yero,Sã²Nia Martinez-Servat,Raquel Planell,Mario Ferrer-Navarro,Xavier Daura,Pol Huedo,Isidre Gibert

doi:10.3389/fcimb.2015.00041

Abstract

Quorum Sensing (QS) mediated by Acyl Homoserine Lactone (AHL) molecules are probably the most widespread and studied among Gram-negative bacteria. Canonical AHL systems are composed by a synthase (LuxI family) and a regulator element (LuxR family), whose genes are usually adjacent in the genome. However, incomplete AHL-QS machinery lacking the synthase LuxI is frequently observed in Proteobacteria, and the regulator element is then referred as LuxR solo. It has been shown that certain LuxR solos participate in interspecific communication by detecting signals produced by different organisms. In the case of Stenotrophomonas maltophilia, a preliminary genome sequence analysis revealed numerous putative luxR genes, none of them associated to a luxI gene. From these, the hypothetical LuxR solo Smlt1839, here designated SmoR, presents a conserved AHL binding domain and a helix-turn-helix DNA binding motif. Its genomic organization—adjacent to hchA gene—indicate that SmoR belongs to the new family “LuxR regulator chaperone HchA-associated.” AHL-binding assays revealed that SmoR binds to AHLs in-vitro, at least to oxo-C8-homoserine lactone, and it regulates operon transcription, likely by recognizing a conserved palindromic regulatory box in the hchA upstream region. Supplementation with concentrated supernatants from Pseudomonas aeruginosa, which contain significant amounts of AHLs, promoted swarming motility in S. maltophilia. Contrarily, no swarming stimulation was observed when the P. aeruginosa supernatant was treated with the lactonase AiiA from Bacillus subtilis, confirming that AHL contributes to enhance the swarming ability of S. maltophilia. Finally, mutation of smoR resulted in a swarming alteration and an apparent insensitivity to the exogenous AHLs provided by P. aeruginosa. In conclusion, our results demonstrate that S. maltophilia senses AHLs produced by neighboring bacteria through the LuxR solo SmoR, regulating population behaviors such as swarming motility.

Highlights

Bacterial cells can communicate with each other to facilitate their rapid adaptation to fluctuations in the environment
A subsequent protein alignment with known orphan regulators from distinct Proteobacteria including PpoR from P. putida, SdiA from S. enterica, OryR from X. oryzae pv. oryzae, and TraR from A. tumefaciens, revealed that at the N-terminal domain four out of six residues involved in Acyl Homoserine Lactone (AHL) binding (Patankar and González, 2009) are conserved in SmoR (Figure 1)
Since S. maltophilia frequently cohabit with AHL-producing bacteria –i.e., P. aeruginosa (Moskowitz et al, 2005)– we investigated the effect that P. aeruginosa AHLs could have on S. maltophilia regulation, on swarming motility

Summary

Introduction

Bacterial cells can communicate with each other to facilitate their rapid adaptation to fluctuations in the environment This cell-cell communication mechanism, known as quorum sensing (QS), relies primarily on the production, detection, and response to diffusible signal molecules ( called autoinducers) in a cell-density dependent manner (Fuqua et al, 1994; Whitehead et al, 2001; Fuqua and Greenberg, 2002; Federle and Bassler, 2003). Through this QS communication, numerous bacterial species regulate a variety of functions such as biofilm formation, motility, antibiotic resistance, toxin production, exopolysaccharide synthesis, and extracellular enzyme production among others (Miller and Bassler, 2001). The DNAbinding domain includes three highly conserved aminoacids, while the AHL-binding domain presents six hydrophobic or aromatic residues displaying remarkable variability (18-25%) (Zhang et al, 2002)

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