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. 2001 Mar;67(3):1198-209.
doi: 10.1128/AEM.67.3.1198-1209.2001.

Acyl-homoserine lactone production is more common among plant-associated Pseudomonas spp. than among soilborne Pseudomonas spp

M Elasri  1 , S Delorme, P Lemanceau, G Stewart, B Laue, E Glickmann, P M Oger, Y Dessaux
Affiliations

Acyl-homoserine lactone production is more common among plant-associated Pseudomonas spp. than among soilborne Pseudomonas spp

M Elasri et al. Appl Environ Microbiol. 2001 Mar.

Abstract

A total of 137 soilborne and plant-associated bacterial strains belonging to different Pseudomonas species were tested for their ability to synthesize N-acyl-homoserine lactones (NAHL). Fifty-four strains synthesized NAHL. Interestingly, NAHL production appears to be more common among plant-associated than among soilborne Pseudomonas spp. Indeed, 40% of the analyzed Pseudomonas syringae strains produced NAHL which were identified most often as the short-chain NAHL, N-hexanoyl-L-homoserine lactone, N-(3-oxo-hexanoyl)-homoserine lactone, and N-(3-oxo-octanoyl)-L-homoserine lactone (no absolute correlation between genomospecies of P. syringae and their ability to produce NAHL could be found). Six strains of fluorescent pseudomonads, belonging to the species P. chlororaphis, P. fluorescens, and P. putida, isolated from the plant rhizosphere produced different types of NAHL. In contrast, none of the strains isolated from soil samples were shown to produce NAHL. The gene encoding the NAHL synthase in P. syringae pv. maculicola was isolated by complementation of an NAHL-deficient Chromobacterium mutant. Sequence analysis revealed the existence of a luxI homologue that we named psmI. This gene is sufficient to confer NAHL synthesis upon its bacterial host and has strong homology to psyI and ahlI, two genes involved in NAHL production in P. syringae pv. tabaci and P. syringae pv. syringae, respectively. We identified another open reading frame that we termed psmR, transcribed convergently in relation to psmI and partly overlapping psmI; this gene encodes a putative LuxR regulatory protein. This gene organization, with luxI and luxR homologues facing each other and overlapping, has been found so far only in the enteric bacteria Erwinia and Pantoea and in the related species P. syringae pv. tabaci.

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Figures

FIG. 1
FIG. 1
Production of NAHL by various isolates of Pseudomonas. Supernatant extracts were obtained as indicated in Materials and Methods from strains of the P. tomato genomospecies: 1, CFBP 1573; 2, CFBP 1620; 3, CFBP 1702; 5, CFBP 2215; 6, CFBP 11007t; 7, CFBP 10912–9; and 8, CFBP 2212. S1 was a mixture of keto-NAHL (OBHL, 4; OHHL, 3; OOHL, 2; and ODHL, 1) used as a migration standard; S2, another migration standard, was a mixture of reduced NAHL (BHL, 3; HHL, 2; and OOHL, 1). (A) The sensor strain was Agrobacterium NT1(pDCI41E33) (43), which exhibits a high level of sensitivity toward reduced NAHL (concentration of standards according to Shaw et al. [43]). (B) The sensor strain was Chromobacterium CVO26 (32), which senses preferentially very-short-chain (C6 and C8) keto-NAHL (concentration of standards according to McClean et al. [32]).
FIG. 2
FIG. 2
Production of NAHL by the cloned psmI gene. Concentrated extracts of bacterial spent supernatants were obtained and analyzed as indicated in Materials and Methods using the Agrobacterium sensor strain NT1(pDCI41E33) (43). Extracts were obtained from P. tomato pv. persicae CFBP 1573 (lane 1) and CFBP 1573(pMES-A) (lane 2). A result identical to that shown in lane 2 was obtained using wild-type P. syringae pv. maculicola strain CFBP 10912–9 (not shown). S, migration standard consisting of OHHL (top) and OOHL (middle).
FIG. 3
FIG. 3
(A) Genetic organization of the psmI-psmR locus from P. syringae pv. maculicola strain CFBP 10912–9. In the diagram in the center of panel A, the putative identified ORFs are represented by arrows indicating the direction of transcription. The upper diagram shows a detail of the overlap between the psmI and psmR genes. The lower diagram shows a detail of the promoter region of the psmI gene. The sequences of the putative regulatory elements (−35, −10, and RBS) are underlined. The position of the putative lux box is indicated by the convergent arrows. The gentamicin cassette used to disrupt the psmI gene was inserted at the SspI site shown above the psmI ORF. (B) Sequence alignment of lux boxes from the psmI gene of P. syringae pv. maculicola, the luxI gene of P. fischeri, the esaI gene of P. stewartii, and the traA gene of A. tumefaciens.
FIG. 4
FIG. 4
Relatedness of the PsmI protein to other NAHL synthases. (A) Protein sequence alignment of PsmI with PsyI, AhlI, and LuxI, NAHL synthases from P. syringae pv. tabaci, P. syringae pv. syringae, and P. fischeri, respectively. Bold letters and boxes indicate identity; grey shading indicates similarity. (B) Similarity and identity with other LuxI-like proteins.
FIG. 5
FIG. 5
Relatedness of the PsmR protein to other LuxR-type regulators. (A) Protein sequence alignment of PsmR with PsyR and LuxR from P. syringae pv. tabaci and P. fischeri, respectively. Bold letters and boxes indicate identity; grey shading indicates similarity. The black bar indicates the putative DNA-binding domain. (B) Similarity and identity with other LuxR-like proteins.
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