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Applied and Environmental Microbiology, January 2007, p. 650-654, Vol. 73, No. 2
0099-2240/07/$08.00+0     doi:10.1128/AEM.01681-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

SHORT REPORT

Cross-Species GacA-Controlled Induction of Antibiosis in Pseudomonads{triangledown}

Christophe Dubuis and Dieter Haas*

Département de Microbiologie Fondamentale, Université de Lausanne, CH-1015 Lausanne, Switzerland

Received 19 July 2006/ Accepted 1 November 2006


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ABSTRACT
 
Signal extracts prepared from culture supernatants of Pseudomonas fluorescens CHA0 and Pseudomonas aeruginosa PAO stimulated GacA-dependent expression of small RNAs and hence of antibiotic compounds in both hosts. Pseudomonas corrugata LMG2172 and P. fluorescens SBW25 also produced signal molecules stimulating GacA-controlled antibiotic synthesis in strain CHA0, illustrating a novel, N-acyl-homoserine lactone-independent type of interspecies communication.


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INTRODUCTION
 
In dense populations of many bacterial genera, cells communicate with one another by emitting and sensing chemical signals. These signal molecules regulate gene expression and enable the cells to engage collectively in various developmental processes and in the ability to colonize specific niches, in particular host organisms. As the extracellular signal concentrations increase with increasing cell population densities, it has been proposed that in this way the bacteria measure their population densities, and this phenomenon has been termed quorum sensing. Widely occurring and well-studied quorum-sensing signals include N-acyl-homoserine lactones (AHLs) in gram-negative bacteria, modified oligopeptides in gram-positive bacteria, and autoinducer 2 (AI-2) (a furanosyl diester) in both gram-negative and -positive bacteria (3, 10, 16, 40). Furthermore, some signal molecules having a relatively narrow host range have been characterized, for instance, the Pseudomonas quinolone signal (PQS) (2-heptyl-3-hydroxy-4-quinolone) in Pseudomonas and Burkholderia spp., cis-11-methyl-2-dodecenoate in Xanthomonas spp. and related genera, and 3-hydroxy-palmitate methyl ester in Ralstonia spp (5, 9, 41). When a signal molecule is shared by different species living in close association, interspecies communication can result (2, 30, 31).

The root-colonizing, plant-beneficial soil bacterium Pseudomonas fluorescens CHA0 produces several extracellular antibiotics and enzymes. Together, these exoproducts are important for the organism's ability to antagonize the development of fungal root pathogens and to suppress root diseases caused by these pathogens (12, 13). During in vitro cultivation, the exoproduct genes are expressed in a cell density-dependent manner, as is typical of a quorum-sensing response (1, 14, 20, 34). Both transcriptional and posttranscriptional regulatory mechanisms contribute to this expression pattern. However, global posttranscriptional control by the Gac/Rsm signal transduction pathway plays a decisive part. P. fluorescens CHA0 mutants that are defective in the GacS/GacA two-component system express exoproduct genes at a very low basal level throughout growth (4, 21, 42). In strain CHA0, the GacS/GacA two-component system positively controls the expression of three small regulatory RNAs termed RsmX, RsmY, and RsmZ. Together, they sequester the translational repressors RsmA and RsmE and thereby relieve posttranscriptional repression of target genes, e.g., phlA (involved in the biosynthesis of the antibiotic 2,4-diacetylphloroglucinol) and aprA (encoding exoprotease AprA) (14, 18, 29, 39). The Gac/Rsm cascade also positively regulates the synthesis of extracellular signal molecules which act as autoinducers of the cascade (7, 14, 18, 39, 42). The chemical nature of these signals is not known. However, they are not related to AHLs, AI-2, or peptides (14). GacS- and GacA-negative mutants are signal blind (42).

Gac/Rsm signal transduction cascades occur in many different gram-negative bacteria (15). Here we investigated whether signal molecules activating the Gac/Rsm cascade are produced by Pseudomonas species other than P. fluorescens CHA0 and, if so, whether there is interspecies communication via this regulatory cascade. As a primary assay for GacA-dependent signal activity, we used reporter gene constructs which measure transcriptional activation of the small RNA genes rsmY and rsmZ; these genes are induced two- to fourfold by saturating signal concentrations in the presence of functional GacA (7, 18).


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Cross talk between P. fluorescens CHA0 and P. aeruginosa PAO.
 
P. fluorescens CHA0 and the opportunistic human pathogen Pseudomonas aeruginosa PAO1 were grown in glycerol-Casamino Acids medium (34). Culture supernatants from these strains were acidified with HCl and extracted with dichloromethane, yielding crude signal preparations, as previously described (7, 18). The CHA0 signal markedly stimulated the expression of transcriptional rsmYCHA0-lacZ and rsmZCHA0-lacZ fusions in the wild-type CHA0 (Fig. 1A and B), as reported before (14, 39). In this assay, addition of either PQS, cis-11-methyl-2-dodecenoate, or 3-hydroxypalmitate methyl ester, each at 10 µM, had no effect (data not shown). Thus, none of these bacterial signals qualifies as a likely candidate for the CHA0 signal. However, a signal preparation from the wild-type P. aeruginosa PAO1 activated both fusions in strain CHA0, although signal activity appeared to be weaker than that of the CHA0 signal (Fig. 1A and B). An extract prepared from the gacA mutant PAO6281 provided very little signal activity (Fig. 1A and B), whereas an extract obtained from the lasI rhlI mutant PAO-JP2, which is devoid of AHLs (26), had wild-type activity (data not shown). In a reciprocal experiment, transcriptional rsmYPAO-lacZ and rsmZPAO-lacZ fusions were used as chromosomal insertions in P. aeruginosa strain PAO1. (Note that the P. aeruginosa genome contains two GacA-regulated small RNA genes, rsmY and rsmZ, but no rsmX homolog [17, 19].) Both reporter fusions were induced by signal preparations of strains CHA0 and PAO, although the PAO signal did not fully activate rsmYPAO-lacZ. Again, the gacA mutant PAO6281 produced a very small amount of signal (Fig. 1C and D). These results show that P. aeruginosa PAO produces a GacA-dependent signal and that the PAO and CHA0 signals can cross-activate transcription of the rsmY and rsmZ genes in the heterologous background.


Figure 1
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  		FIG. 1. Cross talk between P. aeruginosa PAO1 and P. fluorescens CHA0. The signal activities of P. aeruginosa PAO1 (squares), P. aeruginosa PAO6281 (gacA) (circles), and P. fluorescens CHA0 (triangles) were tested in reporter strains grown in 20 ml nutrient yeast broth (36) in 50-ml Erlenmeyer flasks with shaking; the medium was amended with 0.05% (vol/vol) Triton X-100 to avoid cell clumping. An equivalent of 50 ml of extracted culture supernatant dissolved in 100 µl methanol (7) was added as a standard signal preparation. Control mixtures (diamonds) contained 100 µl methanol instead of extracted supernatant. Reporter strains were P. fluorescens CHA0/pME6916 (rsmYCHA0-lacZ) (A), P. fluorescens CHA0/pME6091 (rsmZCHA0-lacZ) (B), P. aeruginosa PAO6558 (rsmYPAO-lacZ) (C), and P. aeruginosa PAO6554 (rsmZPAO-lacZ) (D). The incubation temperatures were 30°C for strain CHA0 and 37°C for strain PAO. ß-Galactosidase measurements (24) were carried out in triplicate using cells permeabilized with 5% (vol/vol) toluene. Experiments were done three times. The symbols indicate averages, and the error bars show standard deviations. OD600, optical density at 600 nm.

We confirmed these observations by assaying cellular activities that strongly depend on the functions of GacA and RsmY plus RsmZ. In P. fluorescens CHA0 we chose to monitor phlA expression by using a translational 'lacZ reporter in plasmid pME6702 (29). This construct specifically records posttranscriptional regulation; the phlA promoter, which responds to transcriptional effectors such as 2,4-diacetylphloroglucinol and other phenolic compounds (1, 34), was replaced by the constitutively expressed tac promoter. The expression of phlA'-'lacZ was induced about fourfold by the CHA0 signal preparation and about threefold by the PAO signal extract, whereas the gacA mutant PAO6281 was almost devoid of signal activity (Fig. 2). In P. aeruginosa PAO, we chose to assay the formation of the antibiotic pyocyanin, whose synthesis is distinctly dependent on the GacA system (19, 28). Ten milliliters of nutrient yeast broth (36) was inoculated with strain PAO1; after 16 h of incubation at 37°C, signal molecules extracted from 50-ml portions of various cultures were added and incubation was continued for 4 h. Pyocyanin concentrations in the cultures were then determined as previously described (8, 28). A signal preparation from strain CHA0 increased pyocyanin production by 15.9% ± 1.4%, whereas a signal extract from the AHL-deficient mutant PAO-JP2 enhanced pyocyanin production by 10.6% ± 0.7%, relative to the control without addition (2.7 µg/ml = 100%). Strain PAO-JP2 was used in order to avoid any effect of AHLs on pyocyanin production. A signal extract of the gacA mutant PAO6281 had no significant influence (≤1.5%) on pyocyanin production.


Figure 2
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  		FIG. 2. Stimulation of phlA gene expression in P. fluorescens CHA0 by signal preparations. Signal activities in extracted supernatants from P. aeruginosa PAO1 (squares), P. aeruginosa PAO6281 (gacA) (circles), and P. fluorescens CHA0 (triangles) were tested in the reporter strain P. fluorescens CHA0/pME6702 (phlA'-'lacZ) as described in the legend to Fig. 1. Control mixtures (diamonds) contained 100 µl methanol instead of extracted supernatant. The incubation temperature was 30°C. ß-Galactosidase measurements were carried out in triplicate using cells permeabilized with 5% (vol/vol) toluene. Experiments were done three times. The symbols indicate averages, and the error bars show standard deviations. OD600, optical density at 600 nm.


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Stimulation of antibiosis in strain CHA0 by antibiotic-negative Pseudomonas spp.
 
We wondered whether environmental isolates of Pseudomonas spp. might produce signals that activate the Gac/Rsm cascade in strain CHA0. In a collection of some 30 strains, the entire spectrum ranging from high to low or undetectable signal activity was found (6). We selected three strains that did not produce antibiotics under our experimental conditions: the biocontrol strain P. fluorescens SBW25 (25); the plant pathogen Pseudomonas corrugata LMG2172, which causes tomato pith necrosis (33, 38); and the industrial lipase producer Pseudomonas alcaligenes Ps93 (11). Signal preparations from strains SBW25 and LMG2172 stimulated the expression of rsmY-lacZ, rsmZ-lacZ, and ptac-phlA'-'lacZ fusions in strain CHA0, albeit less effectively than did the homologous CHA0 signal. No activity was detected in a culture supernatant of strain Ps93 (Fig. 3A, B, and C). On nutrient agar, colonies of SBW25 and LMG2172 markedly stimulated antibiotic production in a neighboring colony of strain CHA0, as detected by a Bacillus subtilis overlay (Fig. 3D). We presume that the CHA0 antibiotic that is produced predominantly under these conditions is 2,4-diacetylphloroglucinol. The significance of the biphasic antibiotic halos seen in the CHA0-SBW25 and CHA0-LMG2172 interactions is not clear. As expected from the results of Fig. 3A, B, and C, strain Ps93 had no significant effect on antibiotic production in strain CHA0 (Fig. 3D). These experiments demonstrate that both plant-beneficial and -pathogenic strains have the potential to cross-induce antibiosis in strain CHA0 and that the signal molecules produced by strains SBW25 and LMG2172 are diffusible in agar. Furthermore, the data in Fig. 3C suggest that this effect occurs at a posttranscriptional level. Qualitative assays for AHLs were positive for strain LMG2172 but negative for strains SBW25 and Ps93 (Table 1); thus, at least in the case of SBW25, signal activity was not correlated with AHL production.


Figure 3
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  		FIG. 3. Effects of strains P. fluorescens SBW25, P. corrugata LMG 2172, and P. alcaligenes Ps93 on the Gac/Rsm cascade and antibiosis in strain CHA0. (A to C) Signal activities in extracted supernatants from P. fluorescens CHA0 (triangles), P. fluorescens SBW25 (empty circles), P. corrugata LMG 2172 (filled circles), and P. alcaligenes Ps93 (filled diamonds) were tested in CHA0 reporter strains as described in the legend to Fig. 1. Reporter strains were P. fluorescens CHA0/pME6916 (rsmYCHA0-lacZ) (A), P. fluorescens CHA0/pME6091 (rsmZCHA0-lacZ) (B), and P. fluorescens CHA0/pME6702 (ptac-phlA'-'lacZ) (C). Control mixtures (empty diamonds) contained 100 µl methanol instead of extracted supernatant. ß-Galactosidase measurements were carried out in triplicate. Experiments were done three times. The symbols indicate averages, and the error bars show standard deviations. OD600, optical density at 600 nm. (D) Antibiotic production by P. fluorescens CHA0 in the presence P. fluorescens SBW25, P. corrugata LMG 2172, or P. alcaligenes Ps93. Strains SBW25, LMG 2172 and Ps93 were inoculated by placing 5-µl drops of overnight cultures onto nutrient agar (36). After incubation at 30°C for 24 h, 5-µl drops of a CHA0 culture were added and incubation continued for 24 h. An overlay with Bacillus subtilis revealed antibiotic production by growth inhibition zones.


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  		TABLE 1. Bacterial strains and plasmids used in this study

Further investigation to find signal-producing bacteria that do not belong to the Pseudomonas spp. revealed that culture extracts from Vibrio harveyi BB120 and Vibrio natriegens had high signal activities in assays with P. fluorescens reporter strains. By contrast, an Escherichia coli DH5{alpha} extract had no detectable activity (data not shown).


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Concluding remarks.
 
In P. aeruginosa, the GacS/GacA system modulates the quorum-sensing response by regulating AHL synthesis (19, 28). In Vibrio cholerae, the GacS/GacA (= VarS/VarA) system acts on the expression of the central virulence regulator LuxO, in parallel with two other quorum-sensing pathways involving AI-2 and cholera autoinducer 1, respectively (22). In P. fluorescens CHA0, the absence of quorum-sensing mechanisms controlled by AHLs and AI-2 (14, 27) has facilitated the detection of signals that activate the Gac/Rsm cascade. As we have shown here, such signals are not confined to strain CHA0. Their existence in plant-beneficial and -pathogenic pseudomonads suggests considerable scope for cross talk in ecosystems. Moreover, as both V. harveyi and V. natriegens appear to produce signal molecules that induce the Gac/Rsm pathway in P. fluorescens, it is conceivable that V. cholerae might also use similar signals in the VarS/VarA branch of quorum sensing.


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ACKNOWLEDGMENTS
 
This work was supported by the Swiss National Foundation for Scientific Research (project 31-64048.00) and the European Union (projects QLK3-2000-31759 and QLK3-CT-2002-0286).

We thank Cornelia Reimmann for critically reading the manuscript, Paul Williams for providing a sample of PQS, and Lian-Hui Zhang for supplying a sample of cis-11-methyl-2-dodecenoate.


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FOOTNOTES
 
* Corresponding author. Mailing address: Département de Microbiologie Fondamentale, Université de Lausanne, CH-1015 Lausanne, Switzerland. Phone: 41 21 692 56 31. Fax: 41 21 692 56 35. E-mail: Dieter.Haas{at}unil.ch. Back

{triangledown} Published ahead of print on 10 November 2006. Back


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Applied and Environmental Microbiology, January 2007, p. 650-654, Vol. 73, No. 2
0099-2240/07/$08.00+0     doi:10.1128/AEM.01681-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.




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