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Applied and Environmental Microbiology, March 2001, p. 1198-1209, Vol. 67, No. 3
Institut des Sciences Végétales,
CNRS UPR040, 91198 Gif-sur-Yvette Cedex,1 and
UMR INRA-Université de Bourgogne BBCE-IPM, CMSE-INRA,
21034 Dijon Cedex,2 France, and
University of Nottingham, Leicester, Sutton Bonington,
United Kingdom3
Received 24 August 2000/Accepted 12 December 2000
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.
In most habitats, microbes compete
to ensure their survival and multiplication. In the plant and soil
environments, the mechanisms that allow a bacterium to outcompete other
microbes are diverse (for reviews, see references 6,
8, and 47). Some of these traits are
expressed constitutively, i.e., at any moment in the life of the
microbial cell. Others are expressed only at times most favorable to
allow an efficient biological effect. The regulation of these processes
may depend on environmental parameters or alterations sensed by the
microbes (see, for example, references 25 and 34; for a review, see reference 5), such as
changes in microbial cell density. Indeed, microbes have evolved
regulatory systems allowing gene expression only when the microbial
cell density is appropriate. Such a phenomenon, which couples the
microbial cell density to the expression of the relevant biological
traits, is known as quorum sensing (QS) (for reviews, see references
20, 24, 41, and
46).
The mechanism underlying QS has been described for several microbes,
including gram-negative bacteria, gram-positive bacteria, and
streptomycetes (26). It involves the synthesis of
low-molecular-weight molecules that diffuse in and out of the bacterial
cell. As the bacterial population density increases, the amount of
signal molecules synthesized and, consequently, their concentration in
the environment increase. Once a critical concentration is reached, the
signal molecules can be bound by a ligand protein, which acts as a
transcription regulator in the microbial cell, allowing, upon binding,
the expression of QS-regulated genes (for reviews, see references
20, 24, 41, and
46).
In gram-negative bacteria, the QS signal molecules are almost
exclusively N-acyl-homoserine lactones (NAHL). Light
emission by the fish symbiont Photobacterium fischeri (also
known as Vibrio fischeri) was the first biological function
known to be regulated in a QS-dependent fashion (13). In
this bacterium, the NAHL-derived mediator was identified as
N-(3-oxo-hexanoyl)-homoserine lactone (OHHL)
(14), the synthesis of which relies on the activity of the
NAHL synthase LuxI (encoded at the luxI locus). OHHL can be bound by LuxR (encoded by the luxR gene), which in turn is
converted, upon binding, to a functional transcription regulator (for a
review, see reference 46). This regulator attaches to a
20-nucleotide, inverted-repeated sequence located upstream of the
operon encoding the proteins responsible for luminescence
(16), allowing its transcription. This palindrome sequence
is known as the lux operator or the lux box. It
has been found in the promoter regions of several QS-regulated genes
(see, for example, references 1, 2, and 19). Interestingly, the first gene of the lux
operon is luxI. Thus, the activation of the lux
operon stimulates the production of the protein responsible for the
production of OHHL (44).
Several bacterial traits are known to be regulated by LuxI- and
LuxR-like proteins as a function of cell density (41).
Indeed, luxI and luxR sequences have been
detected in various gram-negative bacteria, and the production of NAHL
signal molecules is widespread (4). These characteristics
apply to plant-associated bacteria whether they are beneficial or
deleterious for plant growth and health (37). Among the
systems described so far, the conjugal transfer of the Ti plasmid of
Agrobacterium tumefaciens depends on the presence of the
relevant opine(s) in the environment as well as on a QS regulatory
mechanism (18, 39). Similarly, the production of
macerating exoenzymes (40) or that of the antibiotic
carbapenem by Erwinia carotovora strains is regulated in a
cell-density-dependent fashion (33; for a review, see reference 46). All the above functions involve the production of
different NAHL, which differ from one species to the other or one
strain to the other but whose structures are closely related.
Fluorescent pseudomonads have also developed QS-regulated synthesis of
secondary metabolites implicated in antagonistic activities against
plant pathogens, such as phenazines and pyoverdines (36, 45,
51). Because of the role of QS in the regulation of important physiological processes in plant-bacterium associations and because NAHL production in plant-associated Pseudomonas species has
been investigated only in a small number of studies (4,
12), we decided to conduct a broad survey of NAHL production
among pseudomonads isolated from plant tissues, the plant rhizosphere,
or the bulk soil. NAHL production was not uncommon among
plant-associated pseudomonads but was not detected in soil isolates.
Among the plant-associated bacteria, members of the pathogenic
Pseudomonas syringae and related species often produced
NAHL. We therefore decided to characterize the genetic organization of
the NAHL-dependent regulatory system in a representative isolate,
P. syringae pv. maculicola strain CFBP 10912-9.
Genes involved in QS regulation were isolated and analyzed. They appear
to be distantly related members of the luxR-luxI gene
family, with an unusual organization characterized by luxR
and luxI facing and overlapping each other.
(Part of this work was presented at the 9th International Congress on
Molecular Plant-Microbe Interactions, Amsterdam, The Netherlands, July
1999.)
Bacterial strains and growth conditions.
Pseudomonas strains and their origins and characteristics
are listed in Tables 1, 2 and
3.
The cytochrome c oxidase-positive strains of fluorescent
pseudomonads are a representative subset of the diversity of a larger
collection of strains (n = 340) isolated from two bulk
soils and the rhizosphere of two plant species cultivated in these two
soils (28). All bacterial strains were different, even
though they belong to the same genomospecies and the same pathovar.
Three complementary NAHL biosensors were used: A. tumefaciens strain NT1(pDCI41E33) (43),
Chromobacterium violaceum strain CVO26
(32), and Escherichia coli strain JM109(pSB401)
(50). Plasmid pDCI41E33 from A. tumefaciens harbors traR but not traI and
contains a traG::lacZ fusion. CVO26 is
a mini-Tn5-generated mutant of C. violaceum
strain ATCC 31532 with all genes involved in violacein production and
mutated copies of two regulatory genes, making violacein production
dependent upon exogenous NAHL. Plasmid pSB401 harbors the
luxR gene and the lux operon of P. fischeri with a deleted luxI region, making light
emission dependent on the presence of exogenous NAHL. Other E. coli strains used were DH5
0099-2240/01/$04.00+0 DOI: 10.1128/AEM.67.3.1198-1209.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Acyl-Homoserine Lactone Production Is More
Common among Plant-Associated Pseudomonas spp. than
among Soilborne Pseudomonas spp.
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
(42) and DB82(pRK2013)
(11).
TABLE 1.
Names, origins, and NAHL-producing capacities of strains
of cytochrome c oxidase-negative species of
fluorescent pseudomonadsa
TABLE 2.
Names, origins, and NAHL-producing capacities of strains
of cytochrome c oxidase-positive species of fluorescent
pseudomonadsa
TABLE 3.
Names, origins, and NAHL-producing capacities of strains
of nonfluorescent species of Pseudomonasa
-D-galactopyranoside (X-Gal) was used at 40 µg/ml when necessary.
Chemicals. QS systems involve the production of several NAHL with closely related structures. We designate these molecules as a function of the number of carbon atoms of the lipid moiety and as a function of the substitution at position 3 of the fatty acid chains. The molecules are designated as follows: HSL, N-acyl-L-homoserine lactone; BHL, N-butanoyl-L-homoserine lactone (or C4-HSL); HHL, N-hexanoyl-L-homoserine lactone (or C6-HSL); OHL, N-octanoyl-L-homoserine lactone (or C8-HSL); DHL, N-decanoyl-L-homoserine lactone (or C10-HSL); OBHL, N-(3-oxo-butanoyl)-L-homoserine lactone (or 3-oxo-C4-HSL); OHHL, N-(3-oxo-hexanoyl)-L-homoserine lactone (or 3-oxo-C6-HSL); OOHL, N-(3-oxo-octanoyl)-L-homoserine lactone (or 3-oxo-C8-HSL); ODHL, N-(3-oxo-decanoyl)-L-homoserine lactone (or 3-oxo-C10 HSL); and OdDHL, N-(3-oxo-dodecanoyl)-L-homoserine lactone (or 3-oxo-C12-HSL). Authentic NAHL samples were kindly provided by Paul Williams (University of Nottingham).
NAHL extraction. For rapid determination of NAHL production in liquid medium, 1-ml samples of the strains were cultured in KBm. Strains were grown to stationary phase and centrifuged for 10 min at ca. 10,000 × g and 4°C. A 250-µl sample of the native culture supernatant was used to load wells in plate assays as described below. Strains identified as positive were further tested on ABG medium and retested on KBm. The spent culture supernatant was extracted as follows. Bacteria were grown in 5 ml of ABG medium or KBm to stationary phase. The media were centrifuged for 10 min at 7,500 × g and 4°C. The supernatant was extracted twice with 100% ethyl acetate to yield 10 ml of extract. The extract was dried over anhydrous sodium sulfate, filtered, and evaporated to dryness in a rotary evaporator at room temperature. The dried extract was resuspended in 600 µl of 100% ethyl acetate, evaporated again in a rotary evaporator at room temperature, and resuspended in 50 µl of 100% ethyl acetate. The final volume of the extract was therefore 1/100 that of the original culture medium.
NAHL detection and characterization. Individual strains were screened for the production of NAHL by two different assays. First, strains were screened on solid medium in a streak plate assay as described by Piper et al. (38) using the NAHL biosensors C. violaceum CVO26 and E. coli JM109(pSB401) on LBm and A. tumefaciens NT1(pDCI41E33) on ABM supplemented with 40 µg of X-Gal/ml. This assay was used to survey NAHL production by growing bacteria. Second, the presence of NAHL in native culture supernatants was assayed by the plate assay of McClean et al. (32) using the same three biosensors. Assay plates were incubated for 24 h for Chromobacterium and E. coli and for up to 48 h for Agrobacterium. NAHL produced by strains positive in any of the above-mentioned screens were further characterized by thin-layer chromatography (TLC) essentially as described by Shaw et al. (43) using the Agrobacterium sensor or by McClean et al. (32) using the Chromobacterium sensor. The concentrated extract was spotted onto a C18 reverse-phase TLC plate developed with a methanol-water solvent mixture. After elution, the plate was overlaid with soft agar containing bacterial indicators; this procedure generated a chromogenic compound upon sensing of a trace amount of one or more NAHL.
Modifications to the previously published protocols were as follows. TLC plates were C18 reverse-phase TLC plates (Silicagel; 60 Å, 20 by 20 cm, 0.2-mm thick). Elution buffers were methanol-water (60/40, vol/vol) for general use and methanol-water (70/30, vol/vol) for improved resolution of NAHL with acyl chains longer than eight carbon atoms. Characterization of the NAHL was based on the evaluation of the Rfs and shapes of the spots and on the differential responses of the sensor strains (including "reverse detection" by Chromobacterium [32]). An NAHL multistandard was always spotted on the TLC plates before migration of and along with the analyzed samples. The distributions of NAHL producers in different classes, defined according to their origins and to their relationships with the plant (soilborne isolates, nonpathogenic isolates from roots or leaves, and pathogenic isolates), were compared pairwise to a theoretical even distribution by a chi-square test.DNA manipulations and sequencing.
All molecular techniques,
such as DNA extraction and restriction analysis, were performed
using standard protocols (42). Routine cloning at various
sites of the ColE1-derived vector pUC19 (or related vectors) was done
with E. coli strain DH5 as a recipient strain. A genomic
DNA bank was obtained from 10912-9 by cloning the dephosphorylated
restriction products of a partial Sau3AI digestion of
genomic DNA from this strain at the BamHI site of the
broad-host-range cosmid vector pCP13/B (10) according to standard protocols (42). When necessary, cosmid clones
were transferred to gram-negative recipients by triparental mating with
DB82(pRK2013) (11).
Nucleotide sequence accession number. Sequences determined here have been deposited in GenBank under accession number AF234628.
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RESULTS |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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NAHL production is more common among plant-associated than among
soilborne Pseudomonas spp.
Using the protocols
described in Materials and Methods, strains which induced the
production of violacein (or which inhibited it) in the C. violaceum sensor, strains which activated the biosynthesis of
beta-galactosidase in A. tumefaciens NT1(pDCI41E33), and
strains which induced light emission in E. coli
JM109(pSB401) remained NAHL producers. The others were regarded as
nonproducing strains under our experimental conditions. The results of
this analysis and the identification of the synthesized NAHL molecules
are shown in Tables 1, 2 and 3 and in Fig.
1. As the characterization of the NAHL
molecules is based on the examination of the shapes and
Rfs of the spots and on the
differential responses of the sensors (with respect to standard
reference samples), the identification results must be interpreted with
care.
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2 = 11.53, P < 0.05).
Cloning of the genes responsible for NAHL production in P. syringae pv. maculicola. The above results indicate that NAHL production is not uncommon among plant-associated Pseudomonas species and especially among strains of P. syringae. However, little is known about the biological traits regulated via QS in P. syringae. To identify the NAHL biosynthetic pathway and the relevant regulated biological functions, we attempted to identify the genes involved in the synthesis of these compounds by a P. syringae strain. The strain chosen for this study was P. syringae pv. maculicola strain CFBP 10912-9 (P. tomato genomospecies) (Table 1), essentially because it produces large amounts of OHHL and OOHL.
To isolate the genes responsible for NAHL production, a genomic cosmid library of 10912-9 DNA was conjugated en masse by triparental mating into a rifampin-resistant derivative of the biosensor CVO26. Screening of ca. 5,000 transconjugants selected as being resistant to tetracycline and rifampin was used to identify the genes encoding the production of NAHL; this procedure yielded 20 clones that restored violacein production in the biosensor. The recombinant plasmids in the clones, all with inserts ranging from 20 to 35 kb, contained one or more similarly sized EcoRI and XhoI fragments and could be organized in two classes according to their restriction patterns. A representative of each class, termed pMES-A and pMES-B, was retained for further studies. The two cosmids were transferred into the non-NAHL-producing P. syringae pv. persicae strain CFBP 1573 (Table 1). Both conferred to that strain the ability to produce NAHL. Furthermore, TLC profiles of concentrated culture supernatants from CFBP 1573(pMES-A) and 10912-9 were indistinguishable (Fig. 2). The region of overlap between the two cosmid classes was mapped, subcloned into the ColE1-based vector pUC19, and introduced into E. coli DH5, which does
not produce any detectable NAHL. Two pUC19-derived clones, containing a
ca. 2-kb XhoI fragment (pMEX-A) and a 4.5-kb PstI
fragment (pMEP-A), conferred to that strain the ability to produce the
same NAHL signal molecules as the parent strain, P. syringae
pv. maculicola strain CFBP 10912-9 (Fig. 2), even in the absence of
isopropyl--D-thiogalactopyranoside (IPTG).
Interestingly, the original cosmid clones, pMES-A and pMES-B, did not
confer to the E. coli strain the ability to produce NAHL.
Similarly, two pUC19-derived clones containing the 2-kb XhoI fragment and the 4.5-kb PstI fragment in the
orientations opposite those in pMEX-A and pMEP-A, respectively, did not
induce the production of NAHL in DH5.
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Sequence analysis and identification of psmI and
psmR
The DNA sequence of the 2-kb
XhoI/XhoI fragment and that of its
adjacent regions were determined. DNA sequence analysis revealed the
presence of three ORFs organized as shown in Fig.
3. One of the three ORFs, which we named
psmI, could encode a 244-amino-acid protein with an
estimated mass of 27.16 kDa. This sequence is closely related to
those of two luxI gene homologues, ahlI
(12) and psyI (P. M. Oger et
al., unpublished data [GenBank accession number AF266600]), found in
other members of the P. syringae genomospecies (Fig.
4). The product of this ORF is only
distantly related to the other LuxI proteins. The psmI
ORF is preceded by sequences with reasonable matches to consensus
ribosome binding site (RBS) sequences and 
10 and 35 promoter
elements (Fig. 3). In addition, we were able to identify a sequence
closely related to the lux box consensus sequence at
positions 76 to 56 upstream of the psmI start codon,
indicating that this ORF could be regulated by a QS-dependent
regulator. Interestingly, this regulatory box lies between the best
matches to 35 and 10 sequences and overlaps the putative 10
sequence (Fig. 3). Since psmI is the only ORF on the
2-kb XhoI fragment of pMEX-A whose product shows
homology to NAHL synthases, its expression must be responsible
for NAHL synthesis in DH5(pMEX-A). Interestingly, the
XhoI site used for the cloning lies within the
psmI ORF. Therefore, the truncated psmI
ORF of pMEX-A still encodes a functional or partially functional NAHL
synthase.
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Analysis of psmI by complementation and mutational analysis. To confirm the involvement of psmI in NAHL synthesis, we recloned the 4.5-kb PstI fragment in the broad-host-range vector pBBR1MCS-3 and transferred it by triparental mating to P. fluorescens recipient strain 1855.344, which does not produce any NAHL (4; unpublished results). Strain 1855.344 harboring the cloned 4.5-kb PstI fragment now produced the same NAHL as wild-type strain 10912-9. A cassette encoding gentamycin resistance was cloned at the SspI site of the 4.5-kb PstI fragment to disrupt psmI (Fig. 3). The resulting construction was also transferred to 1855.344. The resulting transconjugants did not produce any NAHL (data not shown).
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DISCUSSION |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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The strain survey presented in the first part of this study indicates that NAHL production is not uncommon among plant-associated Pseudomonas strains. Several conclusions can be drawn. For instance, among oxidase-negative Pseudomonas strains, no clear correlation between taxonomic position and NAHL production is evident, with the exception of the 8 strains of the P. porri genomospecies (which did not appear to produce NAHL) and the 13 P. savastanoi strains (which all produced HHL and OHHL). During the course of this work, two surveys of NAHL production by gram-negative strains were published (4, 12). A few strains of the P. syringae group were examined for NAHL production. Some discrepancies between those studies and ours can be observed, e.g., for two P. savastanoi strains (CFBP 2088 and CFBP 2093). While Cha et al. (4) did not observe NAHL production for these strains, we report here that they do produce the NAHL signal molecules HHL and OHHL. This difference most likely results from the different growth conditions used in the two studies. However, this difference emphasizes that NAHL production among the strains analyzed by us and by others might have an even wider distribution. Strains which did not produce any NAHL under our experimental conditions might indeed produce such signal molecules under other growth conditions, e.g., in a more favorable or in an "inducing" environment, as reported for the opine-dependent NAHL synthesis involved in the regulation of Ti plasmid transfer in Agrobacterium (for a review, see reference 18).
As indicated above, most of the analyzed Pseudomonas strains produced short-chain NAHL (eight or fewer carbon atoms, e.g., HHL, OHHL, and OOHL). This feature is not due to a technical bias, since two of the biosensors are able to detect long-chain NAHL (Chromobacterium [reverse staining] and Agrobacterium) (32, 43). Indeed, one of the soil P. putida strains was found to produce ODHL and possibly OdDHL, two "long-chain" NAHL. The generalized production of HHL and OHHL by P. syringae strains is interesting and might reflect a common origin for the different QS systems in these strains.
Interestingly, our results go beyond those previously published (4, 12), as they indicate that NAHL production seems more common among pseudomonads closely associated with plants than among their soilborne counterparts. Indeed, the percentage of NAHL producers decreased from 49% among plant-pathogenic bacteria to 28 and 0% among nonpathogenic bacteria associated with the plant and soilborne bacteria, respectively. This finding suggests that the closer the relationship of the bacteria with the host plant, the higher the probability that it produces NAHL. That NAHL production appears to be more common among isolates closely associated with plant tissues may be related to the wealth of available carbon sources (31) in this highly competitive environment. This fact is consistent with the detection of QS-regulated functions in other plant-associated, plant-symbiont, or plant-pathogenic bacteria (for reviews, see references 20, 37, 41, and 46) or in other microbial hosts of rich ecotopes (e.g., Photobacterium, Shigella, and so forth). Alternatively, our results could reveal the limited ability of our experimental conditions to detect NAHL production in soilborne pseudomonads. If this is true, then the observed variation does not correlate with the mere presence of luxI and luxR loci but reflects differences in terms of regulation of these loci (e.g., additional regulatory levels, requirements for unknown inducers, and so forth). However, the statistical analysis demonstrates that these putative differences discriminating soilborne, plant-associated, and plant-pathogenic pseudomonads are statistically and biologically significant, as they correlate with the ecology of the bacteria.
The wide occurrence of NAHL producers among pseudomonads, especially among strains of P. syringae and related species, stands in contrast with the lack of information on the function(s) regulated in a QS-dependent way in these bacteria. A first step toward the elucidation and understanding of the QS-regulated functions in P. syringae strains involves the isolation of the relevant genes. Cloning and sequencing of the region responsible for NAHL production in P. syringae pv. maculicola led to the identification of two genes, psmI and psmR. To our knowledge, this is the first report of the presence of a luxR homologue in P. syringae. Sequence analysis of these genes revealed their high degree of homology to members of the luxI and luxR gene families, especially with the psyI and psyR genes from P. syringae pv. tabaci (Oger et al., unpublished results) and with the ahlI gene from P. syringae pv. syringae (12), respectively.
The psmI gene is likely to code for an NAHL synthase. Several lines of evidence support this hypothesis. First, it has strong homology to other genes encoding such enzymatic activities (Fig. 4). Second, the cloned gene conferred NAHL production upon nonproducing hosts (e.g., P. syringae pv. persicae, P. fluorescens, E. coli, and the two NAHL reporter strains tested). Third, bacteria hosting psmI exhibited a production pattern analogous to that of the P. syringae pv. maculicola strain. Finally, a mutated psmI gene does not confer NAHL production upon the bacterial host anymore. These features clearly indicate that the psmI gene is the necessary and sufficient genetic determinant accounting for the production of all NAHL signal molecules in P. syringae pv. maculicola CFBP 10912-9.
NAHL production in DH5 was observed only with clones harboring the
luxI gene inserted into a pUC19 plasmid (e.g., pMEX-A) and
under the control of the lac promoter and not with the
full-size cosmid clones harboring both the psmI and the
psmR genes, although the psmI gene was
expressed in the P. syringae pv. persicae background. This
result may have been due to the organization or sequence of the
promoter regions of P. syringae pv. maculicola genes that are not recognized by the E. coli transcription machinery,
although the psmI gene is preceded by reasonable matches to
consensus 35 and 10 sequences. This observation has also been
reported for several nonenteric bacterial species, such as P. fluorescens, P. syringae pv. tabaci, and A. tumefaciens. For example, the expression of
Agrobacterium virulence genes in E. coli requires
the presence of the alpha subunit of the RNA polymerase from
Agrobacterium (29). Our data also suggest that
PsmR could act as a repressor which prevents the expression of
psmI. In agreement with this hypothesis, a palindromic,
lux box-like sequence has been detected within the promoter
region of psmI, just upstream of the putative 10 sequence
and overlapping it. Interestingly, this lux box is located
at a position similar to that found in P. stewartii for a
system involving the LuxR-like repressor protein EsaR (3). This finding is also consistent with the observation that in other systems which involve activator proteins, the regulatory lux
sequences are located upstream of the proposed 35 elements (1,
16, 52). Recent results obtained by Luo and Farrand
(30) confirmed that the activity of the LuxR-type
regulator TraR, although an intrinsic property of the molecule, is also
strongly affected by the positioning of the lux box
(17).
Sequence data revealed a gene organization with two genes (psmI and psmR) facing each other and slightly overlapping. This organization is only the third example reported so far for bacteria. The first two were described for Yersinia (48) and Erwinia (Pantoea) (2). Although not demonstrated for P. syringae pv. maculicola or for any of the systems with convergently transcribed luxR and luxI genes, this organization may play an additional role in the regulation of the expression of the two genes, as the elevated transcription of one of the two may impair the expression of the other.
In some organisms, e.g., A. tumefaciens and P. fischeri, the genes regulated in a QS-dependent fashion are located downstream of the traI and luxI genes, respectively, and are coordinately regulated with these genes. In P. syringae pv. maculicola, this appears not to be the case. In this respect, the gene organization of psmI and psmR is similar to that in the enteric bacterium Erwinia (Pantoea), in which QS-regulated genes are not linked to the regulatory loci. The major difference between the organization of QS systems is of interest. In the systems in which a luxI homologue is the first gene of the LuxR-regulated operon, QS regulates only a single function, i.e., conjugal transfer for A. tumefaciens and bioluminescence for P. fischeri. In the systems in which a luxI homologue is not associated with a QS-regulated function, QS is most often involved in a complex regulatory scheme that controls the expression of more than one operon or function. This information suggests that QS may also regulate more than one trait in P. syringae pv. maculicola. Whether the functions regulated in a QS-dependent fashion in P. syringae pathovars are important for plant-microbe associations remains to be determined. However, with respect to previously published data, a possible correlation between NAHL synthesis and pathogenicity (2, 40), siderophore biogenesis (45), swarming (15), or biofilm formation (9) may be proposed.
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ACKNOWLEDGMENTS |
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This work was made possible by an E.U. grant (BIO4 CT96-181) to Y.D. and G.S. M.E. was supported by the same grant, and E.G. was supported by a grant from Académie d'Agriculture de France.
We thank Paul Williams and Andrea Hardman (Nottingham, United Kingdom) for NAHL samples and René Bally and Marie-Louise Bouillant (Lyon, France), Stephen K. Farrand (Champaign-Urbana, Ill.), and Louis Gardan (Angers, France) for helpful discussions and communication of unpublished material.
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FOOTNOTES |
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* Corresponding author. Mailing address: ISV, Bâtiment 23, CNRS, Ave. de la Terrasse, 91198 Gif-sur-Yvette Cedex, France. Phone: 33 1 6982 3690. Fax: 33 1 6982 3695. E-mail: yves.dessaux{at}isv.cnrs-gir.fr.
This paper is dedicated to the memory of Gordon Stewart.
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REFERENCES |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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| 1. | Baldwin, T. O., J. H. Devine, R. C. Heckel, J. W. Lin, and G. S. Shadel. 1989. The complete nucleotide sequence of the lux regulon of Vibrio fischeri and the luxABN region of Photobacterium leiognathi and the mechanism of control of bacterial bioluminescence. J. Biolumin. Chemilumin. 4:326-341[CrossRef][Medline]. |
| 2. |
Beck von Bodman, S., and S. K. Farrand.
1995.
Capsular polysaccharide biosynthesis and pathogenicity in Erwinia stewartii require induction by an N-acylhomoserine lactone autoinducer.
J. Bacteriol.
177:5000-5008 |
| 3. |
Beck von Bodman, S.,
D. R. Majerczak, and D. L. Coplin.
1998.
A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii.
Proc. Natl. Acad. Sci. USA
95:7687-7692 |
| 4. | Cha, C., P. Gao, Y. C. Chen, P. D. Shaw, and S. K. Farrand. 1998. Production of acyl-homoserine lactone quorum-sensing signals by gram-negative plant-associated bacteria. Mol. Plant Microbe Interact. 11:1119-1129[Medline]. |
| 5. |
Chang, C., and R. C. Stewart.
1998.
The two-component system. Regulation of diverse signaling pathways in prokaryotes and eukaryotes.
Plant Physiol.
117:723-731 |
| 6. | Chet, I., A. Ordenlich, R. Shapira, and A. Oppenheim. 1991. Mechanisms of biocontrol of soil-borne plant pathogens by Rhizobacteria, p. 229-236. In D. L. Keister, and P. B. Cregan (ed.), The rhizosphere and plant growth. Kluwer Academic Publishers, Dordrecht, The Netherlands. |
| 7. |
Chilton, M.-D.,
T. C. Currier,
S. K. Farrand,
A. J. Bendich,
M. P. Gordon, and E. W. Nester.
1974.
Agrobacterium tumefaciens and PS8 bacteriophage DNA not detected in crown gall tumor DNA.
Proc. Natl. Acad. Sci. USA
71:3672-3676 |
| 8. | Curl, E. A., and B. Truelove. 1986. Microbial interactions. Adv. Ser. Agric. Sci. 15:140-166. |
| 9. |
Davies, D. G.,
M. R. Parsek,
J. P. Pearson,
B. H. Iglewski,
J. W. Costerton, and E. P. Greenberg.
1998.
The involvement of cell-to-cell signals in the development of a bacterial biofilm.
Science
280:295-298 |
| 10. | Dessaux, Y., J. Tempé, and S. K. Farrand. 1987. Genetic analysis of mannityl opine catabolism in octopine-type Agrobacterium tumefaciens strain 15955. Mol. Gen. Genet. 208:301-308[CrossRef][Medline]. |
| 11. |
Ditta, G.,
S. Stanfield,
D. Corbin, and D. R. Helinski.
1980.
Broad host range DNA cloning system for Gram-negative bacteria: construction of a gene bank of Rhizobium meliloti.
Proc. Natl. Acad. Sci. USA
77:7347-7351 |
| 12. | Dumenyo, C. K., A. Mukherjee, W. Chunn, and A. R. Chatterjee. 1998. Genetic and physiological evidence for the production of N-acyl homoserine lactones by Pseudomonas syringae pv. syringae and other fluorescent plant pathogenic Pseudomonas species. Eur. J. Plant Pathol. 104:569-582[CrossRef]. |
| 13. |
Eberhard, A.
1972.
Inhibition and activation of bacterial luciferase synthesis.
J. Bacteriol.
109:1101-1105 |
| 14. | Eberhard, A., A. L. Burlingame, C. Eberhard, G. L. Kenyon, K. H. Nealson, and N. J. Oppenheimer. 1981. Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20:2444-2449[CrossRef][Medline]. |
| 15. | Eberl, L., M. K. Winson, C. Sternberg, G. S. Stewart, G. Christiansen, S. R. Chhabra, B. Bycroft, P. Williams, S. Molin, and M. Givskov. 1996. Involvement of N-acyl-L-homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol. Microbiol. 20:127-136[Medline]. |
| 16. | Egland, K. A., and E. P. Greenberg. 1999. Quorum sensing in Vibrio fischeri: elements of the luxI promoter. Mol. Microbiol. 31:1197-1204[CrossRef][Medline]. |
| 17. |
Egland, K. A., and E. P. Greenberg.
2000.
Conversion of the Vibrio fischeri transcriptional activator LuxR to a repressor.
J. Bacteriol.
182:805-811 |
| 18. | Farrand, S. K. 1998. Conjugal plasmids and their transfer, p. 199-233. In H. P. Spaink, A. Kondorosi, and P. J. J. Hooykaas (ed.), The Rhizobiaceae. Kluwer Academic Publishers, Dordrecht, The Netherlands. |
| 19. |
Fuqua, C., and S. C. Winans.
1996.
Conserved cis-acting promoter elements are required for density-dependent transcription of Agrobacterium tumefaciens conjugal transfer genes.
J. Bacteriol.
178:435-440 |
| 20. | Fuqua, C., and E. P. Greenberg. 1998. Self perception in bacteria: quorum sensing with acylated homoserine lactones. Curr. Opin. Microbiol. 1:183-189[CrossRef][Medline]. |
| 21. |
Gardan, L.,
C. Bollet,
M. Abu Ghorrah,
F. Grimont, and P. A. D. Grimont.
1992.
DNA relatedness among pathovar strains of Pseudomonas syringae pv. savastanoi Janse (1982) and proposal of Pseudomonas savastanoi sp. nov.
Int. J. Syst. Bacteriol.
42:606-612 |
| 22. |
Gardan, L.,
H. Shafik,
S. Belouin,
R. Broch,
F. Grimont, and P. A. D. Grimont.
1999.
DNA relatedness among the pathovars of Pseudomonas syringae and description of Pseudomonas tremae sp. nov. and Pseudomonas cannabina sp. nov. (ex Sutic and Dowson 1959).
Int. J. Syst. Bacteriol.
49:469-478 |
| 23. | Glickmann, E., L. Gardan, S. Jacquet, S. Hussain, M. Elasri, A. Petit, and Y. Dessaux. 1998. Auxin production is a common feature of most pathovars of Pseudomonas syringae. Mol. Plant Microbe Interact. 11:156-162[Medline]. |
| 24. | Gray, K. M. 1997. Intercellular communication and group behavior in bacteria. Trends Microbiol. 5:184-188[CrossRef][Medline]. |
| 25. | Joshi, H. M., and F. R. Tabita. 1996. A global two component signal transduction system that integrates the control of photosynthesis, carbon dioxide assimilation, and nitrogen fixation. Proc. Natl. Acad. Sci. USA 25:14515-14520. |
| 26. | Kleerebezem, M., L. E. Quadri, O. P. Kuipers, and W. M. de Vos. 1997. Quorum-sensing by peptide pheromones and two-component signal-transduction systems in Gram-positive bacteria. Mol. Microbiol. 24:895-904[CrossRef][Medline]. |
| 27. | Kovach, M. E., P. H. Elzer, D. S. Hill, G. T. Robertson, M. A. Farris, R. M. Roop II, and K. M. Peterson. 1995. Four new derivatives of the broad host range cloning vector, pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176[CrossRef][Medline]. |
| 28. | Latour, X., T. Corberand, G. Laguerre, F. Allard, and P. Lemanceau. 1996. The composition of fluorescent pseudomonad populations associated with roots is influenced by plant and soil type. Appl. Environ. Microbiol. 62:2449-2556[Abstract]. |
| 29. |
Lohrke, S. M.,
S. Nechaev,
H. Yang,
K. Severinov, and S. J. Jin.
1999.
Transcriptional activation of Agrobacterium tumefaciens virulence gene promoters in Escherichia coli requires the A. tumefaciens RpoA gene, encoding the alpha subunit of RNA polymerase.
J. Bacteriol.
181:4533-4539 |
| 30. |
Luo, Z.-Q., and S. K. Farrand.
1999.
Signal-dependent DNA binding and functional domains of the quorum-sensing activator TraR as identified by repressor activity.
Proc. Natl. Acad. Sci. USA
96:9009-9014 |
| 31. | Lynch, J. M., and J. M. Whipps. 1991. Substrate flow in the rhizosphere, p. 15-24. In D. L. Keister, and P. B. Cregan (ed.), The rhizosphere and plant growth. Kluwer Academic Publishers, Dordrecht, The Netherlands. |
| 32. |
McClean, K. H.,
M. K. Winson,
L. Fish,
A. Taylor,
S. R. Chhabra,
M. Camara,
M. Daykin,
J. H. Lamb,
S. Swift,
B. W. Bycroft,
G. S. A. B. Stewart, and P. Williams.
1997.
Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones.
Microbiology
143:3703-3711 |
| 33. |
McGowan, S.,
M. Sebaihia,
S. Jones,
B. Yu,
N. Bainton,
P. F. Chan,
B. Bycroft,
G. S. Stewart,
P. Williams, and G. P. Salmond.
1995.
Carbapenem antibiotic production in Erwinia carotovora is regulated by CarR, a homologue of the LuxR transcriptional activator.
Microbiology
141:541-550 |
| 34. | Mills, S. D., C. A. Jasalavich, and D. A. Cooksey. 1993. A two-component regulatory system required for copper-inducible expression of the copper resistance operon of Pseudomonas syringae. J. Bacteriol. 6:1656-1664. |
| 35. | Murillo, J., H. Shen, D. Gerhold, A. Sharma, D. A. Cooksey, and N. T. Keen. 1994. Characterization of pPT23B, the plasmid involved in syringolide production by Pseudomonas syringae pv. tomato PT23. Plasmid 31:275-287[CrossRef][Medline]. |
| 36. |
Pierson, L. S., III,
V. D. Keppenne, and D. W. Wood.
1994.
Phenazine antibiotic biosynthesis in Pseudomonas aureofaciens 30-84 is regulated by PhzR in response to cell density.
J. Bacteriol.
176:3966-3974 |
| 37. | Pierson, L. S., III, D. W. Wood, and E. A. Pierson. 1998. Homoserine lactone-mediated gene regulation in plant-associated bacteria. Annu. Rev. Phytopathol. 36:207-225[CrossRef][Medline]. |
| 38. | Piper, K. R., S. Beck von Bodman, and S. K. Farrand. 1993. Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction. Nature 362:448-450[CrossRef][Medline]. |
| 39. | Piper, K. R., S. Beck von Bodman, I. Hwang, and S. K. Farrand. 1999. Hierarchical gene regulatory systems arising from fortuitous gene associations: controlling quorum sensing by the opine regulon in Agrobacterium. Mol. Microbiol. 32:1077-1089[CrossRef][Medline]. |
| 40. | Pirhonen, M., D. Flego, R. Heikinheimo, and E. T. Palva. 1993. A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora. EMBO J. 12:2467-2476[Medline]. |
| 41. | Robson, N. D., A. R. J. Cox, S. J. McGowan, B. W. Bycroft, and G. P. C. Salmond. 1997. Bacterial N-acyl-homoserine-lactone-dependent signalling and its potential biotechnological application. Trends Biotechnol. 15:458-464[CrossRef][Medline]. |
| 42. | Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y. |
| 43. |
Shaw, P. D.,
P. Gao,
S. L. Daly,
C. Cha,
J. E. Cronan, Jr.,
K. L. Rinehart, and S. K. Farrand.
1997.
Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography.
Proc. Natl. Acad. Sci. USA
94:6036-6041 |
| 44. | Sitnikov, D. M., J. B. Schineller, and T. O. Baldwin. 1995. Transcriptional regulation of bioluminescence genes from Vibrio fischeri. Mol. Microbiol. 17:801-812[CrossRef][Medline]. |
| 45. | Stintzi, A., K. Evans, J.-M. Meyer, and K. Poole. 1998. Quorum sensing and siderophore biosynthesis in Pseudomonas aeruginosa: lasR/lasI mutants exhibit reduced pyoverdine biosynthesis. FEMS Microbiol. Lett. 166:341-345[CrossRef][Medline]. |
| 46. | Swift, S., N. J. Bainton, and M. K. Winson. 1994. Gram-negative bacterial communication by N-acyl homoserine lactones: a universal language? Trends Microbiol. 2:193-198[CrossRef][Medline]. |
| 47. | Thomashow, L. S., and D. M. Weller. 1991. Role of antibiotics and siderophores in biocontrol of take-all disease of wheat, p. 245-251. In D. L. Keister, and P. B. Cregan (ed.), The rhizosphere and plant growth. Kluwer Academic Publishers, Dordrecht, The Netherlands. |
| 48. | Throup, J. P., M. Camara, G. S. Briggs, M. K. Winson, S. R. Chhabra, B. W. Bycroft, P. Williams, and G. S. Stewart. 1995. Characterisation of the yenI/yenR locus from Yersinia enterocolitica mediating the synthesis of two N-acylhomoserine lactone signal molecules. Mol. Microbiol. 17:345-356[CrossRef][Medline]. |
| 49. | Vaudequin-Dransart, V., A. Petit, C. Poncet, C. Ponsonnet, X. Nesme, J. B. Jones, H. Bouzar, W. S. Chilton, and Y. Dessaux. 1995. Novel Ti plasmids in Agrobacterium strains isolated from fig tree and chrysanthemum tumors and their opinelike molecules. Mol. Plant Microbe Interact. 8:311-321[Medline]. |
| 50. | Winson, M. K., S. Swift, L. Fish, J. P. J. P. Throup, F. Jørgensen, S. R. Chhabra, B. W. Bycroft, P. Williams, and G. S. A. B. Stewart. 1998. Construction of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol. Lett. 163:185-192[CrossRef][Medline]. |
| 51. |
Wood, D. W.,
F. Gong,
M. M. Daykin,
P. Williams, and L. S. Pierson, III.
1997.
N-Acyl-homoserine lactone-mediated regulation of phenazine gene expression by Pseudomonas aureofaciens 30-84 in the wheat rhizosphere.
J. Bacteriol.
179:7663-7670 |
| 52. |
Zhu, J., and S. C. Winans.
1999.
Autoinducer binding by the quorum-sensing regulator TraR increases affinity for target promoters in vitro and decreases TraR turnover rates in whole cells.
Proc. Natl. Acad. Sci. USA
96:4832-4837 |
Applied and Environmental Microbiology, March 2001, p. 1198-1209, Vol. 67, No. 3
0099-2240/01/$04.00+0 DOI: 10.1128/AEM.67.3.1198-1209.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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