scholarly journals Quorum Sensing Regulation in Phytopathogenic Bacteria

2021 ◽  
Vol 9 (2) ◽  
pp. 239
Author(s):  
Julie Baltenneck ◽  
Sylvie Reverchon ◽  
Florence Hommais

Quorum sensing is a type of chemical communication by which bacterial populations control expression of their genes in a coordinated manner. This regulatory mechanism is commonly used by pathogens to control the expression of genes encoding virulence factors and that of genes involved in the bacterial adaptation to variations in environmental conditions. In phytopathogenic bacteria, several mechanisms of quorum sensing have been characterized. In this review, we describe the different quorum sensing systems present in phytopathogenic bacteria, such as those using the signal molecules named N-acyl-homoserine lactone (AHL), diffusible signal factor (DSF), and the unknown signal molecule of the virulence factor modulating (VFM) system. We focus on studies performed on phytopathogenic bacteria of major importance, including Pseudomonas, Ralstonia, Agrobacterium, Xanthomonas, Erwinia, Xylella,Dickeya, and Pectobacterium spp. For each system, we present the mechanism of regulation, the functions targeted by the quorum sensing system, and the mechanisms by which quorum sensing is regulated.

Microbiology ◽  
2003 ◽  
Vol 149 (8) ◽  
pp. 1981-1989 ◽  
Author(s):  
Stéphane Uroz ◽  
Cathy D'Angelo-Picard ◽  
Aurélien Carlier ◽  
Miena Elasri ◽  
Carine Sicot ◽  
...  

Bacteria degrading the quorum-sensing (QS) signal molecule N-hexanoylhomoserine lactone were isolated from a tobacco rhizosphere. Twenty-five isolates degrading this homoserine lactone fell into six groups according to their genomic REP-PCR and rrs PCR-RFLP profiles. Representative strains from each group were identified as members of the genera Pseudomonas, Comamonas, Variovorax and Rhodococcus. All these isolates degraded N-acylhomoserine lactones other than the hexanoic acid derivative, albeit with different specificity and kinetics. One of these isolates, Rhodococcus erythropolis strain W2, was used to quench QS-regulated functions of other microbes. In vitro, W2 strongly interfered with violacein production by Chromobacterium violaceum, and transfer of pathogenicity in Agrobacterium tumefaciens. In planta, R. erythropolis W2 markedly reduced the pathogenicity of Pectobacterium carotovorum subsp. carotovorum in potato tubers. These series of results reveal the diversity of the QS-interfering bacteria in the rhizosphere and demonstrate the validity of targeting QS signal molecules to control pathogens with natural bacterial isolates.


2006 ◽  
Vol 188 (9) ◽  
pp. 3365-3370 ◽  
Author(s):  
Yannick Lequette ◽  
Joon-Hee Lee ◽  
Fouzia Ledgham ◽  
Andrée Lazdunski ◽  
E. Peter Greenberg

ABSTRACT The opportunistic pathogen Pseudomonas aeruginosa possesses two complete acyl-homoserine lactone (acyl-HSL) signaling systems. One system consists of LasI and LasR, which generate a 3-oxododecanoyl-homoserine lactone signal and respond to that signal, respectively. The other system is RhlI and RhlR, which generate butanoyl-homoserine lactone and respond to butanoyl-homoserine lactone, respectively. These quorum-sensing systems control hundreds of genes. There is also an orphan LasR-RhlR homolog, QscR, for which there is no cognate acyl-HSL synthetic enzyme. We previously reported that a qscR mutant is hypervirulent and showed that QscR transiently represses a few quorum-sensing-controlled genes. To better understand the role of QscR in P. aeruginosa gene regulation and to better understand the relationship between QscR, LasR, and RhlR control of gene expression, we used transcription profiling to identify a QscR-dependent regulon. Our analysis revealed that QscR activates some genes and represses others. Some of the repressed genes are not regulated by the LasR-I or RhlR-I systems, while others are. The LasI-generated 3-oxododecanoyl-homoserine lactone serves as a signal molecule for QscR. Thus, QscR appears to be an integral component of the P. aeruginosa quorum-sensing circuitry. QscR uses the LasI-generated acyl-homoserine lactone signal and controls a specific regulon that overlaps with the already overlapping LasR- and RhlR-dependent regulons.


2021 ◽  
Vol 8 ◽  
Author(s):  
April C. Armes ◽  
Alison Buchan

Microbial biofilms associated with marine particulate organic matter carry out transformations that influence local and regional biogeochemical cycles. Early microbial colonizers are often hypothesized to “set the stage” for biofilm structure, dynamics, and function via N-acyl homoserine lactone (AHL)-mediated quorum sensing (QS). Production of AHLs, as well as antimicrobials, contributes to the colonization success of members of the Roseobacter clade. One member of this group of abundant marine bacteria, Rhodobacterales sp. Y4I, possesses two QS systems, phaRI (QS1) and pgaRI (QS2). Here, we characterize mutants in both QS systems to provide genetic evidence that the two systems work in hierarchical fashion to coordinate production of the antimicrobial indigoidine as well as biofilm formation. A mutation in pgaR (QS2) results in decreased expression of genes encoding both QS systems as well as those governing the biosynthesis of indigoidine. In contrast, mutations in QS1 did not significantly influence gene expression of QS2. Addition of exogenous AHLs to QS1 and QS2 mutants led to partial restoration of indigoidine production (45–60% of WT) for QS1 but not QS2. Mutational disruptions of QS1 had a more pronounced effect on biofilm development than those in QS2. Finally, we demonstrate that c-di-GMP levels are altered in QS and indigoidine biosynthesis Y4I mutants. Together, these results indicate that pgaRI (QS2) is at the top of a regulatory hierarchy governing indigoidine biosynthesis and that the global regulatory metabolite, c-di-GMP, is likely integrated into the QS circuitry of this strain. These findings provide mechanistic understanding of physiological processes that are important in elucidating factors driving competitiveness of Roseobacters in nature.


Microbiology ◽  
2005 ◽  
Vol 151 (11) ◽  
pp. 3589-3602 ◽  
Author(s):  
B. Koch ◽  
T. Liljefors ◽  
T. Persson ◽  
J. Nielsen ◽  
S. Kjelleberg ◽  
...  

The function of LuxR homologues as quorum sensors is mediated by the binding of N-acyl-l-homoserine lactone (AHL) signal molecules to the N-terminal receptor site of the proteins. In this study, site-directed mutagenesis was carried out of the amino acid residues comprising the receptor site of LuxR from Vibrio fischeri, and the ability of the L42A, L42S, Y62F, W66F, D79N, W94D, V109D, V109T and M135A LuxR mutant proteins to activate green fluorescent protein expression from a PluxI promoter was measured. X-ray crystallographic studies of the LuxR homologue TraR indicated that residues Y53 and W57 form hydrogen bonds to the 1-carbonyl group and the ring carbonyl group, respectively, of the cognate AHL signal. Based on the activity and signal specificity of the LuxR mutant proteins, and on molecular modelling, a model is suggested in which Y62 (corresponding to Y53 in TraR) forms a hydrogen bond with the ring carbonyl group rather than the 1-carbonyl group, while W66 (corresponding to W57 in TraR) forms a hydrogen bond to the 1-carbonyl group. This flips the position of the acyl side chain in the LuxR/signal molecule complex compared to the TraR/signal molecule complex. Halogenated furanones from the marine alga Delisea pulchra and the synthetic signal analogue N-(sulfanylacetyl)-l-homoserine lactone can block quorum sensing. The LuxR mutant proteins were insensitive to inhibition by N-(propylsulfanylacetyl)-l-homoserine lactone. In contrast, the mutations had only a minor effect on the sensitivity of the proteins to halogenated furanones, and the data strongly suggest that these compounds do not compete in a ‘classic’ way with N-3-oxohexanoyl-l-homoserine lactone for the binding site. Based on modelling and experimental data it is suggested that these compounds bind in a non-agonist fashion.


2006 ◽  
Vol 74 (3) ◽  
pp. 1673-1682 ◽  
Author(s):  
Charles F. Sio ◽  
Linda G. Otten ◽  
Robbert H. Cool ◽  
Stephen P. Diggle ◽  
Peter G. Braun ◽  
...  

ABSTRACT The virulence of the opportunistic human pathogen Pseudomonas aeruginosa PAO1 is controlled by an N-acyl-homoserine lactone (AHL)-dependent quorum-sensing system. During functional analysis of putative acylase genes in the P. aeruginosa PAO1 genome, the PA2385 gene was found to encode an acylase that removes the fatty acid side chain from the homoserine lactone (HSL) nucleus of AHL-dependent quorum-sensing signal molecules. Analysis showed that the posttranslational processing of the acylase and the hydrolysis reaction type are similar to those of the beta-lactam acylases, strongly suggesting that the PA2385 protein is a member of the N-terminal nucleophile hydrolase superfamily. In a bioassay, the purified acylase was shown to degrade AHLs with side chains ranging in length from 11 to 14 carbons at physiologically relevant low concentrations. The substituent at the 3′ position of the side chain did not affect activity, indicating broad-range AHL quorum-quenching activity. Of the two main AHL signal molecules of P. aeruginosa PAO1, N-butanoyl-l-homoserine lactone (C4-HSL) and N-(3-oxododecanoyl)-l-homoserine lactone (3-oxo-C12-HSL), only 3-oxo-C12-HSL is degraded by the enzyme. Addition of the purified protein to P. aeruginosa PAO1 cultures completely inhibited accumulation of 3-oxo-C12-HSL and production of the signal molecule 2-heptyl-3-hydroxy-4(1H)-quinolone and reduced production of the virulence factors elastase and pyocyanin. Similar results were obtained when the PA2385 gene was overexpressed in P. aeruginosa. These results demonstrate that the protein has in situ quorum-quenching activity. The quorum-quenching AHL acylase may enable P. aeruginosa PAO1 to modulate its own quorum-sensing-dependent pathogenic potential and, moreover, offers possibilities for novel antipseudomonal therapies.


2012 ◽  
Vol 57 (1) ◽  
pp. 569-578 ◽  
Author(s):  
Moayad Alhariri ◽  
Abdelwahab Omri

ABSTRACTWe sought to investigate alterations in quorum-sensing signal moleculeN-acyl homoserine lactone secretion and in the release ofPseudomonas aeruginosavirulence factors, as well as thein vivoantimicrobial activity of bismuth-ethanedithiol incorporated into a liposome-loaded tobramycin formulation (LipoBiEDT-TOB) administered to rats chronically infected withP. aeruginosa. The quorum-sensing signal moleculeN-acyl homoserine lactone was monitored by using a biosensor organism.P. aeruginosavirulence factors were assessed spectrophotometrically. An agar beads model of chronicPseudomonaslung infection in rats was used to evaluate the efficacy of the liposomal formulation in the reduction of bacterial count. The levels of active tobramycin in the lungs and the kidneys were evaluated by microbiological assay. LipoBiEDT-TOB was effective in disrupting both quorum-sensing signal moleculesN-3-oxo-dodeccanoylhomoserine lactone andN-butanoylhomoserine lactone, as well as significantly (P< 0.05) reducing lipase, chitinase, and protease production. At 24 h after 3 treatments, the CFU counts in lungs of animals treated with LipoBiEDT-TOB were of 3 log10CFU/lung, comparated to 7.4 and 4.7 log10CFU/lung, respectively, in untreated lungs and in lungs treated with free antibiotic. The antibiotic concentration after the last dose of LipoBiEDT-TOB was 25.1 μg/lung, while no tobramycin was detected in the kidneys. As for the free antibiotic, we found 6.5 μg/kidney but could not detect any tobramycin in the lungs. Taken together, LipoBiEDT-TOB reduced the production of quorum-sensing molecules and virulence factors and could highly improve the management of chronic pulmonary infection in cystic fibrosis patients.


2003 ◽  
Vol 185 (3) ◽  
pp. 809-822 ◽  
Author(s):  
Xuesong He ◽  
William Chang ◽  
Deanne L. Pierce ◽  
Laura Ort Seib ◽  
Jennifer Wagner ◽  
...  

ABSTRACT Rhizobium sp. strain NGR234 forms symbiotic, nitrogen-fixing nodules on a wide range of legumes via functions largely encoded by the plasmid pNGR234a. The pNGR234a sequence revealed a region encoding plasmid replication (rep) and conjugal transfer (tra) functions similar to those encoded by the rep and tra genes from the tumor-inducing (Ti) plasmids of Agrobacterium tumefaciens, including homologues of the Ti plasmid quorum-sensing regulators TraI, TraR, and TraM. In A. tumefaciens, TraI, a LuxI-type protein, catalyzes synthesis of the acylated homoserine lactone (acyl-HSL) N-3-oxo-octanoyl-l-homoserine lactone (3-oxo-C8-HSL). TraR binds 3-oxo-C8-HSL and activates expression of Ti plasmid tra and rep genes, increasing conjugation and copy number at high population densities. TraM prevents this activation under noninducing conditions. Although the pNGR234a TraR, TraI, and TraM appear to function similarly to their A. tumefaciens counterparts, the TraR and TraM orthologues are not cross-functional, and the quorum-sensing systems have differences. NGR234 TraI synthesizes an acyl-HSL likely to be 3-oxo-C8-HSL, but traI mutants and a pNGR234a-cured derivative produce low levels of a similar acyl-HSL and another, more hydrophobic signal molecule. TraR activates expression of several pNGR234a tra operons in response to 3-oxo-C8-HSL and is inhibited by TraM. However, one of the pNGR234a tra operons is not activated by TraR, and conjugal efficiency is not affected by TraR and 3-oxo-C8-HSL. The growth rate of NGR234 is significantly decreased by TraR and 3-oxo-C8-HSL through functions encoded elsewhere in the NGR234 genome.


2019 ◽  
Vol 2019 ◽  
pp. 1-10
Author(s):  
Yulia V. Zaitseva ◽  
Olga A. Koksharova ◽  
Valentina A. Lipasova ◽  
Vladimir A. Plyuta ◽  
Ilya V. Demidyuk ◽  
...  

In this study, we investigated the quorum sensing (QS) regulatory system of the psychrotrophic strain Serratia proteamaculans 94 isolated from spoiled refrigerated meat. The strain produced several N-acyl-L-homoserine-lactone (AHL) QS signal molecules, with N-(3-oxo-hexanoyl)-L-homoserine lactone and N-(3-hydroxy-hexanoyl)-L-homoserine lactone as two main types. The sprI and sprR genes encoding an AHL synthase and a receptor regulatory protein, respectively, were cloned and sequenced. Analysis of their nucleotide sequence showed that these genes were transcribed convergently and that their reading frames partly overlapped by 23 bp in the terminal regions. The genes were highly similar to the luxI/luxR-type QS genes of other Gram-negative bacteria. An spr-box (analog of the lux-box) was identified upstream of the sprR gene and found to be overlapped with the sequence of −10 sequence site in the promoter region of this gene. Inactivation of the sprI gene led to the absence of AHL synthesis, chitinolytic activity, and swimming motility; decrease of extracellular proteolytic activity; affected the cellular fatty acid composition; and reduced suppression of the fungal plant pathogen mycelium growth by volatile compounds emitted by strain S. proteamaculans 94. The data obtained demonstrated the important role of the QS system in the regulation of cellular processes in S. proteamaculans 94.


2008 ◽  
Vol 191 (3) ◽  
pp. 890-897 ◽  
Author(s):  
Sara Ferluga ◽  
Vittorio Venturi

ABSTRACT Xanthomonas oryzae pv. oryzae, the causal agent of bacterial leaf blight in rice, contains a regulator that is encoded in the genome, designated OryR, which belongs to the N-acyl homoserine lactone (AHL)-dependent quorum-sensing LuxR subfamily of proteins. However, we previously reported that X. oryzae pv. oryzae does not make AHLs and does not possess a LuxI-family AHL synthase and that the OryR protein is solubilized by a compound present in rice. In this study we obtained further evidence that OryR interacts with a rice signal molecule (RSM) and that the OryR concentration increases when rice is infected with X. oryzae pv. oryzae. We also describe three OryR target promoters which are regulated differently: (i) the neighboring proline iminopeptidase (pip) virulence gene, which is positively regulated by OryR in the presence of the RSM; (ii) the oryR promoter, which is negatively autoregulated independent of the RSM; and (iii) the 1,4-β-cellobiosidase cbsA gene, which is positively regulated by OryR independent of the RSM. We also found that the RSM for OryR is small, is not related to AHLs, and is not able to activate the broad-range AHL biosensor Agrobacterium tumefaciens NT1(pZLQR). Furthermore, OryR does not regulate production of the quorum-sensing diffusible signal factor present in the genus Xanthomonas. Therefore, OryR has unique features and is an important regulator involved in interkingdom communication between the host and the pathogen.


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