Involvement of a Quorum-Sensing-Regulated Lipase Secreted by a Clinical Isolate of
            <i>Burkholderia glumae</i>
            in Severe Disease Symptoms in Rice

Devescovi, Giulia; Bigirimana, Joseph; Degrassi, Giuliano; Cabrio, Laura; LiPuma, John J.; Kim, Jinwoo; Hwang, Ingyu; Venturi, Vittorio

doi:10.1128/aem.00105-07

Cited by 89 publications

(101 citation statements)

References 47 publications

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“…Although it is not classified as a human pathogen, a single case of the isolation of B. glumae from a clinical sample was reported (10), indicating that at least some strains of this pathogen may be associated with opportunistic infections in humans. The phytopathogenicity of B. glumae is caused by multiple factors, including the biosynthesis of toxoflavin (11,12); motility (13); the secretion of virulence factors by a type III secretion system (T3SS) (14); and the production of lipase (15), catalase (16), and pectate lyase (17). Since the expression of many of the respective genes is controlled by AHLs, QS plays a major role during plant infection processes as well (11,18).…”

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confidence: 99%

“…Strain B. glumae BGR1 was reported to possess a single QS system homologous to LuxI/ LuxR, designated TofI/TofR, involved in the biosynthesis and transport of toxoflavin (11). TofI, which is an AHL synthase belonging to the LuxI protein family (15,23), catalyzes the synthesis of an N-hexanoyl-homoserine lactone (C 6 -AHL) and an N-octa-noyl-homoserine lactone (C 8 -AHL) (8,11,24,25). The tofR gene encodes its cognate LuxR-type receptor protein.…”

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confidence: 99%

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Genome-Wide RNA Sequencing Analysis of Quorum Sensing-Controlled Regulons in the Plant-Associated Burkholderia glumae PG1 Strain

Gao

Krysciak

Petersen

et al. 2015

Appl Environ Microbiol

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dBurkholderia glumae PG1 is a soil-associated motile plant-pathogenic bacterium possessing a cell density-dependent regulation system called quorum sensing (QS). Its genome contains three genes, here designated bgaI1 to bgaI3, encoding distinct autoinducer-1 (AI-1) synthases, which are capable of synthesizing QS signaling molecules. Here, we report on the construction of B. glumae PG1 ⌬bgaI1, ⌬bgaI2, and ⌬bgaI3 mutants, their phenotypic characterization, and genome-wide transcriptome analysis using RNA sequencing (RNA-seq) technology. Knockout of each of these bgaI genes resulted in strongly decreased motility, reduced extracellular lipase activity, a reduced ability to cause plant tissue maceration, and decreased pathogenicity. RNA-seq analysis of all three B. glumae PG1 AI-1 synthase mutants performed in the transition from exponential to stationary growth phase revealed differential expression of a significant number of predicted genes. In comparison with the levels of gene expression by wild-type strain B. glumae PG1, 481 genes were differentially expressed in the ⌬bgaI1 mutant, 213 were differentially expressed in the ⌬bgaI2 mutant, and 367 were differentially expressed in the ⌬bgaI3 mutant. Interestingly, only a minor set of 78 genes was coregulated in all three mutants. The majority of the QS-regulated genes were linked to metabolic activities, and the most pronounced regulation was observed for genes involved in rhamnolipid and Flp pilus biosynthesis and the type VI secretion system and genes linked to a clustered regularly interspaced short palindromic repeat (CRISPR)-cas gene cluster. Q uorum sensing (QS) is a cell density-dependent gene regulation system in bacteria (1) in which the population density is sensed through the accumulation of bacterially produced signaling molecules called autoinducers (AIs). This cell-to-cell signaling process allows the microbial population to synchronize group behavior and alter its gene expression accordingly. QS is involved in a wide array of regulatory circuits, among which are pathogenicity, secretion of extracellular proteins, secondary metabolite production, and others (2). Key QS signaling molecules in many Gram-negative bacteria are N-acyl-homoserine lactones (AHLs) (3-5), synthesized mainly through LuxI homologs (EC 2.3.1.184) using S-adenosylmethionine (SAM), and an acyl-acyl carrier protein (acyl-ACP) from the fatty acid biosynthesis pathway (6). LuxR-type receptor/regulator proteins are involved in AHL signal perception. Together with LuxR, other proteins may be part of this regulatory circuit.The motile, rod-shaped Gram-negative soil bacterium Burkholderia glumae is considered to be a seed-borne pathogen that causes panicle blight of rice (7). B. glumae has also been reported to infect other plant species, like tomato, sunflower, and pepper (8, 9). Although it is not classified as a human pathogen, a single case of the isolation of B. glumae from a clinical sample was reported (10), indicating that at least some strains of this pathogen may be associated w...

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Genome-Wide RNA Sequencing Analysis of Quorum Sensing-Controlled Regulons in the Plant-Associated Burkholderia glumae PG1 Strain

Gao

Krysciak

Petersen

et al. 2015

Appl Environ Microbiol

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“…The seedlings were subsequently transferred to new 50-ml test tubes containing sterile perlite and then filled with half-diluted Hoagland solution containing 10 8 CFU of P. aeruginosa PUPa3 inoculant for every gram of perlite present. After 1 day in a 30°C growth chamber the plants were transferred to a full-containment greenhouse for an additional 10 days.…”

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LasI/R and RhlI/R Quorum Sensing in a Strain ofPseudomonas aeruginosaBeneficial to Plants

Steindler

Bertani

Sordi

et al. 2009

Appl Environ Microbiol

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Pseudomonas aeruginosa possesses three quorum-sensing (QS) systems which are key in the expression of a large number of genes, including many virulence factors. Most studies of QS in P. aeruginosa have been performed in clinical isolates and have therefore focused on its role in pathogenicity. P. aeruginosa, however, is regarded as a ubiquitous organism capable of colonizing many different environments and also of establishing beneficial associations with plants. In this study we examined the role of the two N-acyl homoserine lactone systems known as RhlI/R and LasI/R in the environmental rice rhizosphere isolate P. aeruginosa PUPa3. Both the Rhl and Las systems are involved in the regulation of plant growth-promoting traits. The environmental P. aeruginosa PUPa3 is pathogenic in two nonmammalian infection models, and only the double las rhl mutants are attenuated for virulence. In fact it was established that the two QS systems are not hierarchically organized and that they are both important for the colonization of the rice rhizosphere. This is an in-depth genetic and molecular study of QS in an environmental P. aeruginosa strain and highlights several differences with QS regulation in the clinical isolate PAO1.Pseudomonas aeruginosa has been intensively studied by the scientific community because it is an opportunistic pathogen able to chronically colonize and infect cystic fibrosis patients (30). An important aspect of this bacterium is its capability to adapt to the host environment through the extensive and complex transcriptional regulation of an arsenal of virulence genes. A key player in this response is the quorum-sensing (QS) cell-cell communication system, which coordinates the behavior of P. aeruginosa communities. In fact, the transcriptional regulation of many virulence genes is controlled by two N-acyl homoserine lactone (AHL)-dependent QS systems called LasI/R and RhlI/R (16, 48).In the LasI/R system, lasI directs the synthesis of N-(3-oxododecanoyl)-homoserine lactone (3-oxo-C12-HSL), which binds and activates the cognate response regulator LasR, resulting in the regulation of target gene expression. In the RhlI/R system, on the other hand, rhlI directs the synthesis of N-(butanoyl)-homoserine lactone (C4-HSL), which then interacts with the cognate RhlR, influencing transcription of target genes. These two QS systems are probably among the most studied in bacteria, and their regulons are fundamental to the pathogenicity of P. aeruginosa (48). Importantly, the two systems are intimately connected, being hierarchically organized with the LasI/R system regulating the transcription of rhlI-rhlR (29). The two QS regulons overlap, and together they constitute approximately 10% of the genes in P. aeruginosa, including factors like elastase, alkaline protease, exotoxin A, rhamnolipids, and pyocyanin, as well as being important for the regulation of biofilm formation (19,46,58). The two systems are themselves controlled by different regulators, allowing QS to respond and be modulated also by an array of...

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“…Significantly, the CepI/R AHL QS system was found to be involved in the regulation of similar phenotypes in many different species and strains of the BCC, including virulence in several models (reviewed by Eberl, 2006;Venturi et al, 2004). In addition to BCC members, also the plant-pathogenic Burkholderia plantarii and Burkholderia glumae were found to possess a CepI/R-like system producing and responding to C8-AHL and involved in the regulation of virulence-associated factors (Devescovi et al, 2007;Kim et al, 2004;Solis et al, 2006).The purpose of this study was to determine if the new environmental group of plant-associated diazotrophic Burkholderia species possesses an AHL QS system and whether it is important for nitrogen fixation and other important phenotypic features. We established that all the strains tested so far contain at least one highly conserved system, designated BraI/R, which is related to the LasI/R and PpuI/R AHL QS systems of P. aeruginosa and Pseudomonas putida, respectively, and is not similar to the CepI/R system.…”

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The new group of non-pathogenic plant-associated nitrogen-fixing Burkholderia spp. shares a conserved quorum-sensing system, which is tightly regulated by the RsaL repressor

2008

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The new group of non-pathogenic plant-associated nitrogen-fixing Burkholderia spp. shares a conserved quorum-sensing system, which is tightly regulated by the RsaL repressor A novel group of nitrogen-fixing plant-associated Burkholderia species has emerged in the last few years. The purpose of this investigation was to determine if these species possess an Nacylhomoserine lactone (AHL) quorum-sensing (QS) cell-cell signalling system, and whether it is important for nitrogen fixation and other phenotypic features in Burkholderia kururiensis. It was determined that B. kururiensis, and other members of this Burkholderia species cluster, contain at least one highly conserved system, designated BraI/R, which produces and responds to Ndodecanoyl-3-oxo-homoserine lactone (C12-3-oxo-AHL). The BraI/R AHL QS is not involved in the regulation of nitrogen fixation or in several other important phenotypes, indicating that it may not be a global regulatory system. The BraI/R system is similar to LasI/R of Pseudomonas aeruginosa and, as with lasI/R, there is a repressor gene, rsaL, between the braI/R genes. B. kururiensis normally synthesizes very low levels of C12-3-oxo-AHL, but the situation dramatically changes when RsaL is missing since an rsaL mutant displays a marked increase in AHL production. This unique stringent regulation indicates that RsaL could be an on/off switch for AHL QS in B. kururiensis and the ability to produce very high levels of AHL also questions the role of this molecule in the novel group of Burkholderia. The presence of a well-conserved and distinct AHL QS system among all the diazotrophic Burkholderia is a further indication that they are closely related, and that this system might play an important and conserved role in the lifestyle of this novel group of bacterial species. INTRODUCTIONThe genus Burkholderia in recent years has been phylogenetically well defined, consisting of species that are functionally remarkably diverse (Coenye & Vandamme, 2003). In fact, Burkholderia species have been isolated from many different environmental niches, including soil and water, and can form associations with plants, animals and humans. Phylogenetic trees, based on 16S rRNA sequence analysis, show clearly the separation of the genus Burkholderia into two major clusters (Caballero-Mellado et al., 2007), one of them mainly represented by plant, animal and human pathogenic species, including the opportunistic human ones referred to as Burkholderia cepacia complex (BCC) (Coenye & Vandamme, 2003). The BCC, a group of at least nine species, has received most attention by the scientific community since, besides being isolated from diverse environmental sources, they have also been recovered from clinical specimens. Patients with cystic fibrosis (CF) are particularly susceptible to members of the BCC, which can cause serious chronic lung infections and, together with Pseudomonas aeruginosa, represent the biggest threat to CF individuals (Coenye & LiPuma, 2003;LiPuma, 2003). Other members of the genus Burkholderia ca...

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Involvement of a Quorum-Sensing-Regulated Lipase Secreted by a Clinical Isolate of Burkholderia glumae in Severe Disease Symptoms in Rice

Cited by 89 publications

References 47 publications

Genome-Wide RNA Sequencing Analysis of Quorum Sensing-Controlled Regulons in the Plant-Associated Burkholderia glumae PG1 Strain

Genome-Wide RNA Sequencing Analysis of Quorum Sensing-Controlled Regulons in the Plant-Associated Burkholderia glumae PG1 Strain

LasI/R and RhlI/R Quorum Sensing in a Strain ofPseudomonas aeruginosaBeneficial to Plants

The new group of non-pathogenic plant-associated nitrogen-fixing Burkholderia spp. shares a conserved quorum-sensing system, which is tightly regulated by the RsaL repressor

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