Dataset Information

Modulation of Inter-kingdom Communication by PhcBSR Quorum Sensing System in Ralstonia solanacearum Phylotype I Strain GMI1000.

ABSTRACT: Ralstonia solanacearum is a ubiquitous soil-borne plant pathogenic bacterium, which frequently encounters and interacts with other soil cohabitants in competition for environmental niches. Ralsolamycin, which is encoded by the rmy genes, has been characterized as a novel inter-kingdom interaction signal that induces chlamydospore development in fungi. In this study, we provide the first genetic evidence that the rmy gene expression is controlled by the PhcBSR quorum sensing (QS) system in strain GMI1000. Mutation of phcB could lead to significant reduction of the expression levels of the genes involved in ralsolamycin biosynthesis. In addition, both the phcB and rmy mutants were attenuated in induction of chlamydospore formation in Fusarium oxysporum f. cubense and diminished in the ability to compete with the sugarcane pathogen Sporisorium scitamineum. Agreeable with the pattern of QS regulation, transcriptional expression analysis showed that the transcripts of the rmy genes were increased along with the increment of the bacterial population density. Taken together, the above findings provide new insights into the regulatory mechanisms that the QS system involves in governing the ralsolamycin inter-kingdom signaling system.

SUBMITTER: Li P

PROVIDER: S-EPMC5481312 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Modulation of Inter-kingdom Communication by PhcBSR Quorum Sensing System in Ralstonia solanacearum Phylotype I Strain GMI1000.

Li Peng P Yin Wenfang W Yan Jinli J Chen Yufan Y Fu Shuna S Song Shihao S Zhou Jianuan J Lyu Mingfa M Deng Yinyue Y Zhang Lian-Hui LH

Frontiers in microbiology 20170623

Ralstonia solanacearum is a ubiquitous soil-borne plant pathogenic bacterium, which frequently encounters and interacts with other soil cohabitants in competition for environmental niches. Ralsolamycin, which is encoded by the rmy genes, has been characterized as a novel inter-kingdom interaction signal that induces chlamydospore development in fungi. In this study, we provide the first genetic evidence that the rmy gene expression is controlled by the PhcBSR quorum sensing ...[more]

PMID: 28690607

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Project description:BackgroundThe infection and virulence functions of diverse plant and animal pathogens that possess quorum sensing systems are regulated by N-acylhomoserine lactones (AHLs) acting as signal molecules. AHL-acylase is a quorum quenching enzyme and degrades AHLs by removing the fatty acid side chain from the homoserine lactone ring of AHLs. This blocks AHL accumulation and pathogenic phenotypes in quorum sensing bacteria.ResultsAn aac gene of undemonstrated function from Ralstonia solanacearum GMI1000 was cloned, expressed in Escherichia coli; it inactivated four AHLs that were tested. The sequence of the 795 amino acid polypeptide was considerably similar to the AHL-acylase from Ralstonia sp. XJ12B with 83% identity match and shared 39% identity with an aculeacin A acylase precursor from the gram-positive actinomycete Actinoplanes utahensis. Aculeacin A is a neutral lipopeptide antibiotic and an antifungal drug. An electrospray ionisation mass spectrometry (ESI-MS) analysis verified that Aac hydrolysed the amide bond of AHL, releasing homoserine lactone and the corresponding fatty acids. However, ESI-MS analysis demonstrated that the Aac could not catalyze the hydrolysis of the palmitoyl moiety of the aculeacin A. Moreover, the results of MIC test of aculeacin A suggest that Aac could not deacylate aculeacin A. The specificity of Aac for AHLs showed a greater preference for long acyl chains than for short acyl chains. Heterologous expression of the aac gene in Chromobacterium violaceum CV026 effectively inhibited violacein and chitinase activity, both of which were regulated by the quorum-sensing mechanism. These results indicated that Aac could control AHL-dependent pathogenicity.ConclusionThis is the first study to find an AHL-acylase in a phytopathogen. Our data provide direct evidence that the functioning of the aac gene (NP520668) of R. solanacearum GMI1000 is via AHL-acylase and not via aculeacin A acylase. Since Aac is a therapeutic potential quorum-quenching agent, its further biotechnological applications in agriculture, clinical and bio-industrial fields should be evaluated in the near future.

Project description:Quorum sensing (QS) is a widely conserved bacterial regulatory mechanism that relies on production and perception of autoinducing chemical signals to coordinate diverse cooperative activities, such as virulence, exoenzyme secretion, and biofilm formation. In Ralstonia solanacearum, a phytopathogen causing severe bacterial wilt diseases in many plant species, previous studies identified the PhcBSR QS system, which plays a key role in regulation of its physiology and virulence. In this study, we found that R. solanacearum strain EP1 contains the genes encoding uncharacterized LuxI/LuxR (LuxI/R) QS homologues (RasI/RasR [designated RasI/R here]). To determine the roles of the RasI/R system in strain EP1, we constructed a specific reporter for the signals catalyzed by RasI. Chromatography separation and structural analysis showed that RasI synthesized primarily N-(3-hydroxydodecanoyl)-homoserine lactone (3-OH-C12-HSL). In addition, we showed that the transcriptional expression of rasI is regulated by RasR in response to 3-OH-C12-HSL. Phenotype analysis unveiled that the RasI/R system plays a critical role in modulation of cellulase production, motility, biofilm formation, oxidative stress response, and virulence of R. solanacearum EP1. We then further characterized this system by determining the RasI/R regulon using transcriptome sequencing (RNA-seq) analysis, which showed that this newly identified QS system regulates the transcriptional expression of over 154 genes associated with bacterial physiology and pathogenic properties. Taken together, the findings from this study present an essential new QS system in regulation of R. solanacearum physiology and virulence and provide new insight into the complicated regulatory mechanisms and networks in this important plant pathogen. IMPORTANCE Quorum sensing (QS) is a key regulator of virulence factors in many plant-pathogenic bacteria. Previous studies unveiled two QS systems (i.e., PhcBSR and SolI/R) in several R. solanacearum strains. The PhcBSR QS system is known for its key roles in regulation of bacterial virulence, and the LuxI/LuxR (SolI/R) QS system appears dispensable for pathogenicity in a number of R. solanacearum strains. In this study, a new functional QS system (i.e., RasI/R) was identified and characterized in R. solanacearum strain EP1 isolated from infected eggplants. Phenotype analyses showed that the RasI/R system plays an important role in regulation of a range of biological activities associated with bacterial virulence. This QS system produces and responds to the QS signal 3-OH-C12-HSL and hence regulates critical bacterial abilities in survival and infection. To date, multiple QS signaling circuits in R. solanacearum strains are still not well understood. Our findings from this study provide new insight into the complicated QS regulatory networks that govern the physiology and virulence of R. solanacearum and present a valid target and clues for the control and prevention of bacterial wilt diseases.

Dataset Information

Modulation of Inter-kingdom Communication by PhcBSR Quorum Sensing System in Ralstonia solanacearum Phylotype I Strain GMI1000.

Publications

Modulation of Inter-kingdom Communication by PhcBSR Quorum Sensing System in <i>Ralstonia solanacearum</i> Phylotype I Strain GMI1000.

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