The Global Virulence Regulators VsrAD and PhcA Control Secondary Metabolism in the Plant Pathogen <i>Ralstonia solanacearum</i>

Schneider, Patrick; Jacobs, Jonathan M.; Neres, João; Aldrich, Courtney C.; Allen, Caitilyn; Nett, Markus; Hoffmeister, Dirk

doi:10.1002/cbic.200900510

Cited by 42 publications

(44 citation statements)

References 87 publications

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“…In addition, HrpGcontrolled functions can also be activated via HrpG post-transcriptional modification, as well as via activation of hrpB transcription by an unidentified environmental metabolic signal(s) perceived in minimal culture medium (Genin et al, 1992;Brito et al, 1999;Plener et al, 2010). Beside HrpG, the sensor histidine kinase VsrA controls many other virulence functions (Schell et al, 1994;Huang et al, 1995;Schneider et al, 2009;Meng et al, 2011). In a previous study we showed that a hrpG stop mutation allowed the chimeric Ralstonia to infect nodule cells, via the modulation of T3SS-independent HrpG-controlled functions (Marchetti et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

Experimental evolution of nodule intracellular infection in legume symbionts

et al. 2013

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Soil bacteria known as rhizobia are able to establish an endosymbiosis with legumes that takes place in neoformed nodules in which intracellularly hosted bacteria fix nitrogen. Intracellular accommodation that facilitates nutrient exchange between the two partners and protects bacteria from plant defense reactions has been a major evolutionary step towards mutualism. Yet the forces that drove the selection of the late event of intracellular infection during rhizobium evolution are unknown. To address this question, we took advantage of the previous conversion of the plant pathogen Ralstonia solanacearum into a legume-nodulating bacterium that infected nodules only extracellularly. We experimentally evolved this draft rhizobium into intracellular endosymbionts using serial cycles of legume-bacterium cocultures. The three derived lineages rapidly gained intracellular infection capacity, revealing that the legume is a highly selective environment for the evolution of this trait. From genome resequencing, we identified in each lineage a mutation responsible for the extracellular-intracellular transition. All three mutations target virulence regulators, strongly suggesting that several virulence-associated functions interfere with intracellular infection. We provide evidence that the adaptive mutations were selected for their positive effect on nodulation. Moreover, we showed that inactivation of the type three secretion system of R. solanacearum that initially allowed the ancestral draft rhizobium to nodulate, was also required to permit intracellular infection, suggesting a similar checkpoint for bacterial invasion at the early nodulation/root infection and late nodule cell entry levels. We discuss our findings with respect to the spread and maintenance of intracellular infection in rhizobial lineages during evolutionary times.

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Section: Discussionmentioning

confidence: 99%

Experimental evolution of nodule intracellular infection in legume symbionts

et al. 2013

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“…The production of transaminase and furanone synthase, which are encoded by ralD and ralA , respectively, depends on functional PhcA via the phc QS system. Both the transaminase and furanone synthase are involved in the biosynthesis of ralfuranone I (Schneider et al, 2009; Wackler et al, 2011; Kai et al, 2014). Ralfuranone I is non-enzymatically converted into ralfuranone B in the supernatant (Kai et al, 2016).…”

Section: Feedback Regulation Of the Phc Qs By Ralfuranonesmentioning

confidence: 99%

“…Therefore, the integrated regulation of vsrAD and vsrBC expression by ralfuranones A, B, and J contributes to EPS I production and swimming motility. Furthermore, VsrAD is upstream of PhcA and is involved in the biosynthesis of ralfuranones (Schneider et al, 2009). Therefore, the expression of vsrAD may be feedback-regulated through ralfuranones A, B, and J, leading to the regulation of PhcA function.…”

Section: Regulation Of the Two-component Systems Vsrad And Vsrbc Bymentioning

confidence: 99%

Regulation Involved in Colonization of Intercellular Spaces of Host Plants in Ralstonia solanacearum

et al. 2017

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A soil-borne bacterium Ralstonia solanacearum invading plant roots first colonizes the intercellular spaces of the root, and eventually enters xylem vessels, where it replicates at high levels leading to wilting symptoms. After invasion into intercellular spaces, R. solanacearum strain OE1-1 attaches to host cells and expression of the hrp genes encoding components of the type III secretion system (T3SS). OE1-1 then constructs T3SS and secrets effectors into host cells, inducing expression of the host gene encoding phosphatidic acid phosphatase. This leads to suppressing plant innate immunity. Then, OE1-1 grows on host cells, inducing quorum sensing (QS). The QS contributes to regulation of OE1-1 colonization of intercellular spaces including mushroom-type biofilm formation on host cells, leading to its virulence. R. solanacearum strains AW1 and K60 produce methyl 3-hydroxypalmitate (3-OH PAME) as a QS signal. The methyltransferase PhcB synthesizes 3-OH PAME. When 3-OH PAME reaches a threshold level, it increases the ability of the histidine kinase PhcS to phosphorylate the response regulator PhcR. This results in elevated levels of functional PhcA, the global virulence regulator. On the other hand, strains OE1-1 and GMI1000 produce methyl 3-hydroxymyristate (3-OH MAME) as a QS signal. Among R. solanacearum strains, the deduced PhcB and PhcS amino acid sequences are related to the production of QS signals. R. solanacearum produces aryl-furanone secondary metabolites, ralfuranones, which are extracellularly secreted and required for its virulence, dependent on the QS. Interestingly, ralfuranones affect the QS feedback loop. Taken together, integrated signaling via ralfuranones influences the QS, contributing to pathogen virulence.

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“…From a biosynthetic perspective, micacocidin represents a new and discrete natural product class made by R. solanacearum and expands the known metabolome of this species, which already includes staphyloferrin B (3), the HrpBdependent factor HDF (8), and the ralfuranone family of compounds (37). It is worth mentioning that the availability of the genome sequence of GMI1000 (33) not only was instrumental in the discovery of these metabolites by promoting the development of specific isolation strategies but also granted insights into their biosyntheses (8,42).…”

Section: Discussionmentioning

confidence: 99%

“…Notwithstanding its significance as a pathogen, we know surprisingly little about the secondary metabolome of this bacterium and the ensuing implications for virulence. Recent studies have shown that R. solanacearum is capable of natural product biosynthesis and that the expression of the required biosynthesis genes responds to virulence-associated regulators (8,37), assuming a role of secondary metabolites in host adaptation and/or pathogenesis.…”

mentioning

confidence: 99%

Biosynthesis of a Complex Yersiniabactin-Like Natural Product via the mic Locus in Phytopathogen Ralstonia solanacearum

Kreutzer

Kage

Gebhardt

et al. 2011

Appl Environ Microbiol

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A genome mining study in the plant pathogenic bacterium Ralstonia solanacearum GMI1000 unveiled a polyketide synthase/nonribosomal peptide synthetase gene cluster putatively involved in siderophore biosynthesis. Insertional mutagenesis confirmed the respective locus to be operational under iron-deficient conditions and spurred the isolation of the associated natural product. Bioinformatic analyses of the gene cluster facilitated the structural characterization of this compound, which was subsequently identified as the antimycoplasma agent micacocidin. The metal-chelating properties of micacocidin were evaluated in competition experiments, and the cellular uptake of gallium-micacocidin complexes was demonstrated in R. solanacearum GMI1000, indicating a possible siderophore role. Comparative genomics revealed a conservation of the micacocidin gene cluster in defined, but globally dispersed phylotypes of R. solanacearum.

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The Global Virulence Regulators VsrAD and PhcA Control Secondary Metabolism in the Plant Pathogen Ralstonia solanacearum

Cited by 42 publications

References 87 publications

Experimental evolution of nodule intracellular infection in legume symbionts

Experimental evolution of nodule intracellular infection in legume symbionts

Regulation Involved in Colonization of Intercellular Spaces of Host Plants in Ralstonia solanacearum

Biosynthesis of a Complex Yersiniabactin-Like Natural Product via the mic Locus in Phytopathogen Ralstonia solanacearum

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