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Ralstonia pseudosolanacearum LOV domain protein regulates environmental stress tolerance, iron homeostasis and bacterial wilt virulence

ABSTRACT: Bacteria use diverse sensors to integrate environmental stimuli into physiological responses that ensure fitness and survival. Ralstonia pseudosolanacearum (Rps), a soil-borne plant pathogen that causes bacterial wilt disease, encodes a conserved LOV (light-oxygen-voltage) protein known to mediate photoreception across the tree of life. However, Rps had a minimal LOV-dependent transcriptional response to light. Using clues from functional domains, the lov genomic neighborhood, and in planta transcriptional analyses, we tested the hypothesis that LOV shapes Rps biology in response to stress. We discovered lov modulates Rps stress response and virulence independently of light cues, but in a plant-dependent fashion. A ∆lov mutant had reduced heat tolerance that required a conserved flavin mononucleotide-binding cysteine residue. Deleting lov caused broad metabolic dysregulation, leading to growth defects on several carbon sources. In contrast ∆lov grew better in ex vivo tomato xylem sap and in high-iron medium, a possible consequence of its increased siderophore production. However, LOV is essential for full virulence in the host, mediating attachment to the root surface, stem colonization, and overall symptom development. Together these findings reveal that LOV, which is highly conserved among plant pathogenic Ralstonia, regulates a myriad of functions required for plant fitness independently of light.

ORGANISM(S): Ralstonia pseudosolanacearum

PROVIDER: GSE298975 | GEO | 2025/12/05

REPOSITORIES: GEO

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Project description:Peyraud2016 - Metabolic reconstruction (iRP1476) of Ralstonia solanacearum GMI1000 This model is described in the article: A Resource Allocation Trade-Off between Virulence and Proliferation Drives Metabolic Versatility in the Plant Pathogen Ralstonia solanacearum. Peyraud R, Cottret L, Marmiesse L, Gouzy J, Genin S. PLoS Pathog. 2016 Oct; 12(10): e1005939 Abstract: Bacterial pathogenicity relies on a proficient metabolism and there is increasing evidence that metabolic adaptation to exploit host resources is a key property of infectious organisms. In many cases, colonization by the pathogen also implies an intensive multiplication and the necessity to produce a large array of virulence factors, which may represent a significant cost for the pathogen. We describe here the existence of a resource allocation trade-off mechanism in the plant pathogen R. solanacearum. We generated a genome-scale reconstruction of the metabolic network of R. solanacearum, together with a macromolecule network module accounting for the production and secretion of hundreds of virulence determinants. By using a combination of constraint-based modeling and metabolic flux analyses, we quantified the metabolic cost for production of exopolysaccharides, which are critical for disease symptom production, and other virulence factors. We demonstrated that this trade-off between virulence factor production and bacterial proliferation is controlled by the quorum-sensing-dependent regulatory protein PhcA. A phcA mutant is avirulent but has a better growth rate than the wild-type strain. Moreover, a phcA mutant has an expanded metabolic versatility, being able to metabolize 17 substrates more than the wild-type. Model predictions indicate that metabolic pathways are optimally oriented towards proliferation in a phcA mutant and we show that this enhanced metabolic versatility in phcA mutants is to a large extent a consequence of not paying the cost for virulence. This analysis allowed identifying candidate metabolic substrates having a substantial impact on bacterial growth during infection. Interestingly, the substrates supporting well both production of virulence factors and growth are those found in higher amount within the plant host. These findings also provide an explanatory basis to the well-known emergence of avirulent variants in R. solanacearum populations in planta or in stressful environments. This model is hosted on BioModels Database and identified by: MODEL1612020000. To cite BioModels Database, please use: BioModels Database: An enhanced, curated and annotated resource for published quantitative kinetic models. To the extent possible under law, all copyright and related or neighbouring rights to this encoded model have been dedicated to the public domain worldwide. Please refer to CC0 Public Domain Dedication for more information.

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Ralstonia pseudosolanacearum LOV domain protein regulates environmental stress tolerance, iron homeostasis and bacterial wilt virulence

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