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Gene expression profiling of Ralstonia solanacearum in unexplored environmental niches reveals essential genes to complete its life cycle

ABSTRACT: Bacterial pathogens exhibit a remarkable ability to persist and thrive in diverse ecological niches. Understanding the mechanisms enabling their transition between environments is crucial to control dissemination and potential disease outbreaks. Here, we use Ralstonia solanacearum, the causing agent of the bacterial wilt disease, as a model to investigate the bacterial transcriptomic adaptation to two environments, water and soil, and compare it with the well-studied in planta gene expression. We identified extensive transcriptional reprogramming in response to each environment. Strikingly, gene expression in water resembled expression during late xylem colonization, with an intriguing induction of the type 3 secretion system (T3SS). We reveal that basic pH and also to nutrient scarcity - conditions also encountered in planta during late infection stages - trigger the T3SS induction. In the soil environment, R. solanacearum upregulated stress-responses and alternate carbon source metabolism genes, mostly phenylacetate metabolism and glyoxylate cycle and downregulated virulence-associated genes. Furthermore, we proved through gain- and loss-of-function that genes encoding proteins associated with oxidative stress, such as the oxidative stress regulator OxyR and the catalase KatG, are key for survival of the bacterium in soil. This work identifies essential factors necessary for R. solanacearum to complete its life cycle and provides valuable insights into the biological processes driving pathogen adaptation to unexplored environments out of their hosts.

ORGANISM(S): Ralstonia solanacearum

PROVIDER: GSE239723 | GEO | 2023/12/11

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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Gene expression profiling of Ralstonia solanacearum in unexplored environmental niches reveals essential genes to complete its life cycle

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