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Deciphering how plant pathogenic bacteria disperse and meet: Molecular epidemiology of Xanthomonas citri pv. citri at microgeographic scales in a tropical area of Asiatic citrus canker endemicity.

ABSTRACT: Although some plant pathogenic bacteria represent a significant threat to agriculture, the determinants of their ecological success and evolutionary potential are still poorly understood. Refining our understanding of bacterial strain circulation at small spatial scales and the biological significance and evolutionary consequences of co-infections are key questions. The study of bacterial population biology can be challenging, because it requires high-resolution markers that can be genotyped with a high throughput. Here, we overcame this difficulty for Xanthomonas citri pv. citri, a genetically monomorphic bacterium causing Asiatic citrus canker (ACC). Using a genotyping method that did not require cultivating the bacterium or purifying DNA, we deciphered the pathogen's spatial genetic structure at several microgeographic scales, down to single lesion, in a situation of ACC endemicity. In a grove where copper was recurrently applied for ACC management, copper-susceptible and copper-resistant X. citri pv. citri coexisted and the bacterial population structured as three genetic clusters, suggesting a polyclonal contamination. The range of spatial dependency, estimated for the two largest clusters, was four times greater for the cluster predominantly composed of copper-resistant bacteria. Consistently, the evenness value calculated for this cluster was indicative of increased transmission. Linkage disequilibrium was high even at a tree scale, probably due to a combination of clonality and admixture. Approximately 1% of samples exhibited within-lesion multilocus polymorphism, explained at least in part by polyclonal infections. Canker lesions, which are of major biological significance as an inoculum source, may also represent a preferred niche for horizontal gene transfer. This study points out the potential of genotyping data for estimating the range of spatial dependency of plant bacterial pathogens, an important parameter for guiding disease management strategies.

SUBMITTER: Pruvost O

PROVIDER: S-EPMC6708428 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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Deciphering how plant pathogenic bacteria disperse and meet: Molecular epidemiology of <i>Xanthomonas citri</i> pv. <i>citri</i> at microgeographic scales in a tropical area of Asiatic citrus canker endemicity.

Pruvost Olivier O Boyer Karine K Ravigné Virginie V Richard Damien D Vernière Christian C

Evolutionary applications 20190410 8

Although some plant pathogenic bacteria represent a significant threat to agriculture, the determinants of their ecological success and evolutionary potential are still poorly understood. Refining our understanding of bacterial strain circulation at small spatial scales and the biological significance and evolutionary consequences of co-infections are key questions. The study of bacterial population biology can be challenging, because it requires high-resolution markers that can be genotyped wit ...[more]

PMID: 31462912

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Project description:The Xanthomonas citri pv. citri (X. citri) is a phytopathogenic bacterium that infects different species of citrus plants where it causes canker disease. The adaptation to different habitats is related to the ability of the cells to metabolize and to assimilate diverse compounds, including sulfur, an essential element for all organisms. In Escherichia coli, the necessary sulfur can be obtained by a set of proteins whose genes belong to the cys regulon. Although the cys regulon proteins and their importance have been described in many other bacteria, there are no data related to these proteins in X. citri or in the Xanthomonas genus. The study of the relevance of these systems in these phytopathogenic bacteria that have distinct mechanisms of infection is one essential step toward understanding their physiology. In this work, we used bioinformatics, molecular modeling and transcription analysis (RT-PCR) to identify and characterize the putative cys regulon genes in X. citri.We showed that the ATP Binding Cassette Transporter (ABC transporter) SbpCysUWA for sulfate uptake is conserved in X. citri and translated in presence of sulfate. On the other hand, differently from what is predicted in databases, according molecular modeling and phylogenetic analysis, X. citri does not show a proper taurine transporter, but two different ABC systems related to the alkanesulfonate/sulfonate transport that were recently acquired during evolution. RT-PCR analysis evidenced that these genes and their putative transcriptional regulator CysB are rather transcripted in XAM1, a medium with defined concentration of sulfate, than LB.The presence of at least three distinct systems for sulfate and sulfonates assimilation in X. citri evidenced the importance of these compounds for the bacterium. The transcription of genes involved with alkanesulfonate/sulfur compounds in XAM1 along to CysB suggests that despite the differences in the transporters, the regulation of these systems might be similar to the described for E. coli. Altogether, these results will serve as a foundation for further studies aimed to understanding the relevance of sulfur in growth, virulence and pathogenesis of X. citri and related bacteria.

Project description:BackgroundXanthomonas axonopodis pv. citri (X. a. pv. citri) causes citrus canker that can result in defoliation and premature fruit drop with significant production losses worldwide. Biofilm formation is an important process in bacterial pathogens and several lines of evidence suggest that in X. a. pv. citri this process is a requirement to achieve maximal virulence since it has a major role in host interactions. In this study, proteomics was used to gain further insights into the functions of biofilms.ResultsIn order to identify differentially expressed proteins, a comparative proteomic study using 2D difference gel electrophoresis was carried out on X. a. pv. citri mature biofilm and planktonic cells. The biofilm proteome showed major variations in the composition of outer membrane proteins and receptor or transport proteins. Among them, several porins and TonB-dependent receptor were differentially regulated in the biofilm compared to the planktonic cells, indicating that these proteins may serve in maintaining specific membrane-associated functions including signaling and cellular homeostasis. In biofilms, UDP-glucose dehydrogenase with a major role in exopolysaccharide production and the non-fimbrial adhesin YapH involved in adherence were over-expressed, while a polynucleotide phosphorylase that was demonstrated to negatively control biofilm formation in E. coli was down-regulated. In addition, several proteins involved in protein synthesis, folding and stabilization were up-regulated in biofilms. Interestingly, some proteins related to energy production, such as ATP-synthase were down-regulated in biofilms. Moreover, a number of enzymes of the tricarboxylic acid cycle were differentially expressed. In addition, X. a. pv. citri biofilms also showed down-regulation of several antioxidant enzymes. The respective gene expression patterns of several identified proteins in both X. a. pv. citri mature biofilm and planktonic cells were evaluated by quantitative real-time PCR and shown to consistently correlate with those deduced from the proteomic study.ConclusionsDifferentially expressed proteins are enriched in functional categories. Firstly, proteins that are down-regulated in X. a. pv. citri biofilms are enriched for the gene ontology (GO) terms 'generation of precursor metabolites and energy' and secondly, the biofilm proteome mainly changes in 'outer membrane and receptor or transport'. We argue that the differentially expressed proteins have a critical role in maintaining a functional external structure as well as enabling appropriate flow of nutrients and signals specific to the biofilm lifestyle.

Dataset Information

Deciphering how plant pathogenic bacteria disperse and meet: Molecular epidemiology of Xanthomonas citri pv. citri at microgeographic scales in a tropical area of Asiatic citrus canker endemicity.

Publications

Deciphering how plant pathogenic bacteria disperse and meet: Molecular epidemiology of <i>Xanthomonas citri</i> pv. <i>citri</i> at microgeographic scales in a tropical area of Asiatic citrus canker endemicity.

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