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A LysR-Type Transcriptional Regulator LcrX Is Involved in Virulence, Biofilm Formation, Swimming Motility, Siderophore Secretion, and Growth in Sugar Sources in Xanthomonas axonopodis Pv. glycines.

ABSTRACT: Xanthomonas axonopodis pv. glycines (Xag) is a Gram-negative bacterium that causes bacterial pustule disease in soybean. To acclimate to new environments, the expression of genes in bacteria is controlled directly or indirectly by diverse transcriptional factors. Among them, LysR type transcriptional regulators are well-characterized and abundant in bacteria. In a previous study, comparative proteomic analysis revealed that LysR type carbohydrate-related transcriptional regulator in Xag (LcrX) was more abundant in XVM2, which is a minimal medium, compared with a rich medium. However, the functions of LcrX in Xag have not been characterized. In this study, we generated an LcrX-overexpressing strain, Xag(LcrX), and the knockout mutant strain, Xag?lcrX(EV), to elucidate the functions of LcrX. Bacterial multiplication of Xag(LcrX) in soybean was significantly impaired, indicating that LcrX is related to virulence. Comparative proteomic analysis revealed that LcrX is mainly involved in carbohydrate metabolism/transport and inorganic ion transport/metabolism. Based on the results of proteomics analysis, diverse phenotypic assays were carried out. A gel electrophoresis mobility shift assay demonstrated that LcrX specifically bound to the putative promoter regions of genes encoding putative fructose 1,6-bisphosphatase and protease. Through a 96-well plate assay under various conditions, we confirmed that the growth of Xag(LcrX) was dramatically affected in the presence of various carbon sources, while the growth of Xag?lcrX(EV) was only slightly changed. Biofilm formation activity was reduced in Xag(LcrX) but enhanced in Xag?lcrX(EV). The production of siderophores was also decreased in Xag(LcrX) but not altered in Xag?lcrX(EV). In contrast, LcrX was not associated with exopolysaccharide production, protease activity, or bacterial motility. These findings provide new insights into the functions of a carbohydrate-related transcriptional regulator in Xag.

SUBMITTER: Park H

PROVIDER: S-EPMC6965072 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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A LysR-Type Transcriptional Regulator LcrX Is Involved in Virulence, Biofilm Formation, Swimming Motility, Siderophore Secretion, and Growth in Sugar Sources in Xanthomonas axonopodis Pv. glycines.

Park Hanbi H Do Eunsoo E Kim Minyoung M Park Hye-Jee HJ Lee Jongchan J Han Sang-Wook SW

Frontiers in plant science 20200110

Xanthomonas axonopodis pv. glycines (Xag) is a Gram-negative bacterium that causes bacterial pustule disease in soybean. To acclimate to new environments, the expression of genes in bacteria is controlled directly or indirectly by diverse transcriptional factors. Among them, LysR type transcriptional regulators are well-characterized and abundant in bacteria. In a previous study, comparative proteomic analysis revealed that LysR type carbohydrate-related transcriptional regu ...[more]

PMID: 31998344

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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

A LysR-Type Transcriptional Regulator LcrX Is Involved in Virulence, Biofilm Formation, Swimming Motility, Siderophore Secretion, and Growth in Sugar Sources in Xanthomonas axonopodis Pv. glycines.

Publications

A LysR-Type Transcriptional Regulator LcrX Is Involved in Virulence, Biofilm Formation, Swimming Motility, Siderophore Secretion, and Growth in Sugar Sources in <i>Xanthomonas axonopodis</i> Pv. <i>glycines</i>.

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