Xanthomonas citri subsp. citri requires a genus-specific outer membrane protein and TolB to coordinate cell membrane integrity and virulence

ABSTRACT Xanthomonas citri subsp. citri (Xcc) possesses a Xanthomonas-specific outer membrane protein XAC1347 (OMPXan) that exerts a role in the expression of the type III secretion system for pathogenicity. In this study, we reported that OMPXan was required for salt stress tolerance and cell membr...

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Main Authors: Leilei Wu, Xueyan Zhu, Hang Long, Xinyu Huang, Shuying Zhu, Qi Xue, Ziao Li, Huasong Zou
Format: Article
Language:English
Published: American Society for Microbiology 2025-02-01
Series:Microbiology Spectrum
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Online Access:https://journals.asm.org/doi/10.1128/spectrum.02521-24
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author Leilei Wu
Xueyan Zhu
Hang Long
Xinyu Huang
Shuying Zhu
Qi Xue
Ziao Li
Huasong Zou
author_facet Leilei Wu
Xueyan Zhu
Hang Long
Xinyu Huang
Shuying Zhu
Qi Xue
Ziao Li
Huasong Zou
author_sort Leilei Wu
collection DOAJ
description ABSTRACT Xanthomonas citri subsp. citri (Xcc) possesses a Xanthomonas-specific outer membrane protein XAC1347 (OMPXan) that exerts a role in the expression of the type III secretion system for pathogenicity. In this study, we reported that OMPXan was required for salt stress tolerance and cell membrane integrity, as well as the expression of the gum genes for the production of extracellular polysaccharides. Pull-down and yeast two-hybrid assays revealed that OMPXan interacts with TolB, a substrate of the Tol/Pal membrane protein system. The deletion of tolB resulted in similar phenotypic alterations as the OMPXan mutant in salt stress tolerance, cell membrane integrity, and the expression of hrpG, hrpX, hrpD6, and hrcC for pathogenicity. In contrast, the absence of TolB resulted in an increased level of expression of the gum genes and the production of extracellular polysaccharides. These results indicate that the interaction of OMPXan and TolB coordinates multi-faceted mechanisms to manage environmental stress and pathogenicity.IMPORTANCEThe gram-negative Xanthomoas citri subsp. citri (Xcc) is a causal agent of citrus canker, a serious bacterial disease on citrus plants. Our previous research reported that a Xanthomonas-specific outer membrane protein XAC1347 (OMPXan) is necessary for type III gene expression. This manuscript provided evidence to show that OMPXan interacts with Tol/Pal system substrate TolB. Moreover, OMPXan and TolB are both required for cell membrane integrity, stress adaption, and virulence. The overall results support that OMPXan and TolB coordinate multi-faceted mechanisms to manage environmental stress and pathogenicity.
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publishDate 2025-02-01
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spelling doaj-art-d2c5a0c0c91c487bae9eb99aedf744ed2025-02-04T14:03:41ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-02-0113210.1128/spectrum.02521-24Xanthomonas citri subsp. citri requires a genus-specific outer membrane protein and TolB to coordinate cell membrane integrity and virulenceLeilei Wu0Xueyan Zhu1Hang Long2Xinyu Huang3Shuying Zhu4Qi Xue5Ziao Li6Huasong Zou7School of Life Sciences and Health, Huzhou College, Huzhou, Zhejiang, ChinaSchool of Life Sciences and Health, Huzhou College, Huzhou, Zhejiang, ChinaSchool of Life Sciences and Health, Huzhou College, Huzhou, Zhejiang, ChinaSchool of Life Sciences and Health, Huzhou College, Huzhou, Zhejiang, ChinaSchool of Life Sciences and Health, Huzhou College, Huzhou, Zhejiang, ChinaSchool of Life Sciences and Health, Huzhou College, Huzhou, Zhejiang, ChinaSchool of Life Sciences and Health, Huzhou College, Huzhou, Zhejiang, ChinaSchool of Life Sciences and Health, Huzhou College, Huzhou, Zhejiang, ChinaABSTRACT Xanthomonas citri subsp. citri (Xcc) possesses a Xanthomonas-specific outer membrane protein XAC1347 (OMPXan) that exerts a role in the expression of the type III secretion system for pathogenicity. In this study, we reported that OMPXan was required for salt stress tolerance and cell membrane integrity, as well as the expression of the gum genes for the production of extracellular polysaccharides. Pull-down and yeast two-hybrid assays revealed that OMPXan interacts with TolB, a substrate of the Tol/Pal membrane protein system. The deletion of tolB resulted in similar phenotypic alterations as the OMPXan mutant in salt stress tolerance, cell membrane integrity, and the expression of hrpG, hrpX, hrpD6, and hrcC for pathogenicity. In contrast, the absence of TolB resulted in an increased level of expression of the gum genes and the production of extracellular polysaccharides. These results indicate that the interaction of OMPXan and TolB coordinates multi-faceted mechanisms to manage environmental stress and pathogenicity.IMPORTANCEThe gram-negative Xanthomoas citri subsp. citri (Xcc) is a causal agent of citrus canker, a serious bacterial disease on citrus plants. Our previous research reported that a Xanthomonas-specific outer membrane protein XAC1347 (OMPXan) is necessary for type III gene expression. This manuscript provided evidence to show that OMPXan interacts with Tol/Pal system substrate TolB. Moreover, OMPXan and TolB are both required for cell membrane integrity, stress adaption, and virulence. The overall results support that OMPXan and TolB coordinate multi-faceted mechanisms to manage environmental stress and pathogenicity.https://journals.asm.org/doi/10.1128/spectrum.02521-24citrus cankerXanthomonasTolBouter membrane proteinTol/Palmembrane integrity
spellingShingle Leilei Wu
Xueyan Zhu
Hang Long
Xinyu Huang
Shuying Zhu
Qi Xue
Ziao Li
Huasong Zou
Xanthomonas citri subsp. citri requires a genus-specific outer membrane protein and TolB to coordinate cell membrane integrity and virulence
Microbiology Spectrum
citrus canker
Xanthomonas
TolB
outer membrane protein
Tol/Pal
membrane integrity
title Xanthomonas citri subsp. citri requires a genus-specific outer membrane protein and TolB to coordinate cell membrane integrity and virulence
title_full Xanthomonas citri subsp. citri requires a genus-specific outer membrane protein and TolB to coordinate cell membrane integrity and virulence
title_fullStr Xanthomonas citri subsp. citri requires a genus-specific outer membrane protein and TolB to coordinate cell membrane integrity and virulence
title_full_unstemmed Xanthomonas citri subsp. citri requires a genus-specific outer membrane protein and TolB to coordinate cell membrane integrity and virulence
title_short Xanthomonas citri subsp. citri requires a genus-specific outer membrane protein and TolB to coordinate cell membrane integrity and virulence
title_sort xanthomonas citri subsp citri requires a genus specific outer membrane protein and tolb to coordinate cell membrane integrity and virulence
topic citrus canker
Xanthomonas
TolB
outer membrane protein
Tol/Pal
membrane integrity
url https://journals.asm.org/doi/10.1128/spectrum.02521-24
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