<italic toggle="yes">Pseudomonas savastanoi</italic> Two-Component System RhpRS Switches between Virulence and Metabolism by Tuning Phosphorylation State and Sensing Nutritional Conditions

ABSTRACT Pseudomonas savastanoi uses a type III secretion system (T3SS) to invade host plants. Our previous studies have demonstrated that a two-component system (TCS), RhpRS, enables P. savastanoi to coordinate the T3SS gene expression, which depends on the phosphorylation state of RhpR under diffe...

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Autores principales:	Yingpeng Xie, Xiaolong Shao, Yingchao Zhang, Jingui Liu, Tingting Wang, Weitong Zhang, Canfeng Hua, Xin Deng
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Pseudomonas savastanoi RhpRS T3SS two-component system Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5b631f3d22bc46469354f5680b632eca
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spelling	oai:doaj.org-article:5b631f3d22bc46469354f5680b632eca2021-11-15T15:55:25Z<italic toggle="yes">Pseudomonas savastanoi</italic> Two-Component System RhpRS Switches between Virulence and Metabolism by Tuning Phosphorylation State and Sensing Nutritional Conditions10.1128/mBio.02838-182150-7511https://doaj.org/article/5b631f3d22bc46469354f5680b632eca2019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02838-18https://doaj.org/toc/2150-7511ABSTRACT Pseudomonas savastanoi uses a type III secretion system (T3SS) to invade host plants. Our previous studies have demonstrated that a two-component system (TCS), RhpRS, enables P. savastanoi to coordinate the T3SS gene expression, which depends on the phosphorylation state of RhpR under different environmental conditions. Orthologues of RhpRS are distributed in a wide range of bacterial species, indicating a general regulatory mechanism. How RhpRS uses external signals and the phosphorylation state to exercise its regulatory functions remains unknown. We performed chromatin immunoprecipitation sequencing (ChIP-seq) assays to identify the specific binding sites of RhpR and RhpRD70A in either King’s B medium (KB [a T3SS-inhibiting medium]) or minimal medium (MM [a T3SS-inducing medium]). We identified 125 KB-dependent binding sites and 188 phosphorylation-dependent binding sites of RhpR. In KB, RhpR directly and positively regulated cytochrome c550 production (via ccmA) and alcohol dehydrogenase activity (via adhB) but negatively regulated anthranilate synthase activity (via trpG) and protease activity (via hemB). In addition, phosphorylated RhpR (RhpR-P) directly and negatively regulated the T3SS (via hrpR and hopR1), swimming motility (via flhA), c-di-GMP levels (via PSPPH_2590), and biofilm formation (via algD). It positively regulated twitching motility (via fimA) and lipopolysaccharide production (via PSPPH_2653). Our transcriptome sequencing (RNA-seq) analyses identified 474 and 840 new genes that were regulated by RhpR in KB and MM, respectively. We showed nutrient-rich conditions allowed RhpR to directly regulate multiple metabolic pathways of P. savastanoi and phosphorylation enabled RhpR to specifically control virulence and the cell envelope. The action of RhpRS switched between virulence and regulation of multiple metabolic pathways by tuning its phosphorylation and sensing environmental signals in KB, respectively. IMPORTANCE The plant pathogen Pseudomonas savastanoi invades host plants through a type III secretion system, which is strictly regulated by a two-component system called RhpRS. The orthologues of RhpRS are widely distributed in the bacterial kingdom. The master regulator RhpR specifically depends on the phosphorylation state to regulate the majority of the virulence-related genes. Under nutrient-rich conditions, it modulates many important metabolic pathways, which consist of one-fifth of the genome. We propose that RhpRS uses phosphorylation- and nutrition-dependent mechanisms to switch between regulating virulence and metabolism, and this functionality is widely conserved among bacterial species.Yingpeng XieXiaolong ShaoYingchao ZhangJingui LiuTingting WangWeitong ZhangCanfeng HuaXin DengAmerican Society for MicrobiologyarticlePseudomonas savastanoiRhpRST3SStwo-component systemMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Pseudomonas savastanoi RhpRS T3SS two-component system Microbiology QR1-502
spellingShingle	Pseudomonas savastanoi RhpRS T3SS two-component system Microbiology QR1-502 Yingpeng Xie Xiaolong Shao Yingchao Zhang Jingui Liu Tingting Wang Weitong Zhang Canfeng Hua Xin Deng <italic toggle="yes">Pseudomonas savastanoi</italic> Two-Component System RhpRS Switches between Virulence and Metabolism by Tuning Phosphorylation State and Sensing Nutritional Conditions
description	ABSTRACT Pseudomonas savastanoi uses a type III secretion system (T3SS) to invade host plants. Our previous studies have demonstrated that a two-component system (TCS), RhpRS, enables P. savastanoi to coordinate the T3SS gene expression, which depends on the phosphorylation state of RhpR under different environmental conditions. Orthologues of RhpRS are distributed in a wide range of bacterial species, indicating a general regulatory mechanism. How RhpRS uses external signals and the phosphorylation state to exercise its regulatory functions remains unknown. We performed chromatin immunoprecipitation sequencing (ChIP-seq) assays to identify the specific binding sites of RhpR and RhpRD70A in either King’s B medium (KB [a T3SS-inhibiting medium]) or minimal medium (MM [a T3SS-inducing medium]). We identified 125 KB-dependent binding sites and 188 phosphorylation-dependent binding sites of RhpR. In KB, RhpR directly and positively regulated cytochrome c550 production (via ccmA) and alcohol dehydrogenase activity (via adhB) but negatively regulated anthranilate synthase activity (via trpG) and protease activity (via hemB). In addition, phosphorylated RhpR (RhpR-P) directly and negatively regulated the T3SS (via hrpR and hopR1), swimming motility (via flhA), c-di-GMP levels (via PSPPH_2590), and biofilm formation (via algD). It positively regulated twitching motility (via fimA) and lipopolysaccharide production (via PSPPH_2653). Our transcriptome sequencing (RNA-seq) analyses identified 474 and 840 new genes that were regulated by RhpR in KB and MM, respectively. We showed nutrient-rich conditions allowed RhpR to directly regulate multiple metabolic pathways of P. savastanoi and phosphorylation enabled RhpR to specifically control virulence and the cell envelope. The action of RhpRS switched between virulence and regulation of multiple metabolic pathways by tuning its phosphorylation and sensing environmental signals in KB, respectively. IMPORTANCE The plant pathogen Pseudomonas savastanoi invades host plants through a type III secretion system, which is strictly regulated by a two-component system called RhpRS. The orthologues of RhpRS are widely distributed in the bacterial kingdom. The master regulator RhpR specifically depends on the phosphorylation state to regulate the majority of the virulence-related genes. Under nutrient-rich conditions, it modulates many important metabolic pathways, which consist of one-fifth of the genome. We propose that RhpRS uses phosphorylation- and nutrition-dependent mechanisms to switch between regulating virulence and metabolism, and this functionality is widely conserved among bacterial species.
format	article
author	Yingpeng Xie Xiaolong Shao Yingchao Zhang Jingui Liu Tingting Wang Weitong Zhang Canfeng Hua Xin Deng
author_facet	Yingpeng Xie Xiaolong Shao Yingchao Zhang Jingui Liu Tingting Wang Weitong Zhang Canfeng Hua Xin Deng
author_sort	Yingpeng Xie
title	<italic toggle="yes">Pseudomonas savastanoi</italic> Two-Component System RhpRS Switches between Virulence and Metabolism by Tuning Phosphorylation State and Sensing Nutritional Conditions
title_short	<italic toggle="yes">Pseudomonas savastanoi</italic> Two-Component System RhpRS Switches between Virulence and Metabolism by Tuning Phosphorylation State and Sensing Nutritional Conditions
title_full	<italic toggle="yes">Pseudomonas savastanoi</italic> Two-Component System RhpRS Switches between Virulence and Metabolism by Tuning Phosphorylation State and Sensing Nutritional Conditions
title_fullStr	<italic toggle="yes">Pseudomonas savastanoi</italic> Two-Component System RhpRS Switches between Virulence and Metabolism by Tuning Phosphorylation State and Sensing Nutritional Conditions
title_full_unstemmed	<italic toggle="yes">Pseudomonas savastanoi</italic> Two-Component System RhpRS Switches between Virulence and Metabolism by Tuning Phosphorylation State and Sensing Nutritional Conditions
title_sort	<italic toggle="yes">pseudomonas savastanoi</italic> two-component system rhprs switches between virulence and metabolism by tuning phosphorylation state and sensing nutritional conditions
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/5b631f3d22bc46469354f5680b632eca
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<italic toggle="yes">Pseudomonas savastanoi</italic> Two-Component System RhpRS Switches between Virulence and Metabolism by Tuning Phosphorylation State and Sensing Nutritional Conditions

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