A putative multi-sensor hybrid histidine kinase, BarAAc, inhibits the expression of the type III secretion system regulator HrpG in Acidovorax citrulli

Bacterial fruit blotch (BFB), caused by Acidovorax citrulli, severely damages watermelon, melon, and other cucurbit crops worldwide. Although many virulence determinants have been identified in A. citrulli, including swimming motility, twitching motility, biofilm formation, and the type III secretio...

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Main Authors: Pei Qiao, Mei Zhao, Wei Guan, Ron Walcott, Yunfeng Ye, Yuwen Yang, Tingchang Zhao
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.1064577/full
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author Pei Qiao
Mei Zhao
Mei Zhao
Wei Guan
Ron Walcott
Yunfeng Ye
Yuwen Yang
Tingchang Zhao
author_facet Pei Qiao
Mei Zhao
Mei Zhao
Wei Guan
Ron Walcott
Yunfeng Ye
Yuwen Yang
Tingchang Zhao
author_sort Pei Qiao
collection DOAJ
description Bacterial fruit blotch (BFB), caused by Acidovorax citrulli, severely damages watermelon, melon, and other cucurbit crops worldwide. Although many virulence determinants have been identified in A. citrulli, including swimming motility, twitching motility, biofilm formation, and the type III secretion system (T3SS), research on their regulation is lacking. To study virulence regulation mechanisms, we found a putative histidine kinase BarAAc that may be related to the T3SS regulator HrpG in A. citrulli. We deleted and characterized barAAc (Aave_2063) in A. citrulli Aac5 strain. Compared to the wild-type Aac5, virulence and early proliferation of barAAc mutant in host watermelon cotyledons were significantly increased, and induction of hypersensitive response in non-host tobacco was accelerated, while biofilm formation and swimming motility were significantly reduced. In addition, the transcriptomic analysis revealed that the expression of many T3SS-related genes was upregulated in the ΔbarAAc deletion mutant when cultured in KB medium. Meanwhile, the ΔbarAAc deletion mutant showed increased accumulation of the T3SS regulator HrpG in KB medium, which may account for the increased deployment of T3SS. This suggests that the putative histidine kinase BarAAc is able to repress the T3SS expression by inhibiting HrpG in the KB medium, which appears to be important for rational energy allocation. In summary, our research provides further understanding of the regulatory network of A. citrulli virulence.
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spelling doaj.art-b2e92e983561467386cac4d171416d262022-12-22T03:46:49ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-11-011310.3389/fmicb.2022.10645771064577A putative multi-sensor hybrid histidine kinase, BarAAc, inhibits the expression of the type III secretion system regulator HrpG in Acidovorax citrulliPei Qiao0Mei Zhao1Mei Zhao2Wei Guan3Ron Walcott4Yunfeng Ye5Yuwen Yang6Tingchang Zhao7State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, ChinaDepartment of Plant Pathology, College of Plant Protection, China Agricultural University, Beijing, ChinaDepartment of Plant Pathology, University of Georgia, Athens, GA, United StatesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, ChinaDepartment of Plant Pathology, University of Georgia, Athens, GA, United StatesHorticultural Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, ChinaState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, ChinaBacterial fruit blotch (BFB), caused by Acidovorax citrulli, severely damages watermelon, melon, and other cucurbit crops worldwide. Although many virulence determinants have been identified in A. citrulli, including swimming motility, twitching motility, biofilm formation, and the type III secretion system (T3SS), research on their regulation is lacking. To study virulence regulation mechanisms, we found a putative histidine kinase BarAAc that may be related to the T3SS regulator HrpG in A. citrulli. We deleted and characterized barAAc (Aave_2063) in A. citrulli Aac5 strain. Compared to the wild-type Aac5, virulence and early proliferation of barAAc mutant in host watermelon cotyledons were significantly increased, and induction of hypersensitive response in non-host tobacco was accelerated, while biofilm formation and swimming motility were significantly reduced. In addition, the transcriptomic analysis revealed that the expression of many T3SS-related genes was upregulated in the ΔbarAAc deletion mutant when cultured in KB medium. Meanwhile, the ΔbarAAc deletion mutant showed increased accumulation of the T3SS regulator HrpG in KB medium, which may account for the increased deployment of T3SS. This suggests that the putative histidine kinase BarAAc is able to repress the T3SS expression by inhibiting HrpG in the KB medium, which appears to be important for rational energy allocation. In summary, our research provides further understanding of the regulatory network of A. citrulli virulence.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1064577/fullbarAAcvirulenceHrpGregulationT3SSexpression
spellingShingle Pei Qiao
Mei Zhao
Mei Zhao
Wei Guan
Ron Walcott
Yunfeng Ye
Yuwen Yang
Tingchang Zhao
A putative multi-sensor hybrid histidine kinase, BarAAc, inhibits the expression of the type III secretion system regulator HrpG in Acidovorax citrulli
Frontiers in Microbiology
barAAc
virulence
HrpG
regulation
T3SS
expression
title A putative multi-sensor hybrid histidine kinase, BarAAc, inhibits the expression of the type III secretion system regulator HrpG in Acidovorax citrulli
title_full A putative multi-sensor hybrid histidine kinase, BarAAc, inhibits the expression of the type III secretion system regulator HrpG in Acidovorax citrulli
title_fullStr A putative multi-sensor hybrid histidine kinase, BarAAc, inhibits the expression of the type III secretion system regulator HrpG in Acidovorax citrulli
title_full_unstemmed A putative multi-sensor hybrid histidine kinase, BarAAc, inhibits the expression of the type III secretion system regulator HrpG in Acidovorax citrulli
title_short A putative multi-sensor hybrid histidine kinase, BarAAc, inhibits the expression of the type III secretion system regulator HrpG in Acidovorax citrulli
title_sort putative multi sensor hybrid histidine kinase baraac inhibits the expression of the type iii secretion system regulator hrpg in acidovorax citrulli
topic barAAc
virulence
HrpG
regulation
T3SS
expression
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.1064577/full
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