ZrgA contributes to zinc acquisition in Vibrio parahaemolyticus

ABSTRACT Metals are nutrients essential for almost all lifeforms. Bacteria have evolved several mechanisms to overcome the metal restrictions imposed by the host. Vibrio parahaemolyticus causes severe threats to public health and significant economic losses in shrimp aquaculture. Herein, we report t...

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Main Authors: Chengkun Zheng, Jun Qiu, Yimeng Zhai, Man Wei, Xiaohui Zhou, Xinan Jiao
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:Virulence
Subjects:
Online Access:https://www.tandfonline.com/doi/10.1080/21505594.2022.2156196
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author Chengkun Zheng
Jun Qiu
Yimeng Zhai
Man Wei
Xiaohui Zhou
Xinan Jiao
author_facet Chengkun Zheng
Jun Qiu
Yimeng Zhai
Man Wei
Xiaohui Zhou
Xinan Jiao
author_sort Chengkun Zheng
collection DOAJ
description ABSTRACT Metals are nutrients essential for almost all lifeforms. Bacteria have evolved several mechanisms to overcome the metal restrictions imposed by the host. Vibrio parahaemolyticus causes severe threats to public health and significant economic losses in shrimp aquaculture. Herein, we report that ZrgA contributes to zinc acquisition in this pathogen. The operon VP_RS01455 to VP_RS01475 of V. parahaemolyticus encodes the putative Zn transporter ZrgABCDE, whose homologs are widely distributed in Vibrionaceae. RNA sequencing analysis revealed that V. parahaemolyticus modulates the transcriptome in response to Zn limitation. Genes in the Zinc uptake regulator (Zur) regulon are upregulated during Zn limitation, including three genes annotated to encode Zn-binding proteins. Significant upregulation of these three genes during Zn limitation was also confirmed by quantitative real-time PCR (qRT-PCR) analysis. However, only the mutants containing a VP_RS01470 (zrgA) deletion exhibited impaired growth under Zn-deficient conditions, indicating that VP_RS01470 plays the predominant role in V. parahaemolyticus Zn acquisition. The VP_RS01470 deletion mutant displayed a false appearance of decreased swimming motility under Zn-deficient conditions, as revealed by the fact that the polar flagellar-related genes were not downregulated in the mutant. Moreover, VP_RS01470 deletion produced no noticeable impact on the swarming motility and virulence in mice. qRT-PCR analysis and β-galactosidase activity assays indicated that Zur negatively regulates VP_RS01470 expression in V. parahaemolyticus. Collectively, our findings suggest that ZrgA is required for Zn acquisition in V. parahaemolyticus and highlight the importance of detecting the expression of flagellar genes during analysis of motility of a mutant deficient in growth.
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spelling doaj.art-667ed81802504e939cd3551d78094aec2024-01-03T17:26:57ZengTaylor & Francis GroupVirulence2150-55942150-56082023-12-0114110.1080/21505594.2022.2156196ZrgA contributes to zinc acquisition in Vibrio parahaemolyticusChengkun Zheng0Jun Qiu1Yimeng Zhai2Man Wei3Xiaohui Zhou4Xinan Jiao5Jiangsu Key Laboratory of Zoonosis, Yangzhou University, Yangzhou, ChinaJiangsu Key Laboratory of Zoonosis, Yangzhou University, Yangzhou, ChinaJiangsu Key Laboratory of Zoonosis, Yangzhou University, Yangzhou, ChinaJiangsu Key Laboratory of Zoonosis, Yangzhou University, Yangzhou, ChinaSchool of Public Health and Emergency Management, Southern University of Science and Technology, Shenzhen, P.R. ChinaJiangsu Key Laboratory of Zoonosis, Yangzhou University, Yangzhou, ChinaABSTRACT Metals are nutrients essential for almost all lifeforms. Bacteria have evolved several mechanisms to overcome the metal restrictions imposed by the host. Vibrio parahaemolyticus causes severe threats to public health and significant economic losses in shrimp aquaculture. Herein, we report that ZrgA contributes to zinc acquisition in this pathogen. The operon VP_RS01455 to VP_RS01475 of V. parahaemolyticus encodes the putative Zn transporter ZrgABCDE, whose homologs are widely distributed in Vibrionaceae. RNA sequencing analysis revealed that V. parahaemolyticus modulates the transcriptome in response to Zn limitation. Genes in the Zinc uptake regulator (Zur) regulon are upregulated during Zn limitation, including three genes annotated to encode Zn-binding proteins. Significant upregulation of these three genes during Zn limitation was also confirmed by quantitative real-time PCR (qRT-PCR) analysis. However, only the mutants containing a VP_RS01470 (zrgA) deletion exhibited impaired growth under Zn-deficient conditions, indicating that VP_RS01470 plays the predominant role in V. parahaemolyticus Zn acquisition. The VP_RS01470 deletion mutant displayed a false appearance of decreased swimming motility under Zn-deficient conditions, as revealed by the fact that the polar flagellar-related genes were not downregulated in the mutant. Moreover, VP_RS01470 deletion produced no noticeable impact on the swarming motility and virulence in mice. qRT-PCR analysis and β-galactosidase activity assays indicated that Zur negatively regulates VP_RS01470 expression in V. parahaemolyticus. Collectively, our findings suggest that ZrgA is required for Zn acquisition in V. parahaemolyticus and highlight the importance of detecting the expression of flagellar genes during analysis of motility of a mutant deficient in growth.https://www.tandfonline.com/doi/10.1080/21505594.2022.2156196Vibrio parahaemolyticuszinc acquisitionZrgAZurmotilityvirulence
spellingShingle Chengkun Zheng
Jun Qiu
Yimeng Zhai
Man Wei
Xiaohui Zhou
Xinan Jiao
ZrgA contributes to zinc acquisition in Vibrio parahaemolyticus
Virulence
Vibrio parahaemolyticus
zinc acquisition
ZrgA
Zur
motility
virulence
title ZrgA contributes to zinc acquisition in Vibrio parahaemolyticus
title_full ZrgA contributes to zinc acquisition in Vibrio parahaemolyticus
title_fullStr ZrgA contributes to zinc acquisition in Vibrio parahaemolyticus
title_full_unstemmed ZrgA contributes to zinc acquisition in Vibrio parahaemolyticus
title_short ZrgA contributes to zinc acquisition in Vibrio parahaemolyticus
title_sort zrga contributes to zinc acquisition in vibrio parahaemolyticus
topic Vibrio parahaemolyticus
zinc acquisition
ZrgA
Zur
motility
virulence
url https://www.tandfonline.com/doi/10.1080/21505594.2022.2156196
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