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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Format: | Article |
Language: | English |
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Taylor & Francis Group
2023-12-01
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Series: | Virulence |
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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. |
first_indexed | 2024-03-08T17:13:50Z |
format | Article |
id | doaj.art-667ed81802504e939cd3551d78094aec |
institution | Directory Open Access Journal |
issn | 2150-5594 2150-5608 |
language | English |
last_indexed | 2024-03-08T17:13:50Z |
publishDate | 2023-12-01 |
publisher | Taylor & Francis Group |
record_format | Article |
series | Virulence |
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 |
work_keys_str_mv | AT chengkunzheng zrgacontributestozincacquisitioninvibrioparahaemolyticus AT junqiu zrgacontributestozincacquisitioninvibrioparahaemolyticus AT yimengzhai zrgacontributestozincacquisitioninvibrioparahaemolyticus AT manwei zrgacontributestozincacquisitioninvibrioparahaemolyticus AT xiaohuizhou zrgacontributestozincacquisitioninvibrioparahaemolyticus AT xinanjiao zrgacontributestozincacquisitioninvibrioparahaemolyticus |