Fur functions as an activator of T6SS-mediated bacterial dominance and virulence in Aeromonas hydrophila

Aeromonas hydrophila, a ubiquitous bacterium in aquatic habitats with broad host ranges, has earned the nickname of a ‘Jack-of-all-trades’. However, there is still a limited understanding of the mechanism of how this bacterium fit the competition with other species in dynamic surroundings. The type...

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Main Authors: Jihong Li, Zhihao Wu, Yuting Hou, Yong-An Zhang, Yang Zhou
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.1099611/full
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author Jihong Li
Jihong Li
Jihong Li
Jihong Li
Zhihao Wu
Yuting Hou
Yong-An Zhang
Yong-An Zhang
Yong-An Zhang
Yong-An Zhang
Yong-An Zhang
Yang Zhou
Yang Zhou
Yang Zhou
Yang Zhou
Yang Zhou
author_facet Jihong Li
Jihong Li
Jihong Li
Jihong Li
Zhihao Wu
Yuting Hou
Yong-An Zhang
Yong-An Zhang
Yong-An Zhang
Yong-An Zhang
Yong-An Zhang
Yang Zhou
Yang Zhou
Yang Zhou
Yang Zhou
Yang Zhou
author_sort Jihong Li
collection DOAJ
description Aeromonas hydrophila, a ubiquitous bacterium in aquatic habitats with broad host ranges, has earned the nickname of a ‘Jack-of-all-trades’. However, there is still a limited understanding of the mechanism of how this bacterium fit the competition with other species in dynamic surroundings. The type VI secretion system (T6SS) is macromolecular machinery found in Gram-negative bacteria’s cell envelope that is responsible for bacterial killing and/or pathogenicity toward different host cells. In this study, the depression of A. hydrophila T6SS under iron-limiting conditions was detected. The ferric uptake regulator (Fur) was then found to act as an activator of T6SS by directly binding to the Fur box region in vipA promoter in the T6SS gene cluster. The transcription of vipA was repressed in Δfur. Moreover, the inactivation of Fur resulted in considerable defects in the interbacterial competition activity and pathogenicity of A. hydrophila in vitro and in vivo. These findings provide the first direct evidence that Fur positively regulates the expression and functional activity of T6SS in Gram-negative bacteria and will help to understand the fascinating mechanism of competitive advantage for A. hydrophila in different ecological niches.
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spelling doaj.art-174b5390a04946129edf19d387eed1b12023-02-08T05:02:32ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-02-011310.3389/fmicb.2022.10996111099611Fur functions as an activator of T6SS-mediated bacterial dominance and virulence in Aeromonas hydrophilaJihong Li0Jihong Li1Jihong Li2Jihong Li3Zhihao Wu4Yuting Hou5Yong-An Zhang6Yong-An Zhang7Yong-An Zhang8Yong-An Zhang9Yong-An Zhang10Yang Zhou11Yang Zhou12Yang Zhou13Yang Zhou14Yang Zhou15State Key Laboratory of Agricultural Microbiology, College of Fisheries, Huazhong Agricultural University, Wuhan, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, ChinaDepartment of Microbiology and Immunology, Medical College, China Three Gorges University, Yichang, ChinaShenzhen Institute of Nutrition and Health, Huazhong Agricultural University, Wuhan, ChinaState Key Laboratory of Agricultural Microbiology, College of Fisheries, Huazhong Agricultural University, Wuhan, ChinaState Key Laboratory of Agricultural Microbiology, College of Fisheries, Huazhong Agricultural University, Wuhan, ChinaState Key Laboratory of Agricultural Microbiology, College of Fisheries, Huazhong Agricultural University, Wuhan, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, ChinaHubei Hongshan Laboratory, Wuhan, ChinaLaboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaEngineering Research Center of Green Development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, Wuhan, ChinaState Key Laboratory of Agricultural Microbiology, College of Fisheries, Huazhong Agricultural University, Wuhan, ChinaGuangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, ChinaShenzhen Institute of Nutrition and Health, Huazhong Agricultural University, Wuhan, ChinaEngineering Research Center of Green Development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, Wuhan, ChinaShenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, ChinaAeromonas hydrophila, a ubiquitous bacterium in aquatic habitats with broad host ranges, has earned the nickname of a ‘Jack-of-all-trades’. However, there is still a limited understanding of the mechanism of how this bacterium fit the competition with other species in dynamic surroundings. The type VI secretion system (T6SS) is macromolecular machinery found in Gram-negative bacteria’s cell envelope that is responsible for bacterial killing and/or pathogenicity toward different host cells. In this study, the depression of A. hydrophila T6SS under iron-limiting conditions was detected. The ferric uptake regulator (Fur) was then found to act as an activator of T6SS by directly binding to the Fur box region in vipA promoter in the T6SS gene cluster. The transcription of vipA was repressed in Δfur. Moreover, the inactivation of Fur resulted in considerable defects in the interbacterial competition activity and pathogenicity of A. hydrophila in vitro and in vivo. These findings provide the first direct evidence that Fur positively regulates the expression and functional activity of T6SS in Gram-negative bacteria and will help to understand the fascinating mechanism of competitive advantage for A. hydrophila in different ecological niches.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1099611/fullAeromonas hydrophilaT6SSfurpathogenesisinterbacterial competition activity
spellingShingle Jihong Li
Jihong Li
Jihong Li
Jihong Li
Zhihao Wu
Yuting Hou
Yong-An Zhang
Yong-An Zhang
Yong-An Zhang
Yong-An Zhang
Yong-An Zhang
Yang Zhou
Yang Zhou
Yang Zhou
Yang Zhou
Yang Zhou
Fur functions as an activator of T6SS-mediated bacterial dominance and virulence in Aeromonas hydrophila
Frontiers in Microbiology
Aeromonas hydrophila
T6SS
fur
pathogenesis
interbacterial competition activity
title Fur functions as an activator of T6SS-mediated bacterial dominance and virulence in Aeromonas hydrophila
title_full Fur functions as an activator of T6SS-mediated bacterial dominance and virulence in Aeromonas hydrophila
title_fullStr Fur functions as an activator of T6SS-mediated bacterial dominance and virulence in Aeromonas hydrophila
title_full_unstemmed Fur functions as an activator of T6SS-mediated bacterial dominance and virulence in Aeromonas hydrophila
title_short Fur functions as an activator of T6SS-mediated bacterial dominance and virulence in Aeromonas hydrophila
title_sort fur functions as an activator of t6ss mediated bacterial dominance and virulence in aeromonas hydrophila
topic Aeromonas hydrophila
T6SS
fur
pathogenesis
interbacterial competition activity
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.1099611/full
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