The phoQ gene of Pseudomonas plecoglossicida influences the immune response in Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂ during infection

Pseudomonas plecoglossicida can cause visceral white spot disease in various species of teleost fish, leading to significant economic losses in the aquaculture industry. The PhoP/PhoQ two-component system plays a crucial role in regulating bacterial virulence and maintaining internal environmental b...

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Main Authors: Meiqin Mao, Li He, Xiangyang Lin, Jianshao Wu, Zhixia Zhuang, Xiaoru Wang, Huabin Huang, Qingpi Yan
Format: Article
Language:English
Published: Elsevier 2025-09-01
Series:Aquaculture Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2352513425002820
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author Meiqin Mao
Li He
Xiangyang Lin
Jianshao Wu
Zhixia Zhuang
Xiaoru Wang
Huabin Huang
Qingpi Yan
author_facet Meiqin Mao
Li He
Xiangyang Lin
Jianshao Wu
Zhixia Zhuang
Xiaoru Wang
Huabin Huang
Qingpi Yan
author_sort Meiqin Mao
collection DOAJ
description Pseudomonas plecoglossicida can cause visceral white spot disease in various species of teleost fish, leading to significant economic losses in the aquaculture industry. The PhoP/PhoQ two-component system plays a crucial role in regulating bacterial virulence and maintaining internal environmental balance. In this study, hybrid grouper (Epinephelus fuscoguttatus ♀ × E. lanceolatus ♂) was used as a model to compare the pathogenic differences between the phoQ gene knockout strain (ΔphoQ), the phoQ gene complement strain (C-ΔphoQ), and the wild-type strain (NZBD9). Additionally, transcriptome sequencing was employed to explore the impact of phoQ gene deletion on the host immune response during P. plecoglossicida infection. The results showed that the cumulative survival rate of the ΔphoQ infection group was 10 % higher than that of the NZBD9 group, with significantly reduced bacterial load in the spleen and less tissue damage. Transcriptomic analysis revealed that, compared to the NZBD9 infection group, the ΔphoQ infection group induced 4453 differentially expressed genes, which were enriched in several immune-related pathways according to GO and KEGG analysis. These pathways included 22 immune system pathways, 28 signal transduction pathways, and 9 cell growth and death pathways. Further qRT-PCR analysis confirmed that phoQ gene deletion affected the expression of several immune- and inflammation-related genes, such as IL-1β, IL-6, CD3, C8, CCL2, MHC-II, PGRP6, and SLP2. Particularly during the infection process, the expression level of the PGRP6 gene in the ΔphoQ strain infection group was significantly higher than that in the NZBD9 strain infection group, suggesting that PGRP6 may be involved in the host's immune recognition of P. plecoglossicida. In conclusion, the phoQ gene plays an important role in the pathogenesis of P. plecoglossicida infection in hybrid grouper. The deletion of the phoQ gene significantly affects the pathogenicity of P. plecoglossicida and enhances the host’s immune response, providing a theoretical basis for the potential application of the PhoP/PhoQ system in the immune defense of aquatic animals.
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spelling doaj-art-a83b8a9cb9cf4b64a42bf0656183c0aa2025-08-20T03:40:50ZengElsevierAquaculture Reports2352-51342025-09-014310289610.1016/j.aqrep.2025.102896The phoQ gene of Pseudomonas plecoglossicida influences the immune response in Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂ during infectionMeiqin Mao0Li He1Xiangyang Lin2Jianshao Wu3Zhixia Zhuang4Xiaoru Wang5Huabin Huang6Qingpi Yan7Fisheries College, Jimei University, Xiamen , Fujian 361021, ChinaFisheries College, Jimei University, Xiamen , Fujian 361021, ChinaFisheries Research Institute of Fujian, Xiamen, Fujian 361000, ChinaFisheries Research Institute of Fujian, Xiamen, Fujian 361000, ChinaCollege of Environment and Public Health, Xiamen Huaxia University, Xiamen , Fujian 361024, ChinaCollege of Environment and Public Health, Xiamen Huaxia University, Xiamen , Fujian 361024, ChinaCollege of Environment and Public Health, Xiamen Huaxia University, Xiamen , Fujian 361024, ChinaFisheries College, Jimei University, Xiamen , Fujian 361021, China; Corresponding author.Pseudomonas plecoglossicida can cause visceral white spot disease in various species of teleost fish, leading to significant economic losses in the aquaculture industry. The PhoP/PhoQ two-component system plays a crucial role in regulating bacterial virulence and maintaining internal environmental balance. In this study, hybrid grouper (Epinephelus fuscoguttatus ♀ × E. lanceolatus ♂) was used as a model to compare the pathogenic differences between the phoQ gene knockout strain (ΔphoQ), the phoQ gene complement strain (C-ΔphoQ), and the wild-type strain (NZBD9). Additionally, transcriptome sequencing was employed to explore the impact of phoQ gene deletion on the host immune response during P. plecoglossicida infection. The results showed that the cumulative survival rate of the ΔphoQ infection group was 10 % higher than that of the NZBD9 group, with significantly reduced bacterial load in the spleen and less tissue damage. Transcriptomic analysis revealed that, compared to the NZBD9 infection group, the ΔphoQ infection group induced 4453 differentially expressed genes, which were enriched in several immune-related pathways according to GO and KEGG analysis. These pathways included 22 immune system pathways, 28 signal transduction pathways, and 9 cell growth and death pathways. Further qRT-PCR analysis confirmed that phoQ gene deletion affected the expression of several immune- and inflammation-related genes, such as IL-1β, IL-6, CD3, C8, CCL2, MHC-II, PGRP6, and SLP2. Particularly during the infection process, the expression level of the PGRP6 gene in the ΔphoQ strain infection group was significantly higher than that in the NZBD9 strain infection group, suggesting that PGRP6 may be involved in the host's immune recognition of P. plecoglossicida. In conclusion, the phoQ gene plays an important role in the pathogenesis of P. plecoglossicida infection in hybrid grouper. The deletion of the phoQ gene significantly affects the pathogenicity of P. plecoglossicida and enhances the host’s immune response, providing a theoretical basis for the potential application of the PhoP/PhoQ system in the immune defense of aquatic animals.http://www.sciencedirect.com/science/article/pii/S2352513425002820Pseudomonas plecoglossicidaphoQHybrid grouperPathogenicityImmune response
spellingShingle Meiqin Mao
Li He
Xiangyang Lin
Jianshao Wu
Zhixia Zhuang
Xiaoru Wang
Huabin Huang
Qingpi Yan
The phoQ gene of Pseudomonas plecoglossicida influences the immune response in Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂ during infection
Aquaculture Reports
Pseudomonas plecoglossicida
phoQ
Hybrid grouper
Pathogenicity
Immune response
title The phoQ gene of Pseudomonas plecoglossicida influences the immune response in Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂ during infection
title_full The phoQ gene of Pseudomonas plecoglossicida influences the immune response in Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂ during infection
title_fullStr The phoQ gene of Pseudomonas plecoglossicida influences the immune response in Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂ during infection
title_full_unstemmed The phoQ gene of Pseudomonas plecoglossicida influences the immune response in Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂ during infection
title_short The phoQ gene of Pseudomonas plecoglossicida influences the immune response in Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂ during infection
title_sort phoq gene of pseudomonas plecoglossicida influences the immune response in epinephelus fuscoguttatus ♀ epinephelus lanceolatus ♂ during infection
topic Pseudomonas plecoglossicida
phoQ
Hybrid grouper
Pathogenicity
Immune response
url http://www.sciencedirect.com/science/article/pii/S2352513425002820
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