Lumpfish (Cyclopterus lumpus) Is Susceptible to Renibacterium salmoninarum Infection and Induces Cell-Mediated Immunity in the Chronic Stage

Renibacterium salmoninarum is a Gram-positive, intracellular pathogen that causes Bacterial Kidney Disease (BKD) in several fish species in freshwater and seawater. Lumpfish (Cyclopterus lumpus) is utilized as a cleaner fish to biocontrol sea lice infestation in Atlantic salmon (Salmo salar) farms....

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Autores principales:	Hajarooba Gnanagobal, Trung Cao, Ahmed Hossain, My Dang, Jennifer R. Hall, Surendra Kumar, Doan Van Cuong, Danny Boyce, Javier Santander
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	Bacterial Kidney Disease (BKD) Gram-positive pathogen Renibacterium salmoninarum lumpfish cell-mediated immunity Immunologic diseases. Allergy RC581-607
Acceso en línea:	https://doaj.org/article/3cb1cc0bea4942279e889f55bf5f1658
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spelling	oai:doaj.org-article:3cb1cc0bea4942279e889f55bf5f16582021-11-22T06:31:14ZLumpfish (Cyclopterus lumpus) Is Susceptible to Renibacterium salmoninarum Infection and Induces Cell-Mediated Immunity in the Chronic Stage1664-322410.3389/fimmu.2021.733266https://doaj.org/article/3cb1cc0bea4942279e889f55bf5f16582021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fimmu.2021.733266/fullhttps://doaj.org/toc/1664-3224Renibacterium salmoninarum is a Gram-positive, intracellular pathogen that causes Bacterial Kidney Disease (BKD) in several fish species in freshwater and seawater. Lumpfish (Cyclopterus lumpus) is utilized as a cleaner fish to biocontrol sea lice infestation in Atlantic salmon (Salmo salar) farms. Atlantic salmon is susceptible to R. salmoninarum, and it can transfer the infection to other fish species. Although BKD outbreaks have not been reported in lumpfish, its susceptibility and immune response to R. salmoninarum is unknown. In this study, we evaluated the susceptibility and immune response of lumpfish to R. salmoninarum infection. Groups of lumpfish were intraperitoneally (i.p.) injected with either R. salmoninarum (1×107, 1×108, or 1×109 cells dose-1) or PBS (control). R. salmoninarum infection kinetics and mortality were followed for 98 days post-infection (dpi). Transcript expression levels of 33 immune-relevant genes were measured in head kidney (n = 6) of fish infected with 1×109 cells/dose and compared to the control at 28 and 98 dpi. Infected lumpfish displayed characteristic clinical signs of BKD. Lumpfish infected with high, medium, and low doses had a survival rate of 65%, 93%, and 95%, respectively. Mortality in the high-dose infected group stabilized after 50 dpi, but R. salmoninarum persisted in the fish tissues until 98 dpi. Cytokines (il1β, il8a, il8b), pattern recognition receptors (tlr5a), interferon-induced effectors (rsad2, mxa, mxb, mxc), and iron regulation (hamp) and acute phase reactant (saa5) related genes were up-regulated at 28 dpi. In contrast, cell-mediated adaptive immunity-related genes (cd4a, cd4b, ly6g6f, cd8a, cd74) were down-regulated at 28 dpi, revealing the immune suppressive nature of R. salmoninarum. However, significant upregulation of cd74 at 98 dpi suggests induction of cell-mediated immune response. This study showed that R. salmoninarum infected lumpfish in a similar fashion to salmonid fish species and caused a chronic infection, enhancing cell-mediated adaptive immune response.Hajarooba GnanagobalHajarooba GnanagobalTrung CaoAhmed HossainMy DangJennifer R. HallSurendra KumarSurendra KumarDoan Van CuongDanny BoyceJavier SantanderFrontiers Media S.A.articleBacterial Kidney Disease (BKD)Gram-positive pathogenRenibacterium salmoninarumlumpfishcell-mediated immunityImmunologic diseases. AllergyRC581-607ENFrontiers in Immunology, Vol 12 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bacterial Kidney Disease (BKD) Gram-positive pathogen Renibacterium salmoninarum lumpfish cell-mediated immunity Immunologic diseases. Allergy RC581-607
spellingShingle	Bacterial Kidney Disease (BKD) Gram-positive pathogen Renibacterium salmoninarum lumpfish cell-mediated immunity Immunologic diseases. Allergy RC581-607 Hajarooba Gnanagobal Hajarooba Gnanagobal Trung Cao Ahmed Hossain My Dang Jennifer R. Hall Surendra Kumar Surendra Kumar Doan Van Cuong Danny Boyce Javier Santander Lumpfish (Cyclopterus lumpus) Is Susceptible to Renibacterium salmoninarum Infection and Induces Cell-Mediated Immunity in the Chronic Stage
description	Renibacterium salmoninarum is a Gram-positive, intracellular pathogen that causes Bacterial Kidney Disease (BKD) in several fish species in freshwater and seawater. Lumpfish (Cyclopterus lumpus) is utilized as a cleaner fish to biocontrol sea lice infestation in Atlantic salmon (Salmo salar) farms. Atlantic salmon is susceptible to R. salmoninarum, and it can transfer the infection to other fish species. Although BKD outbreaks have not been reported in lumpfish, its susceptibility and immune response to R. salmoninarum is unknown. In this study, we evaluated the susceptibility and immune response of lumpfish to R. salmoninarum infection. Groups of lumpfish were intraperitoneally (i.p.) injected with either R. salmoninarum (1×107, 1×108, or 1×109 cells dose-1) or PBS (control). R. salmoninarum infection kinetics and mortality were followed for 98 days post-infection (dpi). Transcript expression levels of 33 immune-relevant genes were measured in head kidney (n = 6) of fish infected with 1×109 cells/dose and compared to the control at 28 and 98 dpi. Infected lumpfish displayed characteristic clinical signs of BKD. Lumpfish infected with high, medium, and low doses had a survival rate of 65%, 93%, and 95%, respectively. Mortality in the high-dose infected group stabilized after 50 dpi, but R. salmoninarum persisted in the fish tissues until 98 dpi. Cytokines (il1β, il8a, il8b), pattern recognition receptors (tlr5a), interferon-induced effectors (rsad2, mxa, mxb, mxc), and iron regulation (hamp) and acute phase reactant (saa5) related genes were up-regulated at 28 dpi. In contrast, cell-mediated adaptive immunity-related genes (cd4a, cd4b, ly6g6f, cd8a, cd74) were down-regulated at 28 dpi, revealing the immune suppressive nature of R. salmoninarum. However, significant upregulation of cd74 at 98 dpi suggests induction of cell-mediated immune response. This study showed that R. salmoninarum infected lumpfish in a similar fashion to salmonid fish species and caused a chronic infection, enhancing cell-mediated adaptive immune response.
format	article
author	Hajarooba Gnanagobal Hajarooba Gnanagobal Trung Cao Ahmed Hossain My Dang Jennifer R. Hall Surendra Kumar Surendra Kumar Doan Van Cuong Danny Boyce Javier Santander
author_facet	Hajarooba Gnanagobal Hajarooba Gnanagobal Trung Cao Ahmed Hossain My Dang Jennifer R. Hall Surendra Kumar Surendra Kumar Doan Van Cuong Danny Boyce Javier Santander
author_sort	Hajarooba Gnanagobal
title	Lumpfish (Cyclopterus lumpus) Is Susceptible to Renibacterium salmoninarum Infection and Induces Cell-Mediated Immunity in the Chronic Stage
title_short	Lumpfish (Cyclopterus lumpus) Is Susceptible to Renibacterium salmoninarum Infection and Induces Cell-Mediated Immunity in the Chronic Stage
title_full	Lumpfish (Cyclopterus lumpus) Is Susceptible to Renibacterium salmoninarum Infection and Induces Cell-Mediated Immunity in the Chronic Stage
title_fullStr	Lumpfish (Cyclopterus lumpus) Is Susceptible to Renibacterium salmoninarum Infection and Induces Cell-Mediated Immunity in the Chronic Stage
title_full_unstemmed	Lumpfish (Cyclopterus lumpus) Is Susceptible to Renibacterium salmoninarum Infection and Induces Cell-Mediated Immunity in the Chronic Stage
title_sort	lumpfish (cyclopterus lumpus) is susceptible to renibacterium salmoninarum infection and induces cell-mediated immunity in the chronic stage
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/3cb1cc0bea4942279e889f55bf5f1658
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Lumpfish (Cyclopterus lumpus) Is Susceptible to Renibacterium salmoninarum Infection and Induces Cell-Mediated Immunity in the Chronic Stage

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