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Transcriptome Analysis of Atlantic Salmon (Salmo salar) Skin in Response to Sea Lice and Infectious Salmon Anemia Virus Co-Infection Under Different Experimental Functional Diets

Sea lice (Lepeophtheirus salmonis) are ectoparasitic copepods that cause significant economic loss in marine salmoniculture. In commercial salmon farms, infestation with sea lice can enhance susceptibility to other significant pathogens, such as the highly contagious infectious salmon anemia virus (...

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Autores principales: Cai, Wenlong, Kumar, Surendra, Navaneethaiyer, Umasuthan, Caballero-Solares, Albert, Carvalho, Laura A., Whyte, Shona K., Purcell, Sara L., Gagne, Nellie, Hori, Tiago S., Allen, Melissa, Taylor, Richard G., Balder, Rachel, Parrish, Christopher C., Rise, Matthew L., Fast, Mark D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8763012/
https://www.ncbi.nlm.nih.gov/pubmed/35046944
http://dx.doi.org/10.3389/fimmu.2021.787033
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author Cai, Wenlong
Kumar, Surendra
Navaneethaiyer, Umasuthan
Caballero-Solares, Albert
Carvalho, Laura A.
Whyte, Shona K.
Purcell, Sara L.
Gagne, Nellie
Hori, Tiago S.
Allen, Melissa
Taylor, Richard G.
Balder, Rachel
Parrish, Christopher C.
Rise, Matthew L.
Fast, Mark D.
author_facet Cai, Wenlong
Kumar, Surendra
Navaneethaiyer, Umasuthan
Caballero-Solares, Albert
Carvalho, Laura A.
Whyte, Shona K.
Purcell, Sara L.
Gagne, Nellie
Hori, Tiago S.
Allen, Melissa
Taylor, Richard G.
Balder, Rachel
Parrish, Christopher C.
Rise, Matthew L.
Fast, Mark D.
author_sort Cai, Wenlong
collection PubMed
description Sea lice (Lepeophtheirus salmonis) are ectoparasitic copepods that cause significant economic loss in marine salmoniculture. In commercial salmon farms, infestation with sea lice can enhance susceptibility to other significant pathogens, such as the highly contagious infectious salmon anemia virus (ISAv). In this study, transcriptomic analysis was used to evaluate the impact of four experimental functional feeds (i.e. 0.3% EPA/DHA+high-ω6, 0.3% EPA/DHA+high-ω6+immunostimulant (IS), 1% EPA/DHA+high-ω6, and 1% EPA/DHA+high-ω3) on Atlantic salmon (Salmo salar) during a single infection with sea lice (L. salmonis) and a co-infection with sea lice and ISAv. The overall objectives were to compare the transcriptomic profiles of skin between lice infection alone with co-infection groups and assess differences in gene expression response among animals with different experimental diets. Atlantic salmon smolts were challenged with L. salmonis following a 28-day feeding trial. Fish were then challenged with ISAv at 18 days post-sea lice infection (dpi), and maintained on individual diets, to establish a co-infection model. Skin tissues sampled at 33 dpi were subjected to RNA-seq analysis. The co-infection’s overall survival rates were between 37%-50%, while no mortality was observed in the single infection with lice. With regard to the infection status, 756 and 1303 consensus differentially expressed genes (DEGs) among the four diets were identified in “lice infection vs. pre-infection” and “co-infection vs. pre-infection” groups, respectively, that were shared between the four experimental diets. The co-infection groups (co-infection vs. pre-infection) included up-regulated genes associated with glycolysis, the interferon pathway, complement cascade activity, and heat shock protein family, while the down-regulated genes were related to antigen presentation and processing, T-cell activation, collagen formation, and extracellular matrix. Pathway enrichment analysis conducted between infected groups (lice infection vs. co-infection) resulted in several immune-related significant GO terms and pathways unique to this group, such as “autophagosome”, “cytosolic DNA-sensing pathway” and “response to type I interferons”. Understanding how experimental functional feeds can impact the host response and the trajectory of co-infections will be an essential step in identifying efficacious intervention strategies that account for the complexities of disease in open cage culture.
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spelling pubmed-87630122022-01-18 Transcriptome Analysis of Atlantic Salmon (Salmo salar) Skin in Response to Sea Lice and Infectious Salmon Anemia Virus Co-Infection Under Different Experimental Functional Diets Cai, Wenlong Kumar, Surendra Navaneethaiyer, Umasuthan Caballero-Solares, Albert Carvalho, Laura A. Whyte, Shona K. Purcell, Sara L. Gagne, Nellie Hori, Tiago S. Allen, Melissa Taylor, Richard G. Balder, Rachel Parrish, Christopher C. Rise, Matthew L. Fast, Mark D. Front Immunol Immunology Sea lice (Lepeophtheirus salmonis) are ectoparasitic copepods that cause significant economic loss in marine salmoniculture. In commercial salmon farms, infestation with sea lice can enhance susceptibility to other significant pathogens, such as the highly contagious infectious salmon anemia virus (ISAv). In this study, transcriptomic analysis was used to evaluate the impact of four experimental functional feeds (i.e. 0.3% EPA/DHA+high-ω6, 0.3% EPA/DHA+high-ω6+immunostimulant (IS), 1% EPA/DHA+high-ω6, and 1% EPA/DHA+high-ω3) on Atlantic salmon (Salmo salar) during a single infection with sea lice (L. salmonis) and a co-infection with sea lice and ISAv. The overall objectives were to compare the transcriptomic profiles of skin between lice infection alone with co-infection groups and assess differences in gene expression response among animals with different experimental diets. Atlantic salmon smolts were challenged with L. salmonis following a 28-day feeding trial. Fish were then challenged with ISAv at 18 days post-sea lice infection (dpi), and maintained on individual diets, to establish a co-infection model. Skin tissues sampled at 33 dpi were subjected to RNA-seq analysis. The co-infection’s overall survival rates were between 37%-50%, while no mortality was observed in the single infection with lice. With regard to the infection status, 756 and 1303 consensus differentially expressed genes (DEGs) among the four diets were identified in “lice infection vs. pre-infection” and “co-infection vs. pre-infection” groups, respectively, that were shared between the four experimental diets. The co-infection groups (co-infection vs. pre-infection) included up-regulated genes associated with glycolysis, the interferon pathway, complement cascade activity, and heat shock protein family, while the down-regulated genes were related to antigen presentation and processing, T-cell activation, collagen formation, and extracellular matrix. Pathway enrichment analysis conducted between infected groups (lice infection vs. co-infection) resulted in several immune-related significant GO terms and pathways unique to this group, such as “autophagosome”, “cytosolic DNA-sensing pathway” and “response to type I interferons”. Understanding how experimental functional feeds can impact the host response and the trajectory of co-infections will be an essential step in identifying efficacious intervention strategies that account for the complexities of disease in open cage culture. Frontiers Media S.A. 2022-01-03 /pmc/articles/PMC8763012/ /pubmed/35046944 http://dx.doi.org/10.3389/fimmu.2021.787033 Text en Copyright © 2022 Cai, Kumar, Navaneethaiyer, Caballero-Solares, Carvalho, Whyte, Purcell, Gagne, Hori, Allen, Taylor, Balder, Parrish, Rise and Fast https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Cai, Wenlong
Kumar, Surendra
Navaneethaiyer, Umasuthan
Caballero-Solares, Albert
Carvalho, Laura A.
Whyte, Shona K.
Purcell, Sara L.
Gagne, Nellie
Hori, Tiago S.
Allen, Melissa
Taylor, Richard G.
Balder, Rachel
Parrish, Christopher C.
Rise, Matthew L.
Fast, Mark D.
Transcriptome Analysis of Atlantic Salmon (Salmo salar) Skin in Response to Sea Lice and Infectious Salmon Anemia Virus Co-Infection Under Different Experimental Functional Diets
title Transcriptome Analysis of Atlantic Salmon (Salmo salar) Skin in Response to Sea Lice and Infectious Salmon Anemia Virus Co-Infection Under Different Experimental Functional Diets
title_full Transcriptome Analysis of Atlantic Salmon (Salmo salar) Skin in Response to Sea Lice and Infectious Salmon Anemia Virus Co-Infection Under Different Experimental Functional Diets
title_fullStr Transcriptome Analysis of Atlantic Salmon (Salmo salar) Skin in Response to Sea Lice and Infectious Salmon Anemia Virus Co-Infection Under Different Experimental Functional Diets
title_full_unstemmed Transcriptome Analysis of Atlantic Salmon (Salmo salar) Skin in Response to Sea Lice and Infectious Salmon Anemia Virus Co-Infection Under Different Experimental Functional Diets
title_short Transcriptome Analysis of Atlantic Salmon (Salmo salar) Skin in Response to Sea Lice and Infectious Salmon Anemia Virus Co-Infection Under Different Experimental Functional Diets
title_sort transcriptome analysis of atlantic salmon (salmo salar) skin in response to sea lice and infectious salmon anemia virus co-infection under different experimental functional diets
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8763012/
https://www.ncbi.nlm.nih.gov/pubmed/35046944
http://dx.doi.org/10.3389/fimmu.2021.787033
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