Development of Atlantic Salmon (Salmo salar L.) Under Hypoxic Conditions Induced Sustained Changes in Expression of Immune Genes and Reduced Resistance to Moritella viscosa

Atlantic salmon is characterized with high sensitivity to low dissolved oxygen (DO) levels. Hypoxia can affect diverse biological processes with consequences that can be manifested immediately or with delay. Effects of hypoxia on the immune system and the resistance to a bacterial pathogen were inve...

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Published in:Frontiers in Ecology and Evolution
Main Authors: Krasnov, Aleksei, Burgerhout, Erik, Johnsen, Hanne, Tveiten, Helge, Bakke, Anne Flore, Lund, Hege, Afanasyev, Sergey, Rebl, Alexander, Johansen, Lill-Heidi
Format: Article in Journal/Newspaper
Language:English
Published: Frontiers Media 2021
Subjects:
Online Access:https://hdl.handle.net/10037/22744
https://doi.org/10.3389/fevo.2021.722218
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spelling ftunivtroemsoe:oai:munin.uit.no:10037/22744 2023-05-15T15:32:21+02:00 Development of Atlantic Salmon (Salmo salar L.) Under Hypoxic Conditions Induced Sustained Changes in Expression of Immune Genes and Reduced Resistance to Moritella viscosa Krasnov, Aleksei Burgerhout, Erik Johnsen, Hanne Tveiten, Helge Bakke, Anne Flore Lund, Hege Afanasyev, Sergey Rebl, Alexander Johansen, Lill-Heidi 2021-08-02 https://hdl.handle.net/10037/22744 https://doi.org/10.3389/fevo.2021.722218 eng eng Frontiers Media Frontiers in Ecology and Evolution Norges forskningsråd: 267644 info:eu-repo/grantAgreement/RCN/HAVBRUK2/267644/Norway/Development of tools for assessment of the immune competence of Atlantic salmon smolts and growers// Krasnov, Burgerhout, Johnsen, Tveiten, Bakke AF, Lund, Afanasyev, Rebl, Johansen. Development of Atlantic Salmon (Salmo salar L.) Under Hypoxic Conditions Induced Sustained Changes in Expression of Immune Genes and Reduced Resistance to Moritella viscosa. Frontiers in Ecology and Evolution. 2021;9:1-11 FRIDAID 1929869 doi:10.3389/fevo.2021.722218 2296-701X https://hdl.handle.net/10037/22744 openAccess Copyright 2021 The Author(s) VDP::Agriculture and fishery disciplines: 900::Fisheries science: 920::Fish health: 923 VDP::Landbruks- og Fiskerifag: 900::Fiskerifag: 920::Fiskehelse: 923 Journal article Tidsskriftartikkel Peer reviewed publishedVersion 2021 ftunivtroemsoe https://doi.org/10.3389/fevo.2021.722218 2021-10-13T22:53:55Z Atlantic salmon is characterized with high sensitivity to low dissolved oxygen (DO) levels. Hypoxia can affect diverse biological processes with consequences that can be manifested immediately or with delay. Effects of hypoxia on the immune system and the resistance to a bacterial pathogen were investigated. Two groups were reared at, respectively, normal (NO, 80–100%) and low (LO, 60%) levels of DO over 10 months after which both groups were reared at NO. Smoltification was initiated after 13 months by a winter signal for 6 weeks, followed by constant light for 6 weeks. Samples were collected at the start and end of the constant light period. Expression of 92 immune and stress genes was analyzed in the gill, head kidney, and spleen using a Biomark HD. Most of differentially expressed genes showed higher levels in LO fish compared to NO fish; many immune genes were downregulated during smoltification and these changes were stronger in NO fish. A notable exception was pro-inflammatory genes upregulated in gill of NO fish. Further, salmon were challenged with Moritella viscosa , the causative agent of winter ulcer. Mortality was registered from 5 days post infection (dpi) to the end of trial at 36 dpi. Survival was consistently higher in NO than LO fish, reaching a maximum difference of 18% at 21–23 dpi that reduced to 10% at the end. Analyses with a genome-wide microarray at 36 dpi showed strong responses to the pathogen in gill and spleen. Notable features were the stimulation of eicosanoid metabolism, suggesting an important role of lipid mediators of inflammation, and the downregulation of chemokines. Many immune effectors were activated, including multiple lectins and acute phase proteins, enzymes producing free radicals, and matrix metalloproteinases. The transcriptomic changes induced with a bacterial challenge were similar in NO and LO. After the challenge, interferons a and g and panel of genes of innate antiviral immunity showed higher expression in LO, especially in the gill. The results from the present study suggest that chronic hypoxia in early life stimulated immune genes and attenuated their downregulation associated with smoltification. However, these changes did not improve protection against a bacterial pathogen of major concern in salmon aquaculture. Article in Journal/Newspaper Atlantic salmon Salmo salar University of Tromsø: Munin Open Research Archive Frontiers in Ecology and Evolution 9
institution Open Polar
collection University of Tromsø: Munin Open Research Archive
op_collection_id ftunivtroemsoe
language English
topic VDP::Agriculture and fishery disciplines: 900::Fisheries science: 920::Fish health: 923
VDP::Landbruks- og Fiskerifag: 900::Fiskerifag: 920::Fiskehelse: 923
spellingShingle VDP::Agriculture and fishery disciplines: 900::Fisheries science: 920::Fish health: 923
VDP::Landbruks- og Fiskerifag: 900::Fiskerifag: 920::Fiskehelse: 923
Krasnov, Aleksei
Burgerhout, Erik
Johnsen, Hanne
Tveiten, Helge
Bakke, Anne Flore
Lund, Hege
Afanasyev, Sergey
Rebl, Alexander
Johansen, Lill-Heidi
Development of Atlantic Salmon (Salmo salar L.) Under Hypoxic Conditions Induced Sustained Changes in Expression of Immune Genes and Reduced Resistance to Moritella viscosa
topic_facet VDP::Agriculture and fishery disciplines: 900::Fisheries science: 920::Fish health: 923
VDP::Landbruks- og Fiskerifag: 900::Fiskerifag: 920::Fiskehelse: 923
description Atlantic salmon is characterized with high sensitivity to low dissolved oxygen (DO) levels. Hypoxia can affect diverse biological processes with consequences that can be manifested immediately or with delay. Effects of hypoxia on the immune system and the resistance to a bacterial pathogen were investigated. Two groups were reared at, respectively, normal (NO, 80–100%) and low (LO, 60%) levels of DO over 10 months after which both groups were reared at NO. Smoltification was initiated after 13 months by a winter signal for 6 weeks, followed by constant light for 6 weeks. Samples were collected at the start and end of the constant light period. Expression of 92 immune and stress genes was analyzed in the gill, head kidney, and spleen using a Biomark HD. Most of differentially expressed genes showed higher levels in LO fish compared to NO fish; many immune genes were downregulated during smoltification and these changes were stronger in NO fish. A notable exception was pro-inflammatory genes upregulated in gill of NO fish. Further, salmon were challenged with Moritella viscosa , the causative agent of winter ulcer. Mortality was registered from 5 days post infection (dpi) to the end of trial at 36 dpi. Survival was consistently higher in NO than LO fish, reaching a maximum difference of 18% at 21–23 dpi that reduced to 10% at the end. Analyses with a genome-wide microarray at 36 dpi showed strong responses to the pathogen in gill and spleen. Notable features were the stimulation of eicosanoid metabolism, suggesting an important role of lipid mediators of inflammation, and the downregulation of chemokines. Many immune effectors were activated, including multiple lectins and acute phase proteins, enzymes producing free radicals, and matrix metalloproteinases. The transcriptomic changes induced with a bacterial challenge were similar in NO and LO. After the challenge, interferons a and g and panel of genes of innate antiviral immunity showed higher expression in LO, especially in the gill. The results from the present study suggest that chronic hypoxia in early life stimulated immune genes and attenuated their downregulation associated with smoltification. However, these changes did not improve protection against a bacterial pathogen of major concern in salmon aquaculture.
format Article in Journal/Newspaper
author Krasnov, Aleksei
Burgerhout, Erik
Johnsen, Hanne
Tveiten, Helge
Bakke, Anne Flore
Lund, Hege
Afanasyev, Sergey
Rebl, Alexander
Johansen, Lill-Heidi
author_facet Krasnov, Aleksei
Burgerhout, Erik
Johnsen, Hanne
Tveiten, Helge
Bakke, Anne Flore
Lund, Hege
Afanasyev, Sergey
Rebl, Alexander
Johansen, Lill-Heidi
author_sort Krasnov, Aleksei
title Development of Atlantic Salmon (Salmo salar L.) Under Hypoxic Conditions Induced Sustained Changes in Expression of Immune Genes and Reduced Resistance to Moritella viscosa
title_short Development of Atlantic Salmon (Salmo salar L.) Under Hypoxic Conditions Induced Sustained Changes in Expression of Immune Genes and Reduced Resistance to Moritella viscosa
title_full Development of Atlantic Salmon (Salmo salar L.) Under Hypoxic Conditions Induced Sustained Changes in Expression of Immune Genes and Reduced Resistance to Moritella viscosa
title_fullStr Development of Atlantic Salmon (Salmo salar L.) Under Hypoxic Conditions Induced Sustained Changes in Expression of Immune Genes and Reduced Resistance to Moritella viscosa
title_full_unstemmed Development of Atlantic Salmon (Salmo salar L.) Under Hypoxic Conditions Induced Sustained Changes in Expression of Immune Genes and Reduced Resistance to Moritella viscosa
title_sort development of atlantic salmon (salmo salar l.) under hypoxic conditions induced sustained changes in expression of immune genes and reduced resistance to moritella viscosa
publisher Frontiers Media
publishDate 2021
url https://hdl.handle.net/10037/22744
https://doi.org/10.3389/fevo.2021.722218
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_relation Frontiers in Ecology and Evolution
Norges forskningsråd: 267644
info:eu-repo/grantAgreement/RCN/HAVBRUK2/267644/Norway/Development of tools for assessment of the immune competence of Atlantic salmon smolts and growers//
Krasnov, Burgerhout, Johnsen, Tveiten, Bakke AF, Lund, Afanasyev, Rebl, Johansen. Development of Atlantic Salmon (Salmo salar L.) Under Hypoxic Conditions Induced Sustained Changes in Expression of Immune Genes and Reduced Resistance to Moritella viscosa. Frontiers in Ecology and Evolution. 2021;9:1-11
FRIDAID 1929869
doi:10.3389/fevo.2021.722218
2296-701X
https://hdl.handle.net/10037/22744
op_rights openAccess
Copyright 2021 The Author(s)
op_doi https://doi.org/10.3389/fevo.2021.722218
container_title Frontiers in Ecology and Evolution
container_volume 9
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