Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin

We investigated the immunomodulatory effect of varying levels of dietary ω6/ω3 fatty acids (FA) on Atlantic salmon (Salmo salar) antibacterial response. Two groups were fed either high-18:3ω3 or high-18:2ω6 FA diets for 8 weeks, and a third group was fed for 4 weeks on the high-18:2ω6 diet followed...

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Published in:Frontiers in Molecular Biosciences
Main Authors: Emam, Mohamed, Eslamloo, Khalil, Caballero-Solares, Albert, Lorenz, Evandro Kleber, Xue, Xi, Umasuthan, Navaneethaiyer, Gnanagobal, Hajarooba, Santander, Javier, Taylor, Richard G, Balder, Rachel, Parrish, Christopher C, Rise, Matthew L
Other Authors: Natural Sciences and Engineering Research Council of Canada, Memorial University of Newfoundland, Cargill Aqua Nutrition, Cargill Innovation Center, orcid:0000-0001-7693-0739
Format: Article in Journal/Newspaper
Language:English
Published: Frontiers Media SA 2022
Subjects:
Online Access:http://hdl.handle.net/1893/36797
https://doi.org/10.3389/fmolb.2022.931548
http://dspace.stir.ac.uk/retrieve/c390b234-776f-4545-b735-bd25d57259cd/fmolb-09-931548.pdf
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author Emam, Mohamed
Eslamloo, Khalil
Caballero-Solares, Albert
Lorenz, Evandro Kleber
Xue, Xi
Umasuthan, Navaneethaiyer
Gnanagobal, Hajarooba
Santander, Javier
Taylor, Richard G
Balder, Rachel
Parrish, Christopher C
Rise, Matthew L
author2 Natural Sciences and Engineering Research Council of Canada
Memorial University of Newfoundland
Cargill Aqua Nutrition
Cargill Innovation Center
orcid:0000-0001-7693-0739
author_facet Emam, Mohamed
Eslamloo, Khalil
Caballero-Solares, Albert
Lorenz, Evandro Kleber
Xue, Xi
Umasuthan, Navaneethaiyer
Gnanagobal, Hajarooba
Santander, Javier
Taylor, Richard G
Balder, Rachel
Parrish, Christopher C
Rise, Matthew L
author_sort Emam, Mohamed
collection University of Stirling: Stirling Digital Research Repository
container_title Frontiers in Molecular Biosciences
container_volume 9
description We investigated the immunomodulatory effect of varying levels of dietary ω6/ω3 fatty acids (FA) on Atlantic salmon (Salmo salar) antibacterial response. Two groups were fed either high-18:3ω3 or high-18:2ω6 FA diets for 8 weeks, and a third group was fed for 4 weeks on the high-18:2ω6 diet followed by 4 weeks on the high-18:3ω3 diet and termed “switched-diet”. Following the second 4 weeks of feeding (i.e., at 8 weeks), head kidney tissues from all groups were sampled for FA analysis. Fish were then intraperitoneally injected with either a formalin-killed Renibacterium salmoninarum bacterin (5 × 107 cells mL−1) or phosphate-buffered saline (PBS control), and head kidney tissues for gene expression analysis were sampled at 24 h post-injection. FA analysis showed that the head kidney profile reflected the dietary FA, especially for C18 FAs. The qPCR analyses of twenty-three genes showed that both the high-ω6 and high-ω3 groups had significant bacterin-dependent induction of some transcripts involved in lipid metabolism (ch25ha and lipe), pathogen recognition (clec12b and tlr5), and immune effectors (znrf1 and cish). In contrast, these transcripts did not significantly respond to the bacterin in the “switched-diet” group. Concurrently, biomarkers encoding proteins with putative roles in biotic inflammatory response (tnfrsf6b) and dendritic cell maturation (ccl13) were upregulated, and a chemokine receptor (cxcr1) was downregulated with the bacterin injection regardless of the experimental diets. On the other hand, an inflammatory regulator biomarker, bcl3, was only significantly upregulated in the high-ω3 fed group, and a C-type lectin family member (clec3a) was only significantly downregulated in the switched-diet group with the bacterin injection (compared with diet-matched PBS-injected controls). Transcript fold-change (FC: bacterin/PBS) showed that tlr5 was significantly over 2-fold higher in the high-18:2ω6 diet group compared with other diet groups. FC and FA associations highlighted the role of DGLA (20:3ω6; ...
format Article in Journal/Newspaper
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
id ftunivstirling:oai:dspace.stir.ac.uk:1893/36797
institution Open Polar
language English
op_collection_id ftunivstirling
op_doi https://doi.org/10.3389/fmolb.2022.931548
op_relation Emam M, Eslamloo K, Caballero-Solares A, Lorenz EK, Xue X, Umasuthan N, Gnanagobal H, Santander J, Taylor RG, Balder R, Parrish CC & Rise ML (2022) Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin. Frontiers in Molecular Biosciences , 9. https://doi.org/10.3389/fmolb.2022.931548
http://hdl.handle.net/1893/36797
doi:10.3389/fmolb.2022.931548
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WOS:000864833200001
2089076
op_rights Copyright © 2022 Emam, Eslamloo, Caballero-Solares, Lorenz, Xue, Umasuthan, Gnanagobal, Santander, Taylor, Balder, Parrish and Rise. 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.
http://creativecommons.org/licenses/by/4.0/
publishDate 2022
publisher Frontiers Media SA
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spelling ftunivstirling:oai:dspace.stir.ac.uk:1893/36797 2025-04-13T14:15:58+00:00 Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin Emam, Mohamed Eslamloo, Khalil Caballero-Solares, Albert Lorenz, Evandro Kleber Xue, Xi Umasuthan, Navaneethaiyer Gnanagobal, Hajarooba Santander, Javier Taylor, Richard G Balder, Rachel Parrish, Christopher C Rise, Matthew L Natural Sciences and Engineering Research Council of Canada Memorial University of Newfoundland Cargill Aqua Nutrition Cargill Innovation Center orcid:0000-0001-7693-0739 2022-09-21 application/pdf http://hdl.handle.net/1893/36797 https://doi.org/10.3389/fmolb.2022.931548 http://dspace.stir.ac.uk/retrieve/c390b234-776f-4545-b735-bd25d57259cd/fmolb-09-931548.pdf en eng Frontiers Media SA Emam M, Eslamloo K, Caballero-Solares A, Lorenz EK, Xue X, Umasuthan N, Gnanagobal H, Santander J, Taylor RG, Balder R, Parrish CC & Rise ML (2022) Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin. Frontiers in Molecular Biosciences , 9. https://doi.org/10.3389/fmolb.2022.931548 http://hdl.handle.net/1893/36797 doi:10.3389/fmolb.2022.931548 36213116 WOS:000864833200001 2089076 Copyright © 2022 Emam, Eslamloo, Caballero-Solares, Lorenz, Xue, Umasuthan, Gnanagobal, Santander, Taylor, Balder, Parrish and Rise. 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. http://creativecommons.org/licenses/by/4.0/ Salmo Salar bacterial kidney disease formalin-killed Renibacterium salmoninarum bacterin qPCR Molecular biomarker ω3 and ω6 dietary fatty acids Journal Article VoR - Version of Record 2022 ftunivstirling https://doi.org/10.3389/fmolb.2022.931548 2025-03-18T00:50:09Z We investigated the immunomodulatory effect of varying levels of dietary ω6/ω3 fatty acids (FA) on Atlantic salmon (Salmo salar) antibacterial response. Two groups were fed either high-18:3ω3 or high-18:2ω6 FA diets for 8 weeks, and a third group was fed for 4 weeks on the high-18:2ω6 diet followed by 4 weeks on the high-18:3ω3 diet and termed “switched-diet”. Following the second 4 weeks of feeding (i.e., at 8 weeks), head kidney tissues from all groups were sampled for FA analysis. Fish were then intraperitoneally injected with either a formalin-killed Renibacterium salmoninarum bacterin (5 × 107 cells mL−1) or phosphate-buffered saline (PBS control), and head kidney tissues for gene expression analysis were sampled at 24 h post-injection. FA analysis showed that the head kidney profile reflected the dietary FA, especially for C18 FAs. The qPCR analyses of twenty-three genes showed that both the high-ω6 and high-ω3 groups had significant bacterin-dependent induction of some transcripts involved in lipid metabolism (ch25ha and lipe), pathogen recognition (clec12b and tlr5), and immune effectors (znrf1 and cish). In contrast, these transcripts did not significantly respond to the bacterin in the “switched-diet” group. Concurrently, biomarkers encoding proteins with putative roles in biotic inflammatory response (tnfrsf6b) and dendritic cell maturation (ccl13) were upregulated, and a chemokine receptor (cxcr1) was downregulated with the bacterin injection regardless of the experimental diets. On the other hand, an inflammatory regulator biomarker, bcl3, was only significantly upregulated in the high-ω3 fed group, and a C-type lectin family member (clec3a) was only significantly downregulated in the switched-diet group with the bacterin injection (compared with diet-matched PBS-injected controls). Transcript fold-change (FC: bacterin/PBS) showed that tlr5 was significantly over 2-fold higher in the high-18:2ω6 diet group compared with other diet groups. FC and FA associations highlighted the role of DGLA (20:3ω6; ... Article in Journal/Newspaper Atlantic salmon Salmo salar University of Stirling: Stirling Digital Research Repository Frontiers in Molecular Biosciences 9
spellingShingle Salmo Salar
bacterial kidney disease
formalin-killed Renibacterium salmoninarum bacterin
qPCR
Molecular biomarker
ω3 and ω6 dietary fatty acids
Emam, Mohamed
Eslamloo, Khalil
Caballero-Solares, Albert
Lorenz, Evandro Kleber
Xue, Xi
Umasuthan, Navaneethaiyer
Gnanagobal, Hajarooba
Santander, Javier
Taylor, Richard G
Balder, Rachel
Parrish, Christopher C
Rise, Matthew L
Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin
title Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin
title_full Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin
title_fullStr Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin
title_full_unstemmed Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin
title_short Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin
title_sort nutritional immunomodulation of atlantic salmon response to renibacterium salmoninarum bacterin
topic Salmo Salar
bacterial kidney disease
formalin-killed Renibacterium salmoninarum bacterin
qPCR
Molecular biomarker
ω3 and ω6 dietary fatty acids
topic_facet Salmo Salar
bacterial kidney disease
formalin-killed Renibacterium salmoninarum bacterin
qPCR
Molecular biomarker
ω3 and ω6 dietary fatty acids
url http://hdl.handle.net/1893/36797
https://doi.org/10.3389/fmolb.2022.931548
http://dspace.stir.ac.uk/retrieve/c390b234-776f-4545-b735-bd25d57259cd/fmolb-09-931548.pdf