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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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-09-01
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| Series: | Frontiers in Molecular Biosciences |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmolb.2022.931548/full |
| _version_ | 1818062451417022464 |
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| author | Mohamed Emam Khalil Eslamloo Albert Caballero-Solares Evandro Kleber Lorenz Xi Xue Navaneethaiyer Umasuthan Hajarooba Gnanagobal Javier Santander Richard G. Taylor Rachel Balder Christopher C. Parrish Matthew L. Rise |
| author_facet | Mohamed Emam Khalil Eslamloo Albert Caballero-Solares Evandro Kleber Lorenz Xi Xue Navaneethaiyer Umasuthan Hajarooba Gnanagobal Javier Santander Richard G. Taylor Rachel Balder Christopher C. Parrish Matthew L. Rise |
| author_sort | Mohamed Emam |
| collection | DOAJ |
| 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; anti-inflammatory) and/or EPA (20:5ω3; anti-inflammatory) vs. ARA (20:4ω6; pro-inflammatory) as representative of the anti-inflammatory/pro-inflammatory balance between eicosanoid precursors. Also, the correlations revealed associations of FA proportions (% total FA) and FA ratios with several eicosanoid and immune receptor biomarkers (e.g., DGLA/ARA significant positive correlation with pgds, 5loxa, 5loxb, tlr5, and cxcr1). In summary, dietary FA profiles and/or regimens modulated the expression of some immune-relevant genes in Atlantic salmon injected with R. salmoninarum bacterin. The modulation of Atlantic salmon responses to bacterial pathogens and their associated antigens using high-ω6/high-ω3 diets warrants further investigation. |
| first_indexed | 2024-12-10T14:04:25Z |
| format | Article |
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| institution | Directory Open Access Journal |
| issn | 2296-889X |
| language | English |
| last_indexed | 2024-12-10T14:04:25Z |
| publishDate | 2022-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Molecular Biosciences |
| spelling | doaj.art-7ecb2283829544679b77f122ce292b442022-12-22T01:45:43ZengFrontiers Media S.A.Frontiers in Molecular Biosciences2296-889X2022-09-01910.3389/fmolb.2022.931548931548Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterinMohamed Emam0Khalil Eslamloo1Albert Caballero-Solares2Evandro Kleber Lorenz3Xi Xue4Navaneethaiyer Umasuthan5Hajarooba Gnanagobal6Javier Santander7Richard G. Taylor8Rachel Balder9Christopher C. Parrish10Matthew L. Rise11Department of Ocean Sciences, Memorial University of Newfoundland, St. John’s, NL, CanadaDepartment of Ocean Sciences, Memorial University of Newfoundland, St. John’s, NL, CanadaDepartment of Ocean Sciences, Memorial University of Newfoundland, St. John’s, NL, CanadaDepartment of Ocean Sciences, Memorial University of Newfoundland, St. John’s, NL, CanadaDepartment of Ocean Sciences, Memorial University of Newfoundland, St. John’s, NL, CanadaDepartment of Ocean Sciences, Memorial University of Newfoundland, St. John’s, NL, CanadaMarine Microbial Pathogenesis and Vaccinology Laboratory, Department of Ocean Sciences, Memorial University of Newfoundland, St. John’s, NL, CanadaMarine Microbial Pathogenesis and Vaccinology Laboratory, Department of Ocean Sciences, Memorial University of Newfoundland, St. John’s, NL, CanadaCargill Animal Nutrition and Health, Minneapolis, MN, United StatesCargill Animal Nutrition and Health, Minneapolis, MN, United StatesDepartment of Ocean Sciences, Memorial University of Newfoundland, St. John’s, NL, CanadaDepartment of Ocean Sciences, Memorial University of Newfoundland, St. John’s, NL, CanadaWe 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; anti-inflammatory) and/or EPA (20:5ω3; anti-inflammatory) vs. ARA (20:4ω6; pro-inflammatory) as representative of the anti-inflammatory/pro-inflammatory balance between eicosanoid precursors. Also, the correlations revealed associations of FA proportions (% total FA) and FA ratios with several eicosanoid and immune receptor biomarkers (e.g., DGLA/ARA significant positive correlation with pgds, 5loxa, 5loxb, tlr5, and cxcr1). In summary, dietary FA profiles and/or regimens modulated the expression of some immune-relevant genes in Atlantic salmon injected with R. salmoninarum bacterin. The modulation of Atlantic salmon responses to bacterial pathogens and their associated antigens using high-ω6/high-ω3 diets warrants further investigation.https://www.frontiersin.org/articles/10.3389/fmolb.2022.931548/fullSalmo salarbacterial kidney diseaseformalin-killed Renibacterium salmoninarum bacterinqPCRmolecular biomarkerω3 and ω6 dietary fatty acids |
| spellingShingle | Mohamed Emam Khalil Eslamloo Albert Caballero-Solares Evandro Kleber Lorenz Xi Xue Navaneethaiyer Umasuthan Hajarooba Gnanagobal Javier Santander Richard G. Taylor Rachel Balder Christopher C. Parrish Matthew L. Rise Nutritional immunomodulation of Atlantic salmon response to Renibacterium salmoninarum bacterin Frontiers in Molecular Biosciences Salmo salar bacterial kidney disease formalin-killed Renibacterium salmoninarum bacterin qPCR molecular biomarker ω3 and ω6 dietary fatty acids |
| 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 |
| url | https://www.frontiersin.org/articles/10.3389/fmolb.2022.931548/full |
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