Steroidogenic and innate immune responses in Atlantic salmon are influenced by dietary total lipid, long chain polyunsaturated fatty acids and dissolved oxygen

Citation

Huyben D, Cronin T, Bartie KL, Matthew C, Sissener NH, Hundal BK, Homer NZM, Ruyter B & Glencross B (2023) Steroidogenic and innate immune responses in Atlantic salmon are influenced by dietary total lipid, long chain polyunsaturated fatty acids and dissolved oxygen. Aquaculture, 564, Art. No.: 739028. https://doi.org/10.1016/j.aquaculture.2022.739028

Abstract
Recent studies have found that feeding high levels of long chain polyunsaturated fatty acids (LC-PUFA) influenced the steroid biosynthesis pathway of Atlantic salmon on a transcriptomic level, although research observed on a metabolic level is lacking. Dietary lipid and chronic stress have also been suggested to play a role in steroidogenesis. A study was performed on Atlantic salmon post-smolts (184 g) fed with diets of high and low levels of lipid with and without high levels of LC-PUFA under hypoxic (stressed) or normoxic (unstressed) conditions. Liver, head kidney and blood samples were collected after 35 and 116 days to determine short- and long-term effects. On day 35, dissolved oxygen affected the levels of the steroid hormones 11-deoxycortisol, cortisone and testosterone as well as the relative expression of cyp11a involved in steroidogenesis and ud2a2 involved in sex steroid metabolism. On day 116, an interaction between lipid x LC-PUFA x oxygen was found for cyp11a, hsd3b (steroidogenesis) and ud2a2 genes, whereas LC-PUFA and/or oxygen affected the steroid levels of 11-dehydrocorticosterone, corticosterone, cortisol, dehydroepiandrosterone, pregnenolone and testosterone. The observation that both LC-PUFA and oxygen affected cyp11a expression and the levels of pregnenolone, provides evidence for the influence of both parameters on the rate-limiting point of steroid production, which can take >35 days to establish. The 3-way interaction between lipid, LC-PUFA and dissolved oxygen on the expression of steroid genes suggests that the chronic stressor of hypoxia may be over-riding dietary influences of the lipid and LC-PUFA, though the relative proportion of LC-PUFA within the lipid may play a role as well. In terms of fatty acid composition, low dietary lipid and high LC-PUFA increased the levels of total n-6 and n-3 PUFA in the liver, particularly EPA and DHA, and the head kidney to a lesser extent. In terms of immune pathways, hypoxia influenced cytokine gene expression (tgfb, il10), cellular repair gene expression (gr, hsp70 and hsp90) and eicosanoid levels (PGE2 and LTB5) in the head kidney, while dietary lipid and LC-PUFA influenced cytokines (ifnγ and il1β) and eicosanoids (PGE2 and LTB5). These findings demonstrate that feeding different levels of LC-PUFA significantly alters steroidogenesis and innate immune response in Atlantic salmon post-smolts with additional interactions from dietary lipid and hypoxia stress. These results will significantly impact the aquaculture industry since it demonstrates salmon fed high levels of LC-PUFA are likely more resilient to cope with chronic stressors (e.g. prolonged hypoxia) due to lower corticosteroid levels and upregulated immune response.

Keywords
Cytokines; Fatty acids; Gene expression; Haematology; Hypoxia; LC-MS/MS; Salmonids; Steroids; Stress

Journal
Aquaculture: Volume 564