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

David Huyben, Tarah Mayes, Kerry Bartie, Chessor Matthew, Nini Sissener, Bjørg Kristine Hundal, Natalie Z M Homer, Bente Ruyter, Brett Glencross

Research output: Contribution to journalArticlepeer-review

Abstract / Description of output

Recent studies have found that feeding high levels of long chain polyunsaturated fatty acids (LC-PUFA) influ-
enced 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 ste-
roidogenesis. 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-dehy-
drocorticosterone, corticosterone, cortisol, dehydroepiandrosterone, pregnenolone and testosterone. The obser-
vation 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 aqua-
culture 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.
Original languageEnglish
JournalAquaculture
Early online date5 Nov 2022
DOIs
Publication statusE-pub ahead of print - 5 Nov 2022

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