Influence of Dietary Long-Chain Polyunsaturated Fatty Acids and ω6 to ω3 Ratios on Head Kidney Lipid Composition and Expression of Fatty Acid and Eicosanoid Metabolism Genes in Atlantic Salmon (Salmo salar).

Tomer Katan,Matthew L Rise,Christopher C Parrish,Xi Xue,Albert Caballero-Solares,Richard G Taylor

doi:10.3389/fmolb.2020.602587

Abstract

The interaction of dietary eicosapentaenoic acid and docosahexaenoic acid (EPA+DHA) levels with omega-6 to omega-3 ratios (ω6:ω3), and their impact on head kidney lipid metabolism in farmed fish, are not fully elucidated. We investigated the influence of five plant-based diets (12-week exposure) with varying EPA+DHA levels (0.3, 1.0, or 1.4%) and ω6:ω3 (high ω6, high ω3, or balanced) on tissue lipid composition, and transcript expression of genes involved in fatty acid and eicosanoid metabolism in Atlantic salmon head kidney. Tissue fatty acid composition was reflective of the diet with respect to C18 PUFA and MUFA levels (% of total FA), and ω6:ω3 (0.5–1.5). Fish fed 0.3% EPA+DHA with high ω6 (0.3% EPA+DHA↑ω6) had the highest increase in proportions (1.7–2.3-fold) and in concentrations (1.4-1.8-fold) of arachidonic acid (ARA). EPA showed the greatest decrease in proportion and in concentration (by ~½) in the 0.3% EPA+DHA↑ω6 fed fish compared to the other treatments. However, no differences were observed in EPA proportions among salmon fed the high ω3 (0.3 and 1.0% EPA+DHA) and balanced (1.4% EPA+DHA) diets, and DHA proportions were similar among all treatments. Further, the transcript expression of elovl5a was lowest in the 0.3% EPA+DHA↑ω6 fed fish, and correlated positively with 20:3ω3, 20:4ω3 and EPA:ARA in the head kidney. This indicates that high dietary 18:3ω3 promoted the synthesis of ω3 LC-PUFA. Dietary EPA+DHA levels had a positive impact on elovl5a, fadsd5 and srebp1 expression, and these transcripts positively correlated with tissue ΣMUFA. This supported the hypothesis that LC-PUFA synthesis is positively influenced by tissue MUFA levels in Atlantic salmon. The expression of pparaa was higher in the 0.3% EPA+DHA↑ω6 compared to the 0.3% EPA+DHA↑ω3 fed fish. Finally, significant correlations between head kidney fatty acid composition and the expression of eicosanoid synthesis-related transcripts (i.e., 5loxa, 5loxb, cox1, cox2, ptges2, ptges3, and pgds) illustrated the constitutive relationships among fatty acids and eicosanoid metabolism in salmon.

Highlights

Long-chain polyunsaturated fatty acids (LC-PUFA) such as eicosapentaenoic (EPA, 20:5ω3), docosahexaenoic (DHA, 22:6ω3) and arachidonic (ARA, 20:4ω6) acids play important roles in fish growth, metabolism (Sargent et al, 2002), neural development, health and reproduction (Sargent et al, 1999; Tocher, 2010, 2015)
We investigated the influence of five plant-based diets (12-week exposure) with varying eicosapentaenoic acid and docosahexaenoic acid (EPA+DHA) levels (0.3, 1.0, or 1.4%) and ω6:ω3 on tissue lipid composition, and transcript expression of genes involved in fatty acid and eicosanoid metabolism in Atlantic salmon head kidney
The current study used the same diets and fish population as in Emam et al (2020), with the aim to investigate how diets with low fish oil (FO) inclusion levels impact head kidney lipid composition, and the transcript expression of genes involved in fatty acid and eicosanoid metabolism

Summary

Introduction

Long-chain polyunsaturated fatty acids (LC-PUFA) such as eicosapentaenoic (EPA, 20:5ω3), docosahexaenoic (DHA, 22:6ω3) and arachidonic (ARA, 20:4ω6) acids play important roles in fish growth, metabolism (Sargent et al, 2002), neural development, health and reproduction (Sargent et al, 1999; Tocher, 2010, 2015). Hepatic LC-PUFA synthesis in Atlantic salmon (Salmo salar) is influenced by precursor (18:2ω6 and/or 18:3ω3) availability, as well as the concentration of LC-PUFA (i.e., EPA, ARA, DHA) (Jordal et al, 2005; Glencross et al, 2015; Katan et al, 2019) This pathway is regulated at the transcriptional level and is mediated by transcription factors [e.g., liver X receptor (LXR), sterol regulatory element binding protein (SREBP) 1 and 2, and peroxisome proliferator-activated receptor (PPAR) α, β and γ (Carmona-Antoñanzas et al, 2014; Hixson et al, 2017; Katan et al, 2019; Emam et al, 2020)]. The constitutive regulation of this pathway in salmon head kidney is less well-understood (Betancor et al, 2014), and requires further investigation given the central role of this organ in haematopoetic and immune processes (Tort et al, 2003; Zapata et al, 2006; Gjøen et al, 2007)

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