Interaction between ω 6 and ω 3 fatty acids of different chain lengths regulates Atlantic salmon hepatic gene expression and muscle fatty acid profiles

Abstract

Atlantic salmon smolts (approx. 20-months old) were fed experimental diets with different combinations of omega-6:omega-3 fatty acids (FAs) (high-ω6, high-ω3, or balanced) and eicosapentaenoic acid plus docosahexaenoic acid (EPA + DHA) levels (0.3, 1.0 or 1.4%) for 12 weeks. Muscle FA (% total FA) reflected dietary C₁₈-polyunsaturated FA; however, muscle EPA per cent and content (mg g^-1) were not different in salmon fed high-ω3 or balanced diets. Muscle DHA per cent was similar among treatments, while DHA content increased in fish fed 1.4% EPA + DHA, compared with those fed 0.3-1.0% EPA + DHA combined with high-ω6 FA. Muscle 20:3ω6 (DGLA) content was highest in those fed high-ω6 with 0.3% EPA + DHA. Quantitative polymerase chain reaction analyses on liver RNA showed that the monounsaturated FA synthesis-related gene, scdb, was upregulated in fish fed 1.0% EPA + DHA with high-ω6 compared to those fed 0.3% EPA + DHA. In high-ω3-fed salmon, liver elovl2 transcript levels were higher with 0.3% EPA + DHA than with 1.0% EPA + DHA. In high-ω6-fed fish, elovl2 did not vary with EPA + DHA levels, but it was positively correlated with muscle ARA, 22:4ω3 and DGLA. These results suggest dietary 18:3ω3 elongation contributed to maintaining muscle EPA + DHA levels despite a two- to threefold change in dietary proportions, while 18:2ω6 with 0.3% EPA + DHA increased muscle DGLA more than arachidonic acid (ARA). Positive correlations between hepatic elovl2 and fabp10a with muscle ω6:ω3 and EPA + DHA + ARA, respectively, were confirmed by reanalysing data from a previous salmon trial with lower variations in dietary EPA + DHA and ω6:ω3 ratios. This article is part of the theme issue 'The next horizons for lipids as 'trophic biomarkers': evidence and significance of consumer modification of dietary fatty acids'.

Keywords: EPA and DHA; diet; lipid metabolism biomarkers; ω6:ω3 ratio.

Figure 1.

Effect of diets on the transcript levels of lipid-related biomarkers. (a) Transcripts with putative roles in C₁₈-polyunsaturated fatty acid elongation (elovl2) and the master regulator transcription factor pparaa. (b) Transcripts related to the Krebs cycle (csb), de novo fatty acid synthesis (scdb and fasb) and fatty acid transport (cd36c). The transcript RQs (relative quantities) are shown as mean ± s.e. Bars with different letters are significantly different for a one-way ANOVA across dietary treatments. P-values from a two-way ANOVA are given in the upper table (significance is shown with asterisks (*) on the figure). The listed fatty acids (lower table) are significantly correlated with the corresponding biomarker and placed to show the correlation direction (i.e. green for positive and red for negative). Diets fed: 0.3%EPA+DHA↑ω6, 0.3%EPA+DHA↑ω3, 1%EPA+DHA↑ω6, 1%EPA+DHA↑ω3 and the control diet (1.4% EPA+DHA+balanced levels of ω3+ω6).

Figure 2.

Principal coordinates analysis (PCoA) of the same transcripts and muscle fatty acids from the two trials showing vectors with Pearson's r > 0.45. (a) PCoA and significant bivariate correlations (below on the left in (c)) between muscle fatty acids percent and liver transcript levels for the 0.3–1.4%EPA+DHA trial. (b) PCoA and significant bivariate correlations (below on the right in (c)) between muscle fatty acids percent and liver transcript levels for the 1–1.3%EPA+DHA trial. Transcripts are bolded on both plots. (c) Fatty acid (%) significant correlations with liver transcript levels; an asterisk (*) identifies the results of a different correlation using only groups fed 1.0% and 1.4% EPA+DHA in the 0.3–1.4%EPA+DHA trial.