Effects of genotype and dietary fish oil replacement with vegetable oil on the intestinal transcriptome and proteome of Atlantic salmon (Salmo salar)

Abstract

BackgroundExpansion of aquaculture requires alternative feeds and breeding strategies to reduce dependency on fish oil (FO) and better utilization of dietary vegetable oil (VO). Despite the central role of intestine in maintaining body homeostasis and health, its molecular response to replacement of dietary FO by VO has been little investigated. This study employed transcriptomic and proteomic analyses to study effects of dietary VO in two family groups of Atlantic salmon selected for flesh lipid content, 'Lean' or 'Fat'.ResultsMetabolism, particularly of lipid and energy, was the functional category most affected by diet. Important effects were also measured in ribosomal proteins and signalling. The long-chain polyunsaturated fatty acid (LC-PUFA) biosynthesis pathway, assessed by fatty acid composition and gene expression, was influenced by genotype. Intestinal tissue contents of docosahexaenoic acid were equivalent in Lean salmon fed either a FO or VO diet and expression of LC-PUFA biosynthesis genes was up-regulated in VO-fed fish in Fat salmon. Dietary VO increased lipogenesis in Lean fish, assessed by expression of FAS, while no effect was observed on β-oxidation although transcripts of the mitochondrial respiratory chain were down-regulated, suggesting less active energetic metabolism in fish fed VO. In contrast, dietary VO up-regulated genes and proteins involved in detoxification, antioxidant defence and apoptosis, which could be associated with higher levels of polycyclic aromatic hydrocarbons in this diet. Regarding genotype, the following pathways were identified as being differentially affected: proteasomal proteolysis, response to oxidative and cellular stress (xenobiotic and oxidant metabolism and heat shock proteins), apoptosis and structural proteins particularly associated with tissue contractile properties. Genotype effects were accentuated by dietary VO.ConclusionsIntestinal metabolism was affected by diet and genotype. Lean fish may have higher responsiveness to low dietary n-3 LC-PUFA, up-regulating the biosynthetic pathway when fed dietary VO. As global aquaculture searches for alternative oils for feeds, this study alerts to the potential of VO introducing contaminants and demonstrates the detoxifying role of intestine. Finally, data indicate genotype-specific responses in the intestinal transcriptome and proteome to dietary VO, including possibly structural properties of the intestinal layer and defence against cellular stress, with Lean fish being more susceptible to diet-induced oxidative stress.

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“…The higher expression of mRNA of FAS coincided with the higher hepatic lipid deposition in 100% PO and could be attributed in the lower fatty acid oxidation in higher PO levels. This is in agreement to previous studies by Morais et al (2011), Morais et al (2012) in Atlantic salmon and Peng et al (2014) in juvenile turbot.…”

Fatty Acid‐Specific Alterations in Leptin, PPARα, and CPT‐1 Gene Expression in the Rainbow Trout

“…In the same species, the reduction of dietary LC-PUFA in favor of increased monounsaturated fatty acids (MUFA) and medium chain (C 18 ) PUFA, resulting from the substitution of dietary fish oil with vegetable oils, has been shown to alter the expression of genes related to fatty acid b-oxidation and PPAR [34]. Fish oil substitution by plant ingredients in rainbow trout diets weakly affected hepatic metabolism-related gene [35], while dietary VO increased lipogenesis and down-regulated b-oxidation in Atlantic salmon [36], although metabolic pathways and key regulators may respond differently to alternative plant-based feeds depending on genotype [37].…”

Influence of dietary inclusion of a wet processed faba bean protein isolate on post-smolt Atlantic salmon ( Salmo salar )

“…However, the transcriptomic response in pyloric caeca gave no obvious clues the chemical identity of the factor provoking the adverse reaction, which was perhaps not surprising. There are few studies investigating the molecular response of pyloric intestine to reinforce the present data (Morais et al, 2012;Betancor et al, 2015;De Santis et al, 2015c) as most studies on the effects of dietary plant proteins have focussed on distal intestine (Tacchi et al, 2011(Tacchi et al, , 2012Kortner et al, 2012;Sahlmann et al, 2013;De Santis et al, 2015d;Krol et al, 2016). In salmon fed increasing levels of soybean meal that provoked increasing enteritis, digestive enzyme activities in distal intestine were decreased, as observed in the present study (Krogdahl et al, 2003).…”