Dataset Information

Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: a liver transcriptomic analysis.

ABSTRACT: BACKGROUND: Expansion of aquaculture is seriously limited by reductions in fish oil (FO) supply for aquafeeds. Terrestrial alternatives such as vegetable oils (VO) have been investigated and recently a strategy combining genetic selection with changes in diet formulations has been proposed to meet growing demands for aquaculture products. This study investigates the influence of genotype on transcriptomic responses to sustainable feeds in Atlantic salmon. RESULTS: A microarray analysis was performed to investigate the liver transcriptome of two family groups selected according to their estimated breeding values (EBVs) for flesh lipid content, 'Lean' or 'Fat', fed diets containing either FO or a VO blend. Diet principally affected metabolism genes, mainly of lipid and carbohydrate, followed by immune response genes. Genotype had a much lower impact on metabolism-related genes and affected mostly signalling pathways. Replacement of dietary FO by VO caused an up-regulation of long-chain polyunsaturated fatty acid biosynthesis, but there was a clear genotype effect as fatty acyl elongase (elovl2) was only up-regulated and desaturases (?5 fad and ?6 fad) showed a higher magnitude of response in Lean fish, which was reflected in liver fatty acid composition. Fatty acid synthase (FAS) was also up-regulated by VO and the effect was independent of genotype. Genetic background of the fish clearly affected regulation of lipid metabolism, as PPAR? and PPAR? were down-regulated by the VO diet only in Lean fish, while in Fat salmon SREBP-1 expression was up-regulated by VO. In addition, all three genes had a lower expression in the Lean family group than in the Fat, when fed VO. Differences in muscle adiposity between family groups may have been caused by higher levels of hepatic fatty acid and glycerophospholipid synthesis in the Fat fish, as indicated by the expression of FAS, 1-acyl-sn-glycerol-3-phosphate acyltransferase and lipid phosphate phosphohydrolase 2. CONCLUSIONS: This study has identified metabolic pathways and key regulators that may respond differently to alternative plant-based feeds depending on genotype. Further studies are required but data suggest that it will be possible to identify families better adapted to alternative diet formulations that might be appropriate for future genetic selection programmes.

SUBMITTER: Morais S

PROVIDER: S-EPMC3113789 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: a liver transcriptomic analysis.

Morais Sofia S Pratoomyot Jarunan J Taggart John B JB Bron James E JE Guy Derrick R DR Bell J Gordon JG Tocher Douglas R DR

BMC genomics 20110520

<h4>Background</h4>Expansion of aquaculture is seriously limited by reductions in fish oil (FO) supply for aquafeeds. Terrestrial alternatives such as vegetable oils (VO) have been investigated and recently a strategy combining genetic selection with changes in diet formulations has been proposed to meet growing demands for aquaculture products. This study investigates the influence of genotype on transcriptomic responses to sustainable feeds in Atlantic salmon.<h4>Results</h4>A microarray analy ...[more]

PMID: 21599965

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Project description: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.

Project description:To evolve fish farming in an eco-efficient way, feed production must become less dependent on forage fish-based ingredients and make more use of low trophic level organisms, including microalgae, higher plants, as filter feeding organisms and other ingredients with low competition to established food value chains. Diets nearly free of fish meal and fish oil are not a novelty but are often composed of complex mixtures, containing supplements to meet the farmed animal’s nutritional requirements. Sustaining a growing aquaculture production, maintaining at the same time fish health, welfare, and profitability, and meeting strict environmental and food safety demands, is challenging and requires new technologies, great investments, and more knowledge. A benchmarking feeding trial was performed to demonstrate the main effects of four low trophic raw materials on Atlantic salmon (Salmo salar) growth, metabolism, skin health and fillet quality. To this end, a diet was produced to contain commercially relevant levels of fresh high quality organic FM and FO and was used as a control in the trial (FMFO). Heterotrophically produced Schizochytrium limacinum biomass was used to replace organic FO (HM diet). Spray dried cell wall disrupted biomass of the phototrophically cultured diatom Phaeodactylum tricornutum replaced partly FM and FO (PM diet). Black soldier fly (Hermetia illucens) larvae meal and tunicate (Ciona intestinalis) meal, were used to produce the diets BSFL and TM, respectively, replacing large parts of FM as compared to the FMFO. A fifth test diet was produced combining all test raw materials and removing all FM and FO (0FM0FO diet). All test ingredients were well accepted sustaining high growth rates (TGC values near 4) and feed efficiency (FCR values below 0.9) in salmon showing good gut health and normal metabolic responses. However, none of the treatments reached the growth performance of FMFO. Additional differences between test and control treatments were identified in dietary nutrient apparent digestibility, fish biometrics, blood metabolites and fillet and skin composition. Extensive raw material and dietary chemical characterisation was performed to provide insight on potential shortcomings in the novel low trophic level ingredients which can possibly be overcome combining complementary raw materials.

Project description:BackgroundFish meal and fish oil are increasingly replaced by ingredients from terrestrial sources in the feeds for farmed salmonids due to expanding production and reduced availability of marine feed raw material. Fish oil that is rich in n-3 polyunsaturated fatty acids is considered beneficial to human health in general and to prevent intestinal inflammation and carcinogenesis in particular. In contrast, n-6 fatty acids that are present in many vegetable oils have been associated with increased risk of colitis and colon cancer in rodents and humans, as well as lowered transcription levels of certain stress and antioxidant-related genes in Atlantic salmon.The aim of the present study was to investigate the intestinal health in Atlantic salmon fed with different vegetable oils as partial substitutes of fish oil in the diet. A feed trial lasting for 28 weeks included one reference diet containing fish oil as the sole lipid source and three diets where 80% of the fish oil was replaced by a plant oil blend with either olive oil, rapeseed oil or soybean oil as the main lipid source. These plant oils have intermediate or low n-3/n-6-ratios compared to fish oil having a high n-3/n-6-ratio. The protein and carbohydrate fractions were identical in all the feeds.ResultsMorphometric measurements showed significantly shorter folds in the mid intestine in all groups fed vegetable oils compared to the group fed fish oil. In the distal intestine, the complex folds were significantly shorter in the fish fed soybean oil compared to the fish fed rapeseed oil. Histological and immunohistochemical examination did not show clear difference in the degree of inflammation or proliferation of epithelial cells related to dietary groups, which was further confirmed by real-time RT-PCR which revealed only moderate alterations in the mRNA transcript levels of selected immune-related genes.ConclusionsShortened intestinal folds might be associated with reduced intestinal surface and impaired nutrient absorption and growth, but our results suggest that partial substitution of dietary fish oil with vegetable oils does not have any major negative impact on the intestinal health of Atlantic salmon.

Project description:There is an increasing drive to replace fish oil (FO) in finfish aquaculture diets with vegetable oils (VO), driven by the short supply of FO derived from wild fish stocks. However, little is known of the consequences for fish health after such substitution. The effect of dietary VO on hepatic gene expression, lipid composition and growth was determined in Atlantic salmon (Salmo salar), using a combination of cDNA microarray, lipid, and biochemical analysis. FO was replaced with VO, added to diets as rapeseed (RO), soybean (SO) or linseed (LO) oils.Dietary VO had no major effect on growth of the fish, but increased the whole fish protein contents and tended to decrease whole fish lipid content, thus increasing the protein:lipid ratio. Expression levels of genes of the highly unsaturated fatty acid (HUFA) and cholesterol biosynthetic pathways were increased in all vegetable oil diets as was SREBP2, a master transcriptional regulator of these pathways. Other genes whose expression was increased by feeding VO included those of NADPH generation, lipid transport, peroxisomal fatty acid oxidation, a marker of intracellular lipid accumulation, and protein and RNA processing. Consistent with these results, HUFA biosynthesis, hepatic beta-oxidation activity and enzymic NADPH production were changed by VO, and there was a trend for increased hepatic lipid in LO and SO diets. Tissue cholesterol levels in VO fed fish were the same as animals fed FO, whereas fatty acid composition of the tissues largely reflected those of the diets and was marked by enrichment of 18 carbon fatty acids and reductions in 20 and 22 carbon HUFA.This combined gene expression, compositional and metabolic study demonstrates that major lipid metabolic effects occur after replacing FO with VO in salmon diets. These effects are most likely mediated by SREBP2, which responds to reductions in dietary cholesterol. These changes are sufficient to maintain whole body cholesterol levels but not HUFA levels.

Dataset Information

Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: a liver transcriptomic analysis.

Publications

Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: a liver transcriptomic analysis.

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