Abstract
Salmons raised in aquaculture farms around the world are increasingly subjected to sub-optimal environmental conditions, such as high water temperatures during summer seasons. Aerobic scope increases and lipid metabolism changes are known plasticity responses of fish for a better acclimation to high water temperature. The present study aimed at investigating the effect of high water temperature on the regulation of fatty acid metabolism in juvenile Atlantic salmon fed different dietary ARA/EPA ratios (arachidonic acid, 20:4n-6/ eicosapentaenoic acid, 20:5n-3), with particular focus on apparent in vivo enzyme activities and gene expression of lipid metabolism pathways. Three experimental diets were formulated to be identical, except for the ratio EPA/ARA, and fed to triplicate groups of Atlantic salmon (Salmo salar) kept either at 10°C or 20°C. Results showed that fatty acid metabolic utilisation, and likely also their dietary requirements for optimal performance, can be affected by changes in their relative levels and by environmental temperature in Atlantic salmon. Thus, the increase in temperature, independently from dietary treatment, had a significant effect on the β-oxidation of a fatty acid including EPA, as observed by the apparent in vivo enzyme activity and mRNA expression of pparα -transcription factor in lipid metabolism, including β-oxidation genes- and cpt1 -key enzyme responsible for the movement of LC-PUFA from the cytosol into the mitochondria for β-oxidation-, were both increased at the higher water temperature. An interesting interaction was observed in the transcription and in vivo enzyme activity of Δ5fad–time-limiting enzyme in the biosynthesis pathway of EPA and ARA. Such, at lower temperature, the highest mRNA expression and enzyme activity was recorded in fish with limited supply of dietary EPA, whereas at higher temperature these were recorded in fish with limited ARA supply. In consideration that fish at higher water temperature recorded a significantly increased feed intake, these results clearly suggested that at high, sub-optimal water temperature, fish metabolism attempted to increment its overall ARA status -the most bioactive LC-PUFA participating in the inflammatory response- by modulating the metabolic fate of dietary ARA (expressed as % of net intake), reducing its β-oxidation and favouring synthesis and deposition. This correlates also with results from other recent studies showing that both immune- and stress- responses in fish are up regulated in fish held at high temperatures. This is a novel and fundamental information that warrants industry and scientific attention, in consideration of the imminent increase in water temperatures, continuous expansion of aquaculture operations, resources utilisation in aquafeed and much needed seasonal/adaptive nutritional strategies.
Highlights
As global sea temperatures rise and market demands grow, aquaculture is increasingly encountering sub-optimal conditions due to changing environments [1] and/or expansion into areas outside the ideal range for the species; and this is the case for Atlantic salmon farming along the Australian coast [2]
In consideration that fish at higher water temperature recorded a significantly increased feed intake, these results clearly suggested that at high, sub-optimal water temperature, fish metabolism attempted to increment its overall ARA status -the most bioactive Long chain polyunsaturated fatty acids (LC-PUFA) participating in the inflammatory response- by modulating the metabolic fate of dietary ARA, reducing its β-oxidation and favouring synthesis and PLOS ONE | DOI:10.1371/journal.pone
Dietary treatments had only minor, almost trivial, effects on fatty acid and nutrient digestibility, whereas water temperature resulted in altered digestibility values, with lower nutrient digestibility recorded at lower water temperature [19]
Summary
As global sea temperatures rise and market demands grow, aquaculture is increasingly encountering sub-optimal conditions due to changing environments [1] and/or expansion into areas outside the ideal range for the species; and this is the case for Atlantic salmon farming along the Australian coast [2]. Numerous studies on several teleost species have shown that increase in temperature reduces the accumulation of LC-PUFA in body lipid depots and cell membranes and enhances the deposition of saturated fatty acids, SFA [6, 15,16,17,18]. Water temperature exerts a major impact in fatty acid metabolism and use of energy depots in teleost fish [22], and rises in temperature may change the fish’s requirements for optimal performance of dietary lipids and LC-PUFA [3, 5], as well as energy demand, associated to increases in growth rate. Studies of fatty acid composition and swimming performance in Atlantic salmon held at 8°C suggest that the energy demanded by fish swimming is mainly provided by β-oxidation of 18-carbon unsaturated fatty acids [27], but this might change with increases in water temperature. Recent studies on fish acclimation to high temperatures, showed that aerobic scope increase together with lipid metabolism as a fish plasticity response for a better acclimation to high water temperature [28]
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