Critical assessment of metabolism and related growth and quality traits in trout fed spirulina-supplemented plant-based diets

Nowadays in aquaculture, the nutrition of carnivorous fish species requires the development of sustainable plant-based diets. Supplementation with microorganisms such as spirulina could offer an alternative to full plant-based diets that are inappropriate for carnivorous species such as rainbow trout. However, the benefits and drawbacks of spirulina supplementation on fish performance and metabolism need to be assessed to substantiate spirulina as an appropriate ingredient. The objective of this work was to determine the metabolic utilization of a plant-based diet supplemented with two levels of spirulina (5% and 15%) and to compare it to a full plant-based (PB) and a commercial-like (COM) diet for trout. Spirulina supplementation induced both a decrease in feed intake and an increase in feed efficiency while maintaining growth and a putative reorientation of lipid deposition from viscera to muscle. Fatty acid changes, including an increase in saturated fatty acids, a decrease in monounsaturated fatty acids, and color changes with an increase in b* index (yellow), suggested a slight alteration of the nutritional and visual quality of fish fed a spirulina diet. 1 H NMR metabolomics profiling was used to measure metabolites in experimental feeds and in fish plasma, liver, and muscle. Two specific compounds of the spirulina ingredient were identified and determined to have opposed metabolic fates: i) a quinone-like compound was found to accumulate in liver and ii) β-hydroxybutyrate was found to be completely metabolized. The main metabolites modulated by spirulina in plasma and tissues were involved in energy and amino acid metabolisms. Spirulina supplementation almost suppressed the accumulation of glucose and essential amino acids in fish plasma and muscle induced by the PB diet. However, these compounds, as well as betaine, were found to accumulate in the liver of fish fed spirulina-supplemented diets. An alteration of liver metabolism due to the specific fatty acid profile and quinone-like compound of spirulina is suspected. A correlative approach of fish performance, quality traits, and metabolomic data in plasma and liver suggests that the maintenance of growth rate and feed efficiency using spirulina supplementation of a PB diet requires not only the supply of a well-balanced protein but also the redirection of lipid metabolism. However, observed changes in fatty acid composition and color suggest further alterations of the phospholipid metabolism. This work thus provides a contrasted fate of spirulina supplementation of a PB diet with both expected positive effects and unexpected negative effects that must be investigated further. • The supplementation of a full plant-based diet with spirulina maintain growth and feed efficiency but still below a commercial-like diet. • Specific compounds of spirulina showed contrasted fate in fish : accumulation (quinone-like compound) or metabolism (β-hydroxybutyrate and glucosides). • 1 H NMR metabolomics revealed that spirulina restore amino acids and glucose profiles in plasma and muscle but not in the liver. • Correlation between polar metabolites, free fatty acids, and lipoproteins with growth performance and quality traits are demonstrated.