Molecular Mechanism Involved in Carotenoid Metabolism in Post-Smolt Atlantic Salmon: Astaxanthin Metabolism During Flesh Pigmentation and Its Antioxidant Properties

Abstract

A better understanding of carotenoid dynamics (transport, absorption, metabolism, and deposition) is essential to develop a better strategy to improve astaxanthin (Ax) retention in muscle of Atlantic salmon. To achieve that, a comparison of postsmolt salmon with (+ Ax) or without (− Ax) dietary Ax supplementation was established based on a transcriptomic approach targeting pyloric, hepatic, and muscular tissues. Results in post-smolts showed that the pyloric caeca transcriptome is more sensitive to dietary Ax supplementation compared to the other tissues. Key genes sensitive to Ax supplementation could be identified, such as cd36 in pylorus, agr2 in liver, or fbp1 in muscle. The most modulated genes in pylorus were related to absorption but also metabolism of Ax. Additionally, genes linked to upstream regulation of the ferroptosis pathway were significantly modulated in liver, evoking the involvement of Ax as an antioxidant in this process. Finally, the muscle seemed to be less impacted by dietary Ax supplementation, except for genes related to actin remodelling and glucose homeostasis. In conclusion, the transcriptome data generated from this study showed that Ax dynamics in Atlantic salmon is characterized by a high metabolism during absorption at pyloric caeca level. In liver, a link with a potential of ferroptosis process appears likely via cellular lipid peroxidation. Our data provide insights into a better understanding of molecular mechanisms involved in dietary Ax supplementation, as well as its beneficial effects in preventing oxidative stress and related inflammation in muscle.

Carotenoids modulate stress tolerance and immune responses in aquatic animals

“…New investigations evidenced the intricacy of endogenous bioconversion and deposition of carotenoids in aquatic animals, which for the most part, was related to structural isomerism 95,96 . It was not until recently that researchers began to characterize and elucidate the diverse range of genes and pathways involved in the metabolism and deposition of exogenously derived carotenoids 90,97–99 . Exciting varieties of enzymes and transporter molecules linked to carotenoid‐based integumentary colouration in fish were suggested to be genetically controlled, analogous to findings in mammals and avians 94,100–102 .…”

“…95,96 It was not until recently that researchers began to characterize and elucidate the diverse range of genes and pathways involved in the metabolism and deposition of exogenously derived carotenoids. 90,[97][98][99] Exciting varieties of enzymes and transporter molecules linked to carotenoid-based integumentary colouration in fish were suggested to be genetically controlled, analogous to findings in mammals and avians. 94,[100][101][102] Accordingly, the main regulators in the molecular mechanisms of carotenoid utilization and storage amongst living animals can be potentially enhanced through genetic improvement.…”

Sources, dynamics in vivo, and application of astaxanthin and lutein in laying hens: A review

“…The absorption process for Ax is considered similar to that of lipids due to its fat–soluble properties, mainly involving disruption of the food matrix and molecular linkages, uptake in lipid droplets, micelle formation, and uptake from micelles into enterocytes and incorporation for transport into chylomicrons. Aside from the physiological factors of the gastrointestinal tract mentioned above, Ax absorption can be affected by dietary factors (food matrix, lipids, cholesterol, and fiber), cecal microbiota, and animal age ( Li et al., 2022 ; Schmeisser et al., 2021 ). A decrease in gut microbiota can lead to a lower oral absorbability of Ax in the small intestine ( Li et al., 2022 ).…”

“…After absorption from the gastrointestinal tract, the Ax is transported into the liver for metabolism and delivery to the other organs; of course, the remainder Ax is stored in the tissues. The storage or deposition potential of Ax varies in the liver, skin, fat, egg and muscle, with muscle appearing to have the lowest storage capacity ( Schmeisser et al., 2021 ; Surai et al., 2016 ; Xi et al., 2022 ). Meanwhile, some Ax undergoes physiological decomposition.…”

Histological and transcriptomic analysis of muscular atrophy associated with depleted flesh pigmentation in Atlantic salmon (Salmo salar) exposed to elevated seawater temperatures

“…At the gene expression level, the upregulation of genes involved in proteolysis, aerobic metabolism and collagenase proteolytic pathways was connected with muscle deterioration in rainbow trout 28 . Also, several genes involved in actin remodeling and glucose homeostasis were upregulated in Atlantic salmon fed astaxanthin-supplemented diet 29 . Research so far has focused primarily on defining phenotypic correlations with feed intake or on manipulating type and inclusion rate of pigments in the feed.…”