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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 post-smolt 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.

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adapted from Sztretye et al. 2019). Ax is known to activate IRS-1/AKT pathway triggering the translocation of GLUT4 in the muscular cell membrane allowing glucose uptake. Here, Ax also induced up-regulation of fbp1 responsible of glucose homeostasis via gluconeogenesis or glycolysis. Additionally, coro2a was up-regulated and participates to the actin remodelling needed for GLUT4 translocation initiated by IRS1/PI3K/AKT pathway

Availability of Data and Material

Microarray data will be deposited in the GEO database.

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Acknowledgements

We would like to thank the staff at the IMR Research station in Matre for their help in experimental design and sampling. We would like to also thank Christelle Iaconis for her technical support in gene expression analysis, and for her help in the final revision of the manuscript. Finally, we thank Dr Igor Bendik and Dr Britt Blokker for advising and sharing their knowledge on the generation and analysis of transcriptomic data.

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Open access funding provided by the Institute Of Marine Research. This work was supported by DSM Nutritional Products, Switzerland.

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Correspondence to Jerome Schmeisser.

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Schmeisser, J., Verlhac-Trichet, V., Madaro, A. et al. Molecular Mechanism Involved in Carotenoid Metabolism in Post-Smolt Atlantic Salmon: Astaxanthin Metabolism During Flesh Pigmentation and Its Antioxidant Properties. Mar Biotechnol 23, 653–670 (2021). https://doi.org/10.1007/s10126-021-10055-2

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Keywords

  • Atlantic Salmon
  • Carotenoids
  • Astaxanthin
  • Absorption
  • Antioxidant