Abstract
To improve the production efficiency of yellowtail Seriola quinqueradiata aquaculture, we measured changes in the activities of two lipid metabolism-related enzymes, carnitine palmitoyltransferase 2 (CPT2) and glucose-6-phosphate dehydrogenase (G6PDH), in the dark muscle and livers of 0- and 1 year-old fish over the entire culture period. Concomitantly we also investigated two factors that regulate these enzymes, namely, water temperature and daylength, under natural and controlled light conditions. In 0 year-old fish, high CPT2 activity was observed with increased water temperature/longer daylength, whereas high G6PDH activity was observed with decreased water temperature/shorter daylength. The activities of these enzymes were inversely correlated with each other. The changes in CPT2 and G6PDH activities were similar in 1- and 0 year old fish cultured with and without light control. To determine the major regulatory factors of CPT2 and G6PDH activities, two experiments were performed, starting on the vernal and autumnal equinox days, respectively. Fish were reared under natural and controlled light conditions (light:dark, 12:12 h) in both experiments. CPT2 activity did not differ according to light conditions or water temperature. G6PDH activity did not differ according to light conditions, but an increase in G6PDH activity was confirmed upon lowering of the water temperature. In summary, the activities of these two lipid metabolism-related enzymes changed seasonally and the main regulating factor may be water temperature. These results provide information for determining the appropriate lipid level and fatty acid composition of the seasonal diet for cultured yellowtail.
Similar content being viewed by others
References
Bowyer JN, Qin JG, Smullen RP, Stone DAJ (2012) Replacement of fish oil by poultry oil and canola oil in yellowtail kingfish (Seriola lalandi) at optimal and suboptimal temperatures. Comp Biochem Physiol 356–357:211–222
Bremer JG, Woldegiorgis G, Schalinske K, Shargo E (1985) Carnitine palmitoyltransferase. Activation by palmitoyl-CoA and inactivation by malonyl-CoA. Biochim Biophys Acta 833:9–16
Çiftçi M, Beydemir Ş, Yılmaz H, Altıkat S (2003) Purification of glucose 6-phosphate dehydrogenase from Buffalo (Bubalus bubalis) erythrocytes and investigation of some kinetic properties. Protein Expr Purif 29:304–310
Date K, Yamamoto Y (1988) Seasonal variations with growth in nutritive components in meat of cultured yellowtail Seriola quinqueradiata. Nippon Suisan Gakkaishi 54:1041–1047
Figueiredo-Silva AC, Saravanan S, Schrama JW, Kaushik S, Geurden I (2012) Macronutrient-induced differences in food intake relate with hepatic oxidative metabolism and hypothalamic regulatory neuropeptides in rainbow trout (Oncorhynchus mykiss). Physiol Behav 106:499–505
Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509
Frøyland L, Madsen L, Eckhoff KM, Lie Ø, Berge RK (1998) Carnitine palmitoyltransferase I, carnitine palmitoyltransferase II, and Acyl-CoA oxidase activities in Atlantic salmon (Salmo salar). Lipids 33:923–930
Fukada H, Tadokoro D, Furutani T, Yoshii K, Morioka K, Masumoto T (2009) Effect of discolored Porphyra meal supplemented-diet on growth performance and lipid metabolism in yearling yellowtail (Seriola quinqueradiata). Nippon Suisan Gakkaishi 75(1):64–69. (in Japanese with English abstract)
Fukada H, Taniguchi E, Morioka K, Masumoto T (2017) Effects of replacing fish oil with canola oil on the growth performance, fatty acid composition, and metabolic enzyme activity of juvenile yellowtail Seriola quinqueradiata (Temminck & Schlegel, 1845). Aquac Res 48:5928–5939
Glock GE, Mclean P (1953) Futher studies on the properties and assay of glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase of rat liver. Biochem J 55:400–408
Hashimoto T, Miyazawa S, Gunarso D, Furuta S (1981) α-Amanitin inhibits the oxidation of long chain fatty acids in mouse liver. J Biochem 90:415–421
Hardy RW (2002) Rainbow trout, Oncorhynchus mykiss. In: Webster CD, Lim CE (eds) Nutrient requirements and feeding of finfish for Aquaculture. CABI Publishing, New York, pp 184–202
Ibarz A, Beltrán F-B, Gallardo MA, Sánchez J, Blasco J (2007) Alterations in lipid metabolism and use of energy depots of gilthead sea bream (Sparus aurata) at low temperatures. Aquaculture 262:470–480
Ide T, Murata M, Sugano M (1996) Stimulation of the activities of hepatic fatty acid oxidation enzymes by dietary fat rich in α-linolenic acid in rats. J Lipid Res 37:448–463
Jiang G-Z, Shi H-J, Xu C, Zhang D-D, Liu W-B, Li X-F (2019) Glucose-6-phosphate dehydrogenase in blunt snout bream Megalobrama amblycephala: molecular characterization, tissue distribution, and the responsiveness to dietary carbohydrate levels. Fish Physiol Biochem 45:401–415
Kerner J, Hoppel C (2000) Fatty acid import into mitochondria. Biochim Biophys Acta 1486:1–17
Koshio S (2002) Red sea bream, Pagrus major. In: Webster CD, Lim CE (eds) Nutrient requirements and feeding of finfish for aquaculture. CABI Publishing, New York, pp 51–63
Koven W (2002) Gilthead sea bream, Sparus aurata. In: Webster CD, Lim CE (eds) Nutrient requirements and feeding of finfish for aquaculture. CABI Publishing, New York, pp 64–78
McGarry JD, Brown NF (1997) The mitochondrial carnitine palmitoyltransferase system. From concept to molecular analysis. Eur J Biochem 244:1–14
Masumoto T (2002) Yellowtail, Seriola quinqueradiata. In: Webster CD, Lim CE (eds) Nutrient requirements and feeding of finfish for Aquaculture. CABI Publishing, New York, pp 131–146
Nordgarden U, Oppedal F, Taranger GL, Hemre GI, Hansen T (2003) Seasonally changing metabolism in Atlantic salmon (Salmo salar L.) I—growth and feed conversion ratio. Aquac Nutr 9:287–293
Postic C, Girard J (2008) Contribution of de novo fatty acid synthesis to hepatic steatosis and insulin resistance: lessons from genetically engineered mice. J Clin Invest 118:829–838
Qiu H, Jin M, Li Y, You L, Hou YM, Zhou QC (2017) Dietary lipid sources influence fatty acid composition in tissue of large yellow croaker (Larmichthys crocea) by regulating triacylglycerol synthesis and catabolism at the transcriptional level. PLoS ONE 12:e0169985
Sánchez-muros MJ, García-rejón L, Lupiáñez de la Higuera M (1995) Long-term nutritional effects on the primary liver and kidney metabolism in rainbow trout, Oncorhynchus mykiss (Walbaum): adaptive response to a high-protein/non-carbohydrate diet and starvation of glucose 6-phosphate dehydrogenase activity. Aquac Nutr 1:213–220
Sánchez-muros MJ, García-rejón L, Lupiáñez de la Higuera M (1996) Long-term nutritional effects on the primary liver and kidney metabolism in rainbow trout (Oncorhynchus mykiss). II. Adaptive response of glucose 6-phosphate dehydrogenase activity to high-carbohydrate/low-protein and high-fat/non-carbohydrate diets. Aquac Nutr 2:193–200
Şentürk M, Ceyhun SB, Erdoğan O, Küfrevioğlu Öİ (2009) In vitro and in vivo effects of some pesticides on glucose-6-phosphate dehydrogenase enzyme activity from rainbow trout (Oncorhynchus mykiss) erythrocytes. Pestic Biochem Phys 95:95–99
Sheridan MA (1994) Regulation of lipid metabolism in poikilothermic vertebrates. Comp Biochem Physiol 107B:495–508
Shimeno S, Hosokawa H, Takeda M, Takayama S, Fukui A, Sasaki H (1981) Adaptation of hepatic enzymes to dietary lipid in young yellowtail. Nippon Suisan Gakkaishi 47:63–39 (in Japanese with English abstract)
Shimeno S, Shikata T, Hosokawa H (1992) Seasonal variations of carbohydrate-metabolizing enzyme activity and lipid content in liver of cultured yellowtail. Suisanzousyoku 40:201–206 (in Japanese with English abstract)
Shimeno S, Hosokawa H, Takeda M (1996) Metabolic response of juvenile yellowtail to dietary carbohydrate to lipid ratios. Fish Sci 62:945–949
Shimizu Y, Tada M, Endo K (1973) Seasonal variations in chemical constituents of yellowtail muscle-I. Nippon Suisan Gakkaishi 39:993–999 (in Japanese with English abstract)
Sicuro B, Luzzana U (2016) The state of Seriola spp. other than yellowtail (S. quinqueradiata) farming in the world. Rev Fish Sci Aquac 24:314–325
Strebakken T (2002) Atlantic salmon, Salmo salar. In: Webster CD, Lim CE (eds) Nutrient requirements and feeding of finfish for aquaculture. CABI Publishing, New York, pp 79–102
Stubhaug I, Lie Ø, Torstensen BE (2007) Fatty acid productive value and β-oxidation capacity in Atlantic salmon (Salmo salar L.) fed on different lipid sources along the whole growth period. Aquac Nutr 13:145–155
Suárez MD, Hidaldo MC, Gallego MG, Sanz A, de la Higuera (1995) Influence of the relative proportions of energy yielding nutrients on liver intermediary metabolism of the European eel. Comp Biochem Physiol 111A: 421-428
Turchini GM, Mentasti T, Frøyland L, Orban E, Carpino F, Moretti VM, Valfre F (2003) Effects of alternative dietary lipid sources on performance, tissue chemical composition, mitochondrial fatty acid oxidation capabilities and sensory characteristics in brown trout (Salmo trutta L.). Aquaculture 225:251–267
Yan J, Liao K, Mai K, Qinghui A (2017) Dietary lipid levels affect lipoprotein clearance, fatty acid transport, lipogenesis and lipolysis at the transcriptional level in muscle and adipose tissue of large yellow croaker (Larimichthys crocea). Aquac Res 48:3925–3934
Acknowledgements
This study was conducted in cooperation with Owase Bussan Co., Ltd. for the sampling and provision of fish for this study. This research was supported by grants from the NARO Bio-oriented Technology Research Advancement Institution (Research program on the development of innovative technology).
Author information
Authors and Affiliations
Contributions
HF carried out the analysis of metabiotic enzyme activity, analyzed the data, and wrote the paper. HY carried out the analysis of metabiotic enzyme activity. CM, TM, and KK edited the paper, in addition to designing and coordinating the project.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The original online version of this article was revised to delete data availability statement.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Fukada, H., Yabuki, H., Miura, C. et al. Regulation of lipid metabolism by water temperature and photoperiod in yellowtail Seriola quinqueradiata. Fish Sci 89, 191–202 (2023). https://doi.org/10.1007/s12562-022-01664-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12562-022-01664-4