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Journal of Ocean University of China

, Volume 18, Issue 2, pp 519–527 | Cite as

Temperature-Dependent Fatty Acid Composition Change of Phospholipid in Steelhead Trout (Oncorhynchus mykiss) Tissues

  • Chengyue Liu
  • Shuanglin Dong
  • Yangen ZhouEmail author
  • Kunpeng Shi
  • Zhe Pan
  • Dajiang Sun
  • Qinfeng Gao
Article

Abstract

In this study, the changes of the fatty acid composition of phospholipid in different tissues (muscle, heart, brain and spleen) of steelhead trout (Oncorhynchus mykiss) were analyzed when the water temperature decreased gradually from 16°C to 12°C, 8°C, 6°C, 4°C, 2°C and 1°C. Three fish individuals each tank (average weight 70.32 g ± 9.12 g) were collected and used to analysis at each designed temperatures. At normal temperature (16°C), the fatty acid composition of phospholipid of muscle and heart was similar each other. The highest concentration of saturate fatty acids (SFA) was found in the phospholipid of spleen. The brain phospholipid contained higher oleic acid (18:1n9) than the phospholipid of other tissues at 16°C. When the environmental temperature decreased, the concentration of unsaturated fatty acids of phospholipids in all tissues increased, and accordingly the ratio pf the unsaturated to saturated fatty acids (U/S) and unsaturation index (UI) increased, indicating that steelhead trout can compensate temperature- dependent changes in membrane fluidity by remodeling the fatty acid composition of phospholipids. The changes in the fatty acid composition of phospholipid were tissue-specific. At the early stages of the experiment (16°C to 8°C), the fatty acid composition of phospholipid changed remarkably in muscle, heart, and spleen. When temperature decreased to less than 8°C, an obvious response of phospholipid fatty acid was observed in all tissues. The change of phospholipid composition of steelhead trout tissues may be affected by both cold stress and starvation when the temperature decreased to 2°C, and the change of phospholipid composition of muscle was very obvious.

Key words

temperature tissue phospholipid fatty acid steelhead trout Oncorhynchus mykiss 

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Notes

Acknowledgements

The authors would like to thank those who have critically review this manuscript. This study was jointly funded by the National Natural Science Foundation of China (Nos. 31572634 and 31702364), the Fundamental Research Funds for the Central Universities of China (No. 20161205), the Key Research and Development Program of Shandong Province (Nos. 2016CYJS04A01 and 2017CXGC0106), and Science and Technology Planning Project of Guangdong Province, China (No. 2017B030314052).

References

  1. Aho, E., and Vornanen, M., 2001. Cold acclimation increases basal heart rate but decreases its thermal tolerance in rainbow trout (Oncorhynchus mykiss). Journal of Comparative Physiology B Biochemical Systemic & Environmental Physiology, 171 (2): 173–179.CrossRefGoogle Scholar
  2. Bell, J. G., Mcghee, F., Campbell, P. J., and Sargent, J. R., 2003. Rapeseed oil as an alternative to marine fish oil in diets of post–smolt Atlantic salmon (Salmo salar): Changes in flesh fatty acid composition and effectiveness of subsequent fish oil ‘wash out’. Aquaculture, 218 (1–4): 515–528.CrossRefGoogle Scholar
  3. Bell, M. V., and Tocher, D. R., 1989. Molecular species composition of the major phospholipids in brain and retina from rainbow trout (Salmo gairdneri). Biochemical Journal, 264 (3): 909–915.CrossRefGoogle Scholar
  4. Bell, M. V., Henderson, R. J., and Sargent, J. R., 2008. The role of phospholipids in nutrition and metabolism of teleost fish. Aquaculture, 280 (4): 21–34.Google Scholar
  5. Biro, P. A., Morton, A. E., Post, J. R., and Parkinson, E. A., 2004. Over–winter lipid depletion and mortality of age–0 rainbow trout (Oncorhynchus mykiss). Canadian Journal of Fisheries and Aquatic Sciences, 61 (8): 1513–1519.CrossRefGoogle Scholar
  6. Buda, C., Dey, I., Balogh, N., Horvath, L. I., Maderspach, K., Juhasz, M., Yeo, Y. K., and Farkas, T., 1994. Structural order of membranes and composition of phospholipids in fish brain cells during thermal acclimatization. Proceedings of the National Academy of Sciences, 91 (17): 8234–8238.CrossRefGoogle Scholar
  7. Cengiz, E. I., Bayar, A. S., and Kizmaz, V., 2016. The protective effect of vitamin E against changes in fatty acid composition of phospholipid subclasses in gill tissue of Oreochromis niloticus exposed to deltamethrin. Chemosphere, 147 (1): 138–143.CrossRefGoogle Scholar
  8. Cengiz, E. I., Bayar, A. S., Kizmaz, V., Başhan, M., and Satar, A., 2017. Acute toxicity of deltamethrin on the fatty acid composition of phospholipid classes in liver and gill tissues of Nile tilapia. International Journal of Environmental Research, 8: 1–9.Google Scholar
  9. Copeman, L. A., Laurel, B. J., and Parrish, C. C., 2013. Effect of temperature and tissue type on fatty acid signatures of two species of North Pacific juvenile gadids: A laboratory feeding study. Journal of Experimental Marine Biology and Ecology, 448: 188–196.CrossRefGoogle Scholar
  10. Cossins, A. R., and Prosser, C. L., 1982. Variable homeoviscous responses of different brain membranes of thermally–acclimated goldfish. Biochimica et Biophysica Acta, 687 (2): 303.CrossRefGoogle Scholar
  11. Crockett, E. L., 2008. The cold but not hard fats in ectotherms: Consequences of lipid restructuring on susceptibility of biological membranes to peroxidation, a review. Journal of Comparative Physiology B Biochemical Systemic and Environmental Physiology, 178 (7): 795–809.CrossRefGoogle Scholar
  12. Dey, I., Buda, C., Wiik, T., Halver, J. E., and Farkas, T., 1993. Molecular and structural composition of phospholipid membranes in livers of marine and freshwater fish in relation to temperature. Proceedings of the National Academy of Sciences of the United States of America, 90 (16): 7498–7502.CrossRefGoogle Scholar
  13. Donaldson, M. R., Cooke, S. J., Patterson, D. A., and Macdonald, J. S., 2008. Cold shock and fish. Journal of Fish Biology, 73 (7): 1491–1530.CrossRefGoogle Scholar
  14. Fänge, R., and Nilsson, S., 1985. The fish spleen: Structure and function. Experientia, 41 (2): 152.CrossRefGoogle Scholar
  15. Fadhlaoui, M., and Couture, P., 2016. Combined effects of temperature and metal exposure on the fatty acid composition of cell membranes, antioxidant enzyme activities and lipid peroxidation in yellow perch (Perca flavescens). Aquatic Toxicology, 180: 45–55.CrossRefGoogle Scholar
  16. Farkas, T., Fodor, E., Kitajka, K., and Halver, J. E., 2001. Response of fish membranes to environmental temperature. Aquaculture Research, 32 (32): 645–655.CrossRefGoogle Scholar
  17. Fokina, N. N., Ruokolainen, T. R., Bakhmet, I. N., and Nemova, N. N., 2015. Lipid composition in response to temperature changes in blue mussels Mytilus edulis L. from the White Sea. Journal of the Marine Biological Association of the United Kingdon, 1 (8): 1–6.Google Scholar
  18. Folch, J., Lees, M., and Sloane, S. G. H., 1957. A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry, 226 (1): 497–509.Google Scholar
  19. Han, L., Guo, Y., and Dong, S., 2016. Establishment of national offshore aquaculture experimental zone in the Yellow Sea cold water. Pacific Journal, 24 (5): 79–85 (in Chinese with English abstract).Google Scholar
  20. Hazel, J. R., 1979. Influence of thermal acclimation on membrane lipid composition of rainbow trout liver. American Journal of Physiology, 236 (1): 91–101.Google Scholar
  21. Hazel, J. R., and Williams, E. E., 1990. The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Progress in Lipid Research, 29 (3): 167–227.CrossRefGoogle Scholar
  22. Hong, H., Zhou, Y., Wu, H., Luo, Y., and Shen, H., 2014. Lipid content and fatty acid profile of muscle, brain and eyes of seven freshwater fish: A comparative study. Journal of the American Oil Chemists Society, 91 (5): 795–804.CrossRefGoogle Scholar
  23. Hsieh, S. L., Chen, Y. N., and Kuo, C. M., 2003. Physiological responses, desaturase activity, and fatty acid composition in milkfish (Chanos chanos) under cold acclimation. Aquaculture, 220 (1): 903–918.CrossRefGoogle Scholar
  24. Ingemansson, T., Olsson, N. U., and Kaufmann, P., 1993. Lipid composition of light and dark muscle of rainbow trout (Oncorhynchus mykiss) after thermal acclimation: A multivariate approach. Aquaculture, 113 (1): 153–165.CrossRefGoogle Scholar
  25. Jobling, M., and Bendiksen, E. Å., 2015. Dietary lipids and temperature interact to influence tissue fatty acid compositions of Atlantic salmon, Salmo salar L., parr. Aquaculture Research, 34 (15): 1423–1441.CrossRefGoogle Scholar
  26. Kostal, V., and Simek, P., 1998. Changes in fatty acid composition of phospholipids and triacylglycerols after cold–acclimation of an aestivating insect prepupa. Journal of Comparative Physiology, B, 168 (6): 453–460.CrossRefGoogle Scholar
  27. Li, G., Sinclair, A. J., and Li, D., 2011. Comparison of lipid content and fatty acid composition in the edible meat of wild and cultured freshwater and marine fish and shrimps from China. Journal of Agricultural & Food Chemistry, 59 (5): 1871.CrossRefGoogle Scholar
  28. Mellery, J., Geay, F., Stas, C., Tocher, D. R., Kestemont, P., Rollin, X., and Larondelle, Y., 2015. Does the water temperature influence the fatty acid metabolism of rainbow trout (Oncorhynchus mykiss) fed a vegetable diet? Communications in Agricultural & Applied Biological Sciences, 80 (1): 45–49.Google Scholar
  29. Ng, W. K., Sigholt, T., and Bell, G., 2015. The influence of environmental temperature on the apparent nutrient and fatty acid digestibility in Atlantic salmon (Salmo salar L.) fed finishing diets containing different blends of fish oil, rapeseed oil and palm oil. Aquaculture Research, 35 (13): 1228–1237.CrossRefGoogle Scholar
  30. Olsen, Y., 1999. Lipids and Essential Fatty Acids in Aquatic Food Webs: What Can Freshwater Ecologists Learn from Mariculture? Springer Sicence Business Media, New York, 161–202.Google Scholar
  31. Osman, H., and Suriah, A. R., 2001. Fatty acid composition and cholesterol content of selected marine fish in Malaysian waters. Food Chemistry, 73 (1): 55–60.CrossRefGoogle Scholar
  32. Pauly, D., and Zeller, D., 2017. Comments on FAOs State of World Fisheries and Aquaculture (SOFIA 2016). Marine Policy, 77: 176–181.CrossRefGoogle Scholar
  33. Pettegrew, J. W., Panchalingam, K., Mcclure, R. J., Gershon, S., Muenz, L. R., and Levine, J., 2015. Effects of chronic lithium administration on rat brain phosphatidylinositol cycle constituents, membrane phospholipids and amino acids. Bipolar Disorders, 3 (4): 189–201.CrossRefGoogle Scholar
  34. Schregel, W. D., 2013. Changes in tissue–specific fatty acid composition of the freshwater alewife (Alosa pseudoharengus) in response to temperature. Digital Commons at Buffalo State, Paper 9. The State University of New York.Google Scholar
  35. Sigholt, T., and Finstad, B., 1990. Effect of low temperature on seawater tolerance in Atlantic salmon (Salmo salar) smolts. Aquaculture, 84 (2): 167–172.CrossRefGoogle Scholar
  36. Sinensky, M., 1974. Homeoviscous adaptation–A homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America, 71 (2): 522–525.CrossRefGoogle Scholar
  37. Skuladottir, G. V., Schioth, H. B., Gudmundsdottir, E., Richards, B., Gardarsson, F., and Jonsson, L., 1990. Fatty acid composition of muscle, heart and liver lipids in Atlantic salmon, Salmo salar, at extremely low environmental temperature. Aquaculture, 84 (1): 71–80.CrossRefGoogle Scholar
  38. Sloat, M. R., Reeves, G. H., and Jonsson, B., 2014. Individual condition, standard metabolic rate, and rearing temperature influence steelhead and rainbow trout (Oncorhynchus mykiss) life histories. Canadian Journal of Fisheries and Aquatic Sciences, 71 (4): 491–501.CrossRefGoogle Scholar
  39. Snyder, R. J., and Hennessey, T. M., 2003. Cold tolerance and homeoviscous adaptation in freshwater alewives (Alosa pseudoharengus). Fish Physiology and Biochemistry, 29 (2): 117–126.CrossRefGoogle Scholar
  40. Snyder, R. J., Schregel, W. D., and Wei, Y., 2012. Effects of thermal acclimation on tissue fatty acid composition of freshwater alewives (Alosa pseudoharengus). Fish Physiology and Biochemistry, 38 (2): 363–373.CrossRefGoogle Scholar
  41. Stoknes, I., Kland, H., Falch, E., and Synnes, M., 2004. Fatty acid and lipid class composition in eyes and brain from teleosts and elasmobranchs. Comparative Biochemistry and Physiology B: Biochemistry & Molecular Biology, 138 (2): 183–191.CrossRefGoogle Scholar
  42. Stubhaug, I., Lie, Ø., and Torstensen, B. E., 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. Aquaculture Nutrition, 13 (2): 145–155.CrossRefGoogle Scholar
  43. Tocher, D. R., and Glencross, B. D., 2015. Lipids and fatty acids. In: Dietary Nutrients, Additives and Fish Health. Lee, C., ed., John Wiley & Sons, Inc., USA, 355pp.CrossRefGoogle Scholar
  44. Wallaert, C., and Babin, P. J., 1994. Thermal adaptation affects the fatty acid composition of plasma phospholipids in trout. Lipids, 29 (5): 373–376.CrossRefGoogle Scholar
  45. Wijekoon, M. P. A., 2011. Effect of water temperature and diet on cell membrane fluidity and fatty acid composition of muscle, liver, gill and intestine mucosa of adult and juvenile steelhead trout, Oncorhynchus mykiss. PhD thesis. Memorial University of Newfoundland, St. John’s, Newfoundland, Canada.Google Scholar
  46. Wodtke, E., 1978. Lipid adaptation in liver mitochondrial membranes of carp acclimated to different environmental temperatures: Phospholipid composition, fatty acid pattern and cholesterol content. Biochimica Biophysica Acta–Lipids and Lipid Metabolism, 529 (2): 280–291.CrossRefGoogle Scholar
  47. Xu, H., Zhang, D., Yu, D., Lv, C., Luo, H., and Wang, Z., 2015. Molecular cloning and expression analysis of scd1 gene from large yellow croaker Larimichthys crocea under cold stress. Gene, 568 (1): 100–108.CrossRefGoogle Scholar
  48. Ye, C., Wan, F., Sun, Z., Cheng, C., Ling, R., Fan, L., and Wang, A., 2016. Effect of phosphorus supplementation on cell viability, anti–oxidative capacity and comparative proteomic profiles of puffer fish (Takifugu obscurus) under low temperature stress. Aquaculture, 452: 200–208.CrossRefGoogle Scholar
  49. Yeagle, P. L., 1989. Lipid regulation of cell membrane structure and function. The FASEB Journal, 3 (7): 1833–1842.CrossRefGoogle Scholar
  50. Zhang, S., Xu, J., Hou, Y., Xu, S., Miao, M., and Yan, X., 2010. Comparison of fatty acid composition among muscles and visceral organs of Trachinotus ovatus. Food Science, 31 (10): 192–195 (in Chinese with English abstract).Google Scholar

Copyright information

© Ocean University of China, Science Press and Springer-Verlag GmbH Germany 2019

Authors and Affiliations

  • Chengyue Liu
    • 1
    • 2
  • Shuanglin Dong
    • 1
    • 3
  • Yangen Zhou
    • 1
    • 3
    Email author
  • Kunpeng Shi
    • 1
  • Zhe Pan
    • 1
  • Dajiang Sun
    • 1
    • 3
  • Qinfeng Gao
    • 1
    • 3
  1. 1.Key Laboratory of Mariculture of Ministry of EducationOcean University of ChinaQingdaoChina
  2. 2.Key Laboratory of Tropical Marine Bio-Resources and Ecology, Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of OceanologyChinese Academy of SciencesGuangzhouChina
  3. 3.Function Laboratory for Marine Fisheries Science and Food Production ProcessesQingdao National Laboratory for Marine Science and TechnologyQingdaoChina

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