Abstract
In the present study, juvenile rainbow trout (Oncorhynchus mykiss) were acclimated at 5 temperatures. Fish in the control group (C0) were reared at a constant temperature (16°C); trout in four other treatments (A0, A3, A6, and A9) were acclimated to a high temperature (22°C) for 0, 3, 6, and 9 d, respectively, and then returned to normal temperature (16°C) for 7 d. The temperature was then raised to 20°C and the fish were cultured for 40 d. The results showed that the growth rates of A3, A6, and A9) were higher than that of A0 but lower than that of C0. The growth rate of A9 was the highest among the 4 acclimation groups. The activities of serum transaminase and liver antioxidant enzyme significantly increased during acclimation. At the beginning of growth, the activities of enzymes were lower in A3, A6, and A9 with the lowest in A9. In addition, the transcript abundance of heat shock protein (HSP) 60 gene in A9 was not significantly different from that of C0 during growth. HSP70 in A9 significantly increased at the beginning and returned to that of C0 at the end. Our findings indicated that pre-acclimation improved the high temperature tolerance with the best effectiveness observed at 22°C for 9 d. A possible mechanism underlining such phenomenon is the improvement of antioxidant defense system.
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Afonso, L. O. B., Hosoya, S., Osborne, J., Gamperl, A. K., and Johnson, S., 2008. Lack of glucose and hsp70 responses in haddock Melanogrammus aeglefinus (L.) subjected to handling and heat shock. Journal of Fish Biology, 72(1): 157–167.
Arai, A., Mitani, H., Naruse, K., and Shima, A., 1994. Relationship between the induction of proteins in the Hsp70 family and thermosensitivity in 2 species of Oryzias (Pisces). Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology, 109(4): 647–654.
Bahrndorff, S., Maien, J., Loeschcke, V., and Ellers, J., 2009. Dynamics of heat-induced thermal stress resistance and Hsp70 expression in the springtail, Orchesella cincta. Functional Ecology, 23(2): 233–239.
Beitinger, T. L., and Bennett, W. A., 2000. Quantification of the role of acclimation temperature in temperature tolerance of fishes. Environmental Biology of Fishes, 58(3): 277–288.
Besson, M., Vandeputte, M., van Arendonk, J. A. M., Aubin, J., de Boer, I. J. M., Quillet, E., and Komen, H., 2016. Influence of water temperature on the economic value of growth rate in fish farming: The case of sea bass (Dicentrarchus labrax) cage farming in the Mediterranean. Aquaculture, 462: 47–55.
Brown, M. A., Upender, R. P., Hightower, L. E., and Renfro, J. L., 1992. Thermoprotection of a functional epithelium: Heat stress effects on transepithelial transport by flounder renal tubule in primary monolayer-culture. Proceedings of the National Academy of Sciences of the United States of America, 89(8): 3246–3250.
Calosi, P., Bilton, D. T., Spicer, J. I., Votier, S. C., and Atfield, A., 2010. What determines a species’ geographical range? Thermal biology and latitudinal range size relationships in European diving beetles (Coleoptera: Dytiscidae). Journal of Animal Ecology, 79(1): 194–204.
Chance, B., Sies, H., and Boveris, A., 1979. Hydroperoxide metabolism in mammalian organs. Physiological Reviews, 59(3): 527–605.
Choresh, O., Ron, E., and Loya, Y., 2001. The 60-kDa heat shock protein (HSP60) of the sea anemone Anemonia viridis: A potential early warning system for environmental changes. Marine Biotechnology (NY), 3(5): 501–508.
Chung, D. J., Bryant, H. J., and Schulte, P. M., 2017. Thermal acclimation and subspecies-specific effects on heart and brain mitochondrial performance in a eurythermal teleost (Fundulus heteroclitus). Journal of Experimental Biology, 220(8): 1459–1471.
Davies, K. J., 1995. Oxidative stress: The paradox of aerobic life. Biochemical Society Symposium, 61: 1–31.
Dominguez, M., Takemura, A., Tsuchiya, M., and Nakamura, S., 2004. Impact of different environmental factors on the circulating immunoglobulin levels in the Nile tilapia, Oreochromis niloticus. Aquaculture, 241(1-4): 491–500.
Dong, S. L., 2019. Research progress and prospect on large Salmonidae farming at the areas of Cold Water Mass in Yellow Sea. Periodical of Ocean University of China, 49(3): 1–6 (in Chinese with English abstract).
Dowd, W. W., Brill, R. W., Bushnell, P. G., and Musick, J. A., 2006. Standard and routine metabolic rates of juvenile sandbar sharks (Carcharhinus plumbeus), including the effects of body mass and acute temperature change. Fishery Bulletin, 104(3): 323–331.
Feder, M. E., and Hofmann, G. E., 1999. Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Annual Review of Physiology, 61: 243–282.
Gedamu, L., Culham, B., and Heikkila, J. J., 1983. Analysis of the temperature-dependent temporal pattern of heat-shock-protein synthesis in fish cells. Bioscience Reports, 3(7): 647–658.
Halliwell, B., and Gutteridge, J. M. C., 1995. The definition and treatment of antioxidants in biological systems. Free Radical Biology and Medicine, 18(1): 125–126.
He, Y. F., Wu, X. B., Zhu, Y. J., Li, H. C., Li, X. M., and Yang, D. G., 2014. Effect of rearing temperature on growth and thermal tolerance of Schizothorax (Racoma) kozlovi larvae and juveniles. Journal of Thermal Biology, 46: 24–30.
Huang, W. J., Leu, J. H., Tsau, M. T., Chen, J. C., and Chen, L. L., 2011. Differential expression of LvHSP60 in shrimp in response to environmental stress. Fish & Shellfish Immunology, 30(2): 576–582.
Irwin, F., 1995. Superoxide radical and superoxide dismutases. Annual Review of Biochemistry, 64(1): 97–112.
Kalmar, B., and Greensmith, L., 2009. Induction of heat shock proteins for protection against oxidative stress. Advanced Drug Delivery Reviews, 61(4): 310–318.
Li, J., Zhang, Y., Liu, Y., Zhang, Y., Xiao, S., and Yu, Z., 2016. Co-expression of heat shock protein (HSP) 40 and HSP70 in Pinctada martensii response to thermal, low salinity and bacterial challenges. Fish & Shellfish Immunology, 48: 239–243.
Li, M., Li, X. J., Lu, J. H., and Huo, M. F., 2018. The effect of acclimation on heat tolerance of Lasioderma serricorne (Fabricius) (Coleoptera: Anobiidae). Journal of Thermal Biology, 71: 153–157.
Linton, T. K., Morgan, I. J., Reid, S. D., and Wood, C. M., 1998. Long-term exposure to small temperature increase and sublethal ammonia in hard water acclimated rainbow trout: Does acclimation occur? Aquatic Toxicology, 40(2-3): 171–191.
Liu, Y., Ma, D., Zhao, C., Xiao, Z., Xu, S., Xiao, Y., Wang, Y., Liu, Q., and Li, J., 2017. The expression pattern of hsp70 plays a critical role in thermal tolerance of marine demersal fish: Multilevel responses of Paralichthys olivaceus and its hybrids (P. olivaceus ♀ × P. dentatus ♂) to chronic and acute heat stress. Marine Environmental Research, 129: 386–395.
Madeira, C., Mendonca, V., Leal, M. C., Flores, A. A. V., Cabral, H. N., Diniz, M. S., and Vinagre, C., 2017. Thermal stress, thermal safety margins and acclimation capacity in tropical shallow waters–An experimental approach testing multiple end-points in two common fish. Ecological Indicators, 81: 146–158.
Madeira, D., Narciso, L., Cabral, H. N., Diniz, M. S., and Vinagre, C., 2014. Role of thermal niche in the cellular response to thermal stress: Lipid peroxidation and HSP70 expression in coastal crabs. Ecological Indicators, 36: 601–606.
Madeira, D., Narciso, L., Cabral, H. N., Vinagre, C., and Diniz, M. S., 2013. Influence of temperature in thermal and oxidative stress responses in estuarine fish. Comparative Biochemistry and Physiology A-Molecular & Integrative Physiology, 166(2): 237–243.
Martin, J., Horwich, A. L., and Hartl, F. U., 1992. Prevention of protein denaturation under heat stress by the chaperonin Hsp60. Science, 258(5084): 995–998.
Mayer, M. P., and Bukau, B., 2005. Hsp70 chaperones: Cellular functions and molecular mechanism. Cellular and Molecular Life Sciences, 62(6): 670–684.
Md Mizanur, R., Yun, H., Moniruzzaman, M., Ferreira, F., Kim, K. W., and Bai, S. C., 2014. Effects of feeding rate and water temperature on growth and body composition of juvenile Korean rockfish, Sebastes schlegeli (Hilgendorf 1880). Asian-Australasian Journal of Animal Sciences, 27(5): 690–699.
Meyer, H., and Santarius, K. A., 1998. Short-term thermal acclimation and heat tolerance of gametophytes of mosses. Oecologia, 115(1-2): 1–8.
Nakano, K., and Iwama, G., 2002. The 70-kDa heat shock protein response in two intertidal sculpins, Oligocottus maculosus and O. snyderi: Relationship of hsp70 and thermal tolerance. Comparative Biochemistry Physiology A-Molecular & Integrative Physiology, 133(1): 79–94.
Nytro, A. V., Vikingstad, E., Foss, A., Hangstad, T. A., Reynolds, P., Eliassen, G., Elvegard, T. A., Falk-Petersen, I. B., and Imsland, A. K., 2014. The effect of temperature and fish size on growth of juvenile lumpfish (Cyclopterus lumpus L.). Aquaculture, 434: 296–302.
Ohashi, K., Burkart, V., Flohe, S., and Kolb, H., 2000. Cutting edge: Heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. Journal of Immunology, 164(2): 558–561.
Parsell, D. A., and Lindquist, S., 1993. The function of heatshock proteins in stress tolerance–Degradation and reactivation of damaged proteins. Annual Review of Genetics, 27: 437–496.
Pauly, D., and Zeller, D., 2017. Comments on FAOs State of World Fisheries and Aquaculture (SOFIA 2016). Marine Policy, 77: 176–181.
Pfaffl, M. W., 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29(9): e45–e45.
Pirozzi, I., and Booth, M. A., 2009. The routine metabolic rate of mulloway (Argyrosomus japonicus: Sciaenidae) and yellowtail kingfish (Seriola lalandi: Carangidae) acclimated to six different temperatures. Comparative Biochemistry and Physiology A - Molecular & Integrative Physiology, 152(4): 586–592.
Ronisz, D., Larsson, D. G. J., and Forlin, L., 1999. Seasonal variations in the activities of selected hepatic biotransformation and antioxidant enzymes in eelpout (Zoarces viviparus). Comparative Biochemistry and Physiology C-Pharmacology Toxicology & Endocrinology, 124(3): 271–279.
Sappal, R., Fast, M., Stevens, D., Kibenge, F., Siah, A., and Kamunde, C., 2015. Effects of copper, hypoxia and acute temperature shifts on mitochondrial oxidation in rainbow trout (Oncorhynchus mykiss) acclimated to warm temperature. Aquatic Toxicology, 169: 46–57.
Scharf, I., Galkin, N., and Halle, S., 2015. Disentangling the consequences of growth temperature and adult acclimation temperature on starvation and thermal tolerance in the red flour beetle. Evolutionary Biology, 42(1): 54–62.
Schram, E., Bierman, S., Teal, L. R., Haenen, O., van de Vis, H., and Rijnsdorp, A. D., 2013. Thermal preference of juvenile Dover sole (Solea solea) in relation to thermal acclimation and optimal growth temperature. PLoS One, 8(4): e61357.
Semsar-kazerouni, M., and Verberk, W. C. E. P., 2018. It’s about time: Linkages between heat tolerance, thermal acclimation and metabolic rate at different temporal scales in the freshwater amphipod Gammarus fossarum Koch, 1836. Journal of Thermal Biology, 75: 31–37.
Seveso, D., Montano, S., Strona, G., Orlandi, I., Galli, P., and Vai, M., 2014. The susceptibility of corals to thermal stress by analyzing Hsp60 expression. Marine Environmental Research, 99: 69–75.
Sharma, J., Singh, S. P., and Chakrabarti, R., 2017. Effect of temperature on digestive physiology, immune-modulatory parameters, and expression level of Hsp and LDH genes in Catla catla (Hamilton, 1822). Aquaculture, 479: 134–141.
Sharma, S., Reddy, P. V. J., Rohilla, M. S., and Tiwari, P. K., 2006. Expression of HSP60 homologue in sheep blowfly Lucilia cuprina during development and heat stress. Journal of Thermal Biology, 31(7): 546–555.
Sharp, V. A., Miller, D., Bythell, J. C., and Brown, B. E., 1994. Expression of low-molecular-weight Hsp-70 related polypeptides from the symbiotic sea-anemone Anemonia viridis Forskall in response to heat-shock. Journal of Experimental Marine Biology and Ecology, 179(2): 179–193.
Shatilina, Z. M., Riss, H. W., Protopopova, M. V., Trippe, M., Meyer, E. I., Pavlichenko, V. V., Bedulina, D. S., Axenov-Gribanov, D. V., and Timofeyev, M. A., 2011. The role of the heat shock proteins (HSP70 and sHSP) in the thermotolerance of freshwater amphipods from contrasting habitats. Journal of Thermal Biology, 36(2): 142–149.
Shi, H. N., Liu, Z., Zhang, J. P., Kang, Y. J., Wang, J. F., Huang, J. Q., and Wang, W. M., 2015. Short communication: Effect of heat stress on heat-shock protein (Hsp60) mRNA expression in rainbow trout Oncorhynchus mykiss. Genetics and Molecular Research, 14(2): 5280–5286.
Solomon, J. M., Rossi, J. M., Golic, K., McGarry, T., and Lindquist, S., 1991. Changes in hsp70 alter thermotolerance and heat-shock regulation in Drosophila. The New Biologist, 3(11): 1106–1120.
Soltys, B. J., and Gupta, R. S., 1996. Immunoelectron microscopic localization of the 60-kDa heat shock chaperonin protein (Hsp60) in mammalian cells. Experimental Cell Research, 222(1): 16–27.
Sun, L. H., and Chen, H. R., 2014. Effects of water temperature and fish size on growth and bioenergetics of cobia (Rachycentron canadum). Aquaculture, 426: 172–180.
Tromp, J. J., Jones, P. L., Symonds, J. E., Walker, S. P., Pope, A., Pether, S. M. J., and Afonso, L. O. B., 2016. Effects of commercial diets and temperature on the growth performance and stress response of hapuku (Polyprion oxygeneios). Aquaculture, 452: 128–133.
Wang, X. R., Yan, B., Shi, M., Zhou, W., Zekria, D., Wang, H. Z., and Kai, G. Y., 2016. Overexpression of a Brassica campestris HSP70 in tobacco confers enhanced tolerance to heat stress. Protoplasma, 253(3): 637–645.
Wilhelm, D., and Boveris, A., 1993. Antioxidant defenses in marine fish. 2. Elasmobranchs. Comparative Biochemistry and Physiology C - Toxicology & Pharmacology, 106(2): 415–418.
Wilhelm, D., Giulivi, C., and Boveris, A., 1993. Antioxidant defenses in marine fish. 1. Teleosts. Comparative Biochemistry and Physiology C - Toxicology & Pharmacology, 106(2): 409–413.
Xie, Y. J., Song, L., Weng, Z. H., Liu, S. K., and Liu, Z. J., 2015. Hsp90, Hsp60 and sHsp families of heat shock protein genes in channel catfish and their expression after bacterial infections. Fish & Shellfish Immunology, 44(2): 642–651.
Young, P. S., and Cech, J. J., 1996. Environmental tolerances and requirements of splittail. Transactions of the American Fisheries Society, 125(5): 664–678.
Zhou, A., Xie, S., Wang, Z., Chen, Y., Zhang, Y., Fan, L., Zeng, F., and Zou, J., 2018. HSP60 expression profile under different extreme temperature stress in albino northern snakehead, Channa argus. Cell Stress Chaperones, 23(4): 791–796.
Acknowledgements
We would like to thank those who have critically reviewed this manuscript as well as those who helped in supporting this study at the Key Laboratory of Mariculture of Ministry of Education, Ocean University of China, Qingdao, China. This research was supported by the National Natural Science Foundation of China (Nos. 31572 634, 31702364 and 31872575), and the Shandong Province Key Research and Development Plan (Nos. 2016 CYJS04A01, 2017CXGC0106, 2017CXGC0102 and 2018 CXGC0101).
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Jiang, X., Dong, S., Zhou, Y. et al. An Effective Method of Prompting Juvenile Rainbow Trout (Oncorhynchus mykiss) to Cope with Heat Stress. J. Ocean Univ. China 19, 216–224 (2020). https://doi.org/10.1007/s11802-020-4124-y
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DOI: https://doi.org/10.1007/s11802-020-4124-y