Abstract
We evaluated the effects of rearing temperature on the composition of fatty acids and stearoyl-CoA desaturase (SCD) activity and gene expression in GIFT (genetically improved farmed tilapia) tilapia. Three triplicate groups of fish were reared for 40 days at 22, 28, or 34 °C. At the end of the trial, the final body weight of juveniles reared at 28 °C was higher than that of fish reared at 22 or 34 °C. Feed intake, feed efficiency, and the protein efficiency ratio were also higher at 28 °C. The fatty acid composition of muscle tissue differed significantly (P < 0.05) among the treatment groups. The content of SFA decreased with decreasing temperature, whereas the UFA content increased. We observed high levels of PUFA, particularly n-3 PUFAs, in fish reared at the lower temperature. Rearing at low temperature significantly (P < 0.05) increased the expression and activity of the SCD gene. Increased SCD activity and gene expression can increase the biosynthesis of MUFAs in GIFT tilapia muscle. Additionally, cold acclimation can decrease the content of TC and TG in GIFT tilapia, which can help increase cold tolerance.
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Akhtara MS, Pal AK, Sahu NP, Ciji A, Mahanta PC (2014) Higher acclimation temperature modulates the composition of muscle fatty acid of Tor putitora juveniles. Weather Clim Extrem. doi:10.1016/j.wace.2014.03.001
Azaza MS, Dhraief MN, Kraiem MM (2008) Effects of water temperature on growth and sex ratio of juvenile Nile tilapia Oreochromis niloticus (Linneaus) reared in geothermal waters in southern Tunisia. J Therm Biol 192:132–145
Bowden LA, Restall CJ, Rowley AF (1996) The influence of environmental temperature on membrane fluidity, fatty acid composition and lipoxygenase product generation in head kidney leucoctyes of the rainbow trout, Oncorhynchus mykiss. Comp Biochem Physiol 115B:375–382
Brett MT, Müller-Navarra DC, Ballantyne AP, Ravet JL, Goldman CR (2006) Daphnia fatty acid composition reflects that of their diet. Limnol Oceanogr 51:2428–2437
Calabretti A, Cateni F, Procida G, Favretto LG (2003) Influence of environmental temperature on composition of lipids in edible flesh of rainbow trout (Oncorhynchus mykiss). J Sci Food Agric 83:1493–1498
Carine LL, Rosiele L, Marcia C, Vania PV, Carolina RG, Maria RCS, Bernardo B, Gilberto M, Vera MM (2004) Effect of different temperature regimes on metabolic and blood parameters of silver catfish Rhamdia quelen. Aquaculture 239:497–507
Chang BE, Hsieh SL, Kuo CM (2001) Molecular cloning of fulllength DNA encoding delta-9 desaturase through PCR strategies and its genomic organization and expression in grass carp (Ctenopharygodon idella). Mol Rep Dev 58:245–254
Charlotte W, Patrick JB (1994) Thermal adaptation affects the fatty acid composition of plasma phospholipids in trout. Lipids 29:373–376
Chatzifotis S, Panagiotidou M, Papaioannou N (2010) Effect of dietary lipid levels on growth, feed utilization, body composition and serum metabolites of meager (Argyrosomus regius) juveniles. Aquaculture 307:65–70
Cheng SD, Li WY (2004) Overview of essential fatty acid of fish. Curr Fish 10:39–41 (in Chinese)
Cheng HL, Xia DQ, Wu TT (2006) Fatty liver and regulation of lipids metabolism in fish. Chin J Anim Nutr 18:294–298 (in Chinese)
Chou BS, Shiau SY (1999) Both n-6 and n-3 fatty acids are required for maximal growth of juvenile hybrid tilapia. N Am J Aquac 61:13–20
Clark S, Whitmore DH Jr, McMahon RF (1979) Considerations of blood parameters of largemouth bass, Miicropterus salmoides. J Fish Biol 14:147–158
Cordier M, Brichon G, Weber JM, Zwingelstein G (2002) Changes in the fatty acid composition of phospholipids in tissues of farmed sea bass (Dicentrarchus labrax) during an annual cycle. Roles of environmental temperature and salinity. Comp Biochem Physiol 133:281–288
Cui SL, Liu B, Xu P, Xie J, Wang JJ, Zhou M (2013) Effect of emodin on growth, haemotological parameters and HSP70 mRNA expression of Wuchang bream (Megalobrama amblycephala) at two temperatures. Acta Hydrobiol Sin 37:919–928 (in Chinese)
Ding J, Sun W, Chang YQ (2012) Cloning and expression of stearoyl-coenzyme A desaturase and protein tyrosine phosphatase 1B genes from sea urchin Strongylocentrotus intermedius. J Dali Ocean Univ 27:489–494 (in Chinese)
Douglas RT, John DC, James RD, John RS (1994) Effects of salinity on the growth and lipid composition of Atlantic salmon (Salmo salar) and turbot (Scophthalmus maximus) cells in culture. Fish Physiol Biochem 13:451–461
Du ZY, Liu YJ, Zheng WH, Tian LX, Liang GY (2002) The effects of three oil sources and two anti fat liver factors on the growth, nutrient composition and serum biochemistry indexes of Lateolabrax japonicus. J Fish China 26:542–550 (in Chinese)
Duan ZG, Wu JY, Li WS (2011) Research progress on effects of low temperature on tilaplia. South China Fish Sci 7:77–81 (in Chinese)
Dzikowski R, Hulata G, Karplus I, Harpaz S (2001) Effect of temperature and dietary L-carnitine supplementation on reproductive performance of female guppy (poecilia reticulata). Aquaculture 199:323–332
Eilander A, Hundscheid DC, Osendarp SJ, Transler C, Zock PL (2007) Effects of n-3 long chain polyunsaturated fatty acid supplementation on visual and cognitive development throughout childhood: a review of human studies. Prostag Leukotr ESS 76:189–203
Elliot JM (1972) Rates of gastric evacuation in brown trout, Salmo trutta (L.). Freshw Biol 2:1–18
Ellis AE (1981) Stress and modulation of defence mechanisms in fish. In: Pickering AD (ed) Stress and fish. Academic Press, London, pp 147–169
Farkas T (1980) Metabolism of fatty acids in fish: III. Combined effect of environmental temperature and diet on formation and deposition of fatty acids in the carp, Cyprineus carpio Limaeus 1758. Aquaculture 20:29–40
Folch J, Lees M, Stanley GH (1957) A simple method for isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509
Guerreiro H, Peres M, Castro-cunha M, Oliver-teles A (2012) Effect of temperature and dietary protein/lipid ratio on growth performance and nutrient utilization of juvenile Senegalese sole (Solea senegalensis). Aquacul Nutr 18:98–106
Han JC, Liu GY, Mei PS, Huang YP, Liu DF, Chen QW (2010) Effects of temperature on the hematological indices and digestive enzyme activities of Crucian Carp (Carassius auratus). J Hydroecol 3:87–92 (in Chinese)
Harikrishnan R, Kim MC, Kim JS, Balasundaram C, Heo MS (2011) Protective effect of herbal and probiotics enriched diet on haematological and immunity status of Oplegnathus fasciatus (Temminck & Schlegel) against Edwardsiella tarda. Fish Shellfish Immunol 30:886–893
Hazel JR (1984) Effect of temperature on the structure and metabolism of cell membranes in fish. Am J Physiol 246:460–470
Hazel JR, Williams EE (1990) The role of alterations in membrane lipid composition in enabling physiological adaptations of organisms to their physical environment. Prog Lipid Res 29:167–227
He X, Dai QZ, Zhang SR, Hu Y, Jiang GT (2007) Effects of dietary supplementation with conjugated lionleic acid on growth performance and lipids metabolism of two broiler breeds. Chin J Anim Nutr 19:581–587 (in Chinese)
Heinemann FS, Ozols J (2003) Stearoyl-CoA desaturase, a short-lived protein of endoplasmic reticulum with multiple control mechanisms. Prostag Leukotr E 68:123–133
Hilditch TP, Williams PN (1964) The chemical condition of natural fat. Chapman and Hall, London
Hiraoka Y, Nakagawa H, Murachi S (1979) Blood Proportions of rainbow trout in acute hepatotoxity (sic) by carbon tetrachloride. Bull Jpn Soc Sci Fish 45:527–532
Hsieh SL, Kuo CM (2005) Stearoyl-CoA desaturase expression and fatty acid composition in milkfish (Chanos chanos) and grass carp (Ctenopharyngodon idella) during cold acclimation. Comp Biochem Physiol 141B:95–101
Hsieh SL, Liao WL, Kuo CM (2001) Molecular cloning and sequence analysis of stearoyl-CoA desaturase in milkfish, Chanos chanos. Comp Biochem Physiol 130B:467–477
Hsieh SL, Liao WL, Kuo CM (2002) Fatty acid desaturation and stearoyl-CoA desaturase expression in the hepatic microsomes of milkfish, Chanos chanos, under cold shock. J Fish Soc Taiwan 29:31–43
Hsieh SL, Chen YN, Kuo CM (2003) Physiological responses, desaturase activity, and fatty acid composition in milkfish (Chanos chanos) under cold acclimation. Aquaculture 220:903–918
Hsieh SL, Chang HT, Wu CH, Kuo CM (2004) Cloning, tissue distribution and hormonal regulation of stearoyl-CoA desaturase in tilapia, Oreochromis mossambicus. Aquaculture 230:527–546
Hsieh SL, Hu CY, Hsu YT, Hsieh TJ (2007) Influence of dietary lipids on the fatty acid composition and stearoyl-CoA desaturase expression in hybrid tilapia (Oreochromis niloticus × O. aureus) under cold shock. Comp Biochem Physiol 147B:438–444
Huang MH (2008) Analysis and suggestion about tilapia’s large area death from cold in Guangdong. Ocean Fish 3:15–16 (in Chinese)
Huang CH, Huang MC, Hou PC (1998) Effect of dietary lipids on fatty acid composition and lipid peroxidation in sarcoplasmic reticulum of hybrid tilapia, Oreochromis niloticus × O. aureus. Comp Biochem Physiol 120A:331–336
Jeffcoat R, Brawn PR, Safford R, James AT (1977) Properties of rat liver microsome stearoyl-coenzyme A desaturase. Biochem J 161:431–437
Jorge H, Ana MP, Mariano L, Maria TV (2013) Effect of lipid composition of diets and environmental temperature on the performance and fatty acid composition of juvenile European abalone (Haliotis tuberculata L. 1758). Aquaculture 412–413:34–40
Kemp P, Smith MW (1980) Effect of temperature acclimatization on the fatty acid composition of goldfish intestinal lipids. Biochem J 117:9–15
Kheriji S, Cafsi MEL, Masmoudi W, Castell JD, Romdhane MS (2003) Salinity and temperature effects on the lipid composition of mullet sea fry (Mugil cephalus, Linne, 1758). Aquac Int 11:571–582
Li J, Huang GQ, Zhang XM, Wei LZ, Tang X (2010) The growth, energy allocation, and body composition of the brown flounder (Paralichthys olivaceus) during the cycles of high temperature-optimal temperature operation. J Fish China 34:1236–1243 (in Chinese)
Likongwe JS, Stecko TD, Stauffer JR, Carline RF (1996) Combined effects of water temperature and salinity on growth and feed utilization of juvenile Nile tilapia Oreochromis niloticus (Linneaus). Aquaculture 146:37–46
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408
Logue JA, Devries AL, Fodor E, Cossins AR (2000) Lipid compositional correlates of temperature-adaptive interspecific differences in membrane physical structure. J Exp Biol 203:2105–2115
Lu Y, Yang YH, Wang YY, Wang L, Wang RX (2010) Effects of different replacement ratio of fish meal by extruded soybean meal on growth, body composition and hematology indices of rainbow trout (Oncorhynchus mykiss). Chin J Anim Nutr 22:221–227 (in Chinese)
Makoto O, Masazumi N, Tadashi N (1989) Involvement of prostaglandins in the spawning of the scallop, Patinopecten yessoensis. Comp Biochem Physiol 94C:595–601
Michel C, Gerard B, Jean-Michel W, Georges Z (2002) Changes in the fatty acid composition of phospholipids in tissues of farmed sea bass (Dicentrarchus labrax) during an annual cycle. Roles of environmental temperature and salinity. Comp Biochem Physiol 133B:281–288
Monroig O, Tocher DR, Navarro JC (2012) Isolation and functional characterisation of a stearoyl-CoA desaturase from the marine invertebrate Octopus vulgaris. Comp Biochem Physiol 163:46–47
Mu CK, Wang CL (2003) Recent advance in essential fatty acid nutrition of fish. Beverage Ind 24:44–46 (in Chinese)
Musuka CG, Likongwe JS, Kang’ombe J, Jere WWL, Mtethiwa AH (2009) The effect of dietary protein and water temperatures on performance of T. rendalli juveniles reared in indoor tanks. Pak J Nutr 8:1526–1531
Nanton DA, Castell JD (1999) The effects of temperature and dietary fatty acids on the fatty acid composition of harpacticoid copepods, for use as a live food for marine fish larvae. Aquaculture 175:167–181
Olsen RE, Lovaas E, Lie O (1999) The influence of temperature, dietary polyunsaturated fatty acids, α-tocopherol and spermine on fatty acid composition and indices of oxidative stress in juvenile Arctic char, Salvelinus alpinus (L.). Fish Physiol Biochem 20:13–29
Patricia A, Ana LM, Narcisa MB, Tiago R, Maria LN, Rui R, António M (2014) Effect of warming on protein, glycogen and fatty acid content of native and invasive clams. Food Res Int 64:439–445
Peng G, Du YL, Xu SM, Liu PS (2011) Stearoyl-CoA desaturase-1 and lipid metabolism. Chin Bull Life Sci 23:1101–1105 (in Chinese)
Perhar G, Arhonditsis GB, Brett MT (2013) Modelling the role of highly unsaturated fatty acids in planktonic food web processes: sensitivity analysis and examination of contemporary hypotheses. Ecol Inf 13:77–98
Plummer P (1987) Glycogen determination in animal tissues. In: Plummer P (ed) An introduction to practical biochemistry, Third edn. McGraw Hill Book, Maidenhead, p 332
Qiang J, Yang H, Wang H, Kpundeh MD, Xu P (2012) Growth and IGF-I response of juvenile Nile tilapia (Oreochromis niloticus) to changes in water temperature and dietary protein level. J Therm Biol 37:686–695
Qiang J, Yang H, Wang H, Kpundeh MD, Xu P (2013) Interacting effects of water temperature and dietary protein level on hematological parameters in Nile tilapia juveniles, Oreochromis niloticus (L.) and mortality under Streptococcus iniae infection. Fish Shellfish Immunol 34:8–16
Ren HT, Yu JH, Xu P, Tang YK (2012) Influence of dietary fatty acids on muscle fatty acid composition and expression levels of Δ6 desaturase-like and Elovl5-like elongase in common carp (Cyprinus carpiovar. Jian). Comp Biochem Physiol 163B:84–192
Sargent JR, Tacon AGJ (1999) Development of farmed fish: a nutritionally necessary alternative to meat. Proc Nutr Soc 58:377–383
Shen JM, Li RD, Gao FY (2005) Effect of ambient temperature on lipid and fatty acid composition in the oviparous lizards, Phrynocephalus przewalskii. Comp Biochem Physiol 142B:293–301
Sheridan MA (1994) Regulation of lipid metabolism in poikilothermic vertebrates. Comp Biochem Physiol 107B:495–508
Singh RK, Desai AS, Chavan SL (2009) Effect of water temperature on dietary protein requirement, growth and body composition of Asian catfish, Clarias batrachus fry. J Therm Biol 34:8–13
Skalli JH, Robin N, Le Bayon H, Delliou L, Person-Le Ruyet J (2006) Impact of essential fatty acid deficiency and temperature on tissues’ fatty acid composition of European sea bass (Dicentrarchus labrax). Aquaculture 255:223–232
Slater CH, Schreck CB (1998) Season and physiological parameters modulate salmonid leucocyte androgen receptor affinity and abundance. Fish Shellfish Immunol 8:379–391
Sprecher H (2000) Metabolism of highly unsaturated n-3 and n-6 fatty acids. Biochim Biophys Acta 1486:219–231
Stoffel W, Ach KL (1964) The metabolism of unsaturated fatty acids: II. Properties of the chain-elongating enzyme. Apropos of the biohydrogenation of unsaturated fatty acids Hoppe-Seylers Z. Physiol Chem 337:123–133
Tibor F, Istvan C (1976) Biosynthesis of fatty acids by the carp, Cyprinus carpio L., in relation to environmental temperature. Lipid 11:401–407
Tiku PE, Gracey AY, Macartney AI, Beynon RJ, Cossins AR (1996) Cold-induced expression of delta 9-desaturase in carp by transcriptional and posttranslational mechanisms. Science 271:815–818
Trueman RJ, Tiku PE, Caddick MX, Cossins AR (2000) Thermal thresholds of lipid restructuring and delta 9-desaturase expression in the liver of carp (Cyprinus carpio L.). J Exp Biol 203:641–650
Van Kampen EJ, Zijlstra NC (1961) Determination of haemoglobin. Clin Chim Acta 5:719–720
Wang K, Han Y, Dong JG, Hao QR, Zhao RW, Chen XT (2012) Comparison of fatty acids and blood indexes between wild and cultured populations of Culter alburnus in Xingkai Lake. Freshw Fish 42:14–18 (in Chinese)
Waters KM, Ntambi JM (1996) Polyunsaturated fatty acids inhibit hepatic stearoyl-CoA desaturase-1 gene in diabetic mice. Lipids 31:33–36
Wei GL, Xu GC, Gu RB, Xu P (2014) Effects of unsaturated fatty acids on lipid metabolism enzyme activities and muscle components of juvenile Coilia nasus. J Anim Nutr 26:270–278 (in Chinese)
Wodtke E, Cossins AR (1991) Rapid cold-induced changes of membrane order and activity in endoplasmic reticulum of carp liver: a time-course study of thermal acclimation. Biochim Biophys Acta 1064:343–350
Wu YS, Dong GZ, Wang LC, Huang Y, Yu CF, Li ZQ (2000) Effect of chromium-niacin complex supplementation on performance, carcass composition, and blood biochemical parameters in meat-type duck. Acta Zoo Nutrimenta Sinica 12:20–25 (in Chinese)
Xiang X, Chen J, Zhou XH, Li DJ, Wang WJ (2010) Effects of five lipid sources on growth performance and serum biochemical indices of Schizothorax prenanti. Chin J Anim Nutr 22:498–507 (in Chinese)
Xu XL, Ji WJ, Castell JD, O’Dor RK (1994) Influence of dietary lipid sources on fecundity, egg hatchability and fatty acid composition of Chines prawn (Penaus chinensis) broodstock. Aquaculture 119:359–370
Yue YF, Peng SM, Shi ZH, Yin F, Sun P (2011) The effects of fatty acid nutrition on the growth, lipid metabolism and immune performance of the fish. Mod Fish Inf 26:13–19 (in Chinese)
Zhang GL (1991a) The measurements of haematology index of rainbow trout. Salmon Fish 4:82–83 (in Chinese)
Zhang XG (1991b) Study on some blood parameters of Nile tilapia with temperature. Freshw Fish 2:15–17 (in Chinese)
Zhang LJ, Yang HB, Zhang JJ, Cai C (2010) The content of fatty acids in different tissue of tilapia (Qreochromis niloticus). Freshw Fish 40:36–40 (in Chinese)
Zhang R, Zhang YH, Shao D, Wang LD, Gong DQ (2013) The function and regulation of stearoyl-CoA desaturase gene. Chin Bull Life Sci 25:378–382 (in Chinese)
Zhi BJ, Liu W, Wang LB, Duan YY, Chen J (2008) The effect of water temperature on hematology indices of silurus soldatovi. Chin J Fish 21:64–70 (in Chinese)
Zhu RY, Shen WY (2002) Effect of Starvation and Refeeding on Glycogen Metabolism in Grass Carp (Ctenopharyngodon idellus) Fingerling. J Shaoxing Univ 22:23–25 (in Chinese)
Acknowledgments
This study was financed by the following grants: Special Fund for Agro-scientific Research in the Public Interest (2015JBFR04) and the National Science & Technology Program (2012BAD26B03-1). We thank the anonymous reviewers for their advice.
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Ma, X.Y., Qiang, J., He, J. et al. Changes in the physiological parameters, fatty acid metabolism, and SCD activity and expression in juvenile GIFT tilapia (Oreochromis niloticus) reared at three different temperatures. Fish Physiol Biochem 41, 937–950 (2015). https://doi.org/10.1007/s10695-015-0059-4
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DOI: https://doi.org/10.1007/s10695-015-0059-4