Abstract
Global warming due to increasing temperature and contamination in aquatic environment has been found to be inducing cellular metabolic stress in fish. The present study focused on temperature and contamination in aquatic ecosystems and its alleviation/mitigation. Hence, this study was conducted to evaluate the role of zinc to improve growth performance, cellular metabolic stress, and digestive enzymes of the Pangasianodon hypophthalmus reared under lead (Pb) and high temperature. Two hundred and seventy-three fishes were distributed randomly into seven treatments, each with three replicates. Three isocaloric and isonitrogenous diets with graded levels of zinc at 0 mg/kg, 10 mg/kg, and 20 mg/kg were prepared. The Pb in treated water was maintained at the level of 1/21th of LC50 (4 ppm) and maintained at a temperature of 34 °C in exposure groups. The growth performance in terms of weight gain (%), protein efficiency ratio (PER), and specific growth rate (SGR) was found to be inhibited, and the feed conversion ratio (FCR) was enhanced in the Pb and high temperature–exposed group, whereas zinc supplementation has improved weight gain (%), FCR, PER, and SGR. The liver, gill, muscle, and kidney tissues of carbohydrate metabolic enzymes (LDH and MDH), protein metabolic enzymes (ALT and AST), and liver, gill, and muscle G6PDH and ATPase as well as intestinal digestives enzymes (proteases, amylase, and lipase) and intestinal ALP were significantly affected (p < 0.01) by Pb and high temperature exposure to P. hypophthalmus. We herein report the role of zinc in mitigating cellular metabolic stress in fish exposed to Pb and high temperature.
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References
Alayash AI (1989) Zinc and some zinc dependent enzymes in sickle cell anemia. Int J Vitam Nutr Res 59(4):388–389
APHA-AWWA-WEF (1998) Standard methods for the estimation of water and waste water. In: Clesceri LS, Greenberg AE, Eaton AD (eds) American Public Health Association, American Water Works Association, 20th edn. Water Environment Federation, Washington DC
Barroso JB, Peragon J, Garcıa-Salguero L, De la Higuera M, Lupianez JA (1999) Variations in the kinetic behaviour of the NADPH production systems in different tissues of the trout when fed on an amino-acid-based diet at different frequencies. Int J Biochem Cell Biol 31B:277–290
Carvalho SD, Negrao N, Bianco AC (1993) Hormonal regulation of malic enzyme and glucose-6-phosphate dehydrogenase in brown adipose tissue. Am J Phys 264(6):E874–E881
Chan S, Gerson B, Subramaniam S (1998) The role of copper, molybdenum, selenium, and zinc in nutrition and health. Clin Lab Med 18:673–685
Cherry IS, Crandell LA Jr (1932) The specificity of pancreatic lipase: its appearance in blood after pancreatic injury. Am J Phys 100:266–273
Daniela T, Munteanu MC, Andeea CS, Anca D (2012) Changes in lactate dehydrogenase activity in Carassius auratus gibelio (L. Pysces) kidney, gills and intestine induced by acute exposure to copper. Rom Biotech Lett 17(6):7873–7880
De Moss RD (1955) Glucose-6-phosphate and 6-phosphogluconic dehydrogenase from Leuconostoc mesenteroides. In: Colowick SP, Kalpan NO (eds) Methods in enzymology, vol I. Academic, New York, pp 328–332
Diez-Fernandez C, Sanz N, Cascales M (1996) Changes in glucose-6-phosphate dehydrogenase and malic enzyme gene expression in acute hepatic injury induced by thiochetamide. Biochem Pharmacol 51:1159–1163
Drapeau GR (1976) Protease from Staphylococcus aureus. Methods Enzymol 45:469–475
FAO (2014) Fishery and aquaculture statistics. PP 30
Fiess JC, Kunkel-Patterson A, Mathias L, Riley LG, Yancey PH, Hirano T, Grau EG (2007) Effects of environmental salinity and temperature on osmoregulatory ability, organic osmolytes, and plasma hormone profiles in the Mozambique tilapia (Oreochromis mossambicus). Comp Biochem Physiol A-Mol Integr Physiol 146:252–264
Fisk AT, de Wit CA, Wayland M, Kuzyk ZZ et al (2005) An assessment of the toxicological significance of anthropogenic contaminants in Canadian arctic wildlife. Sci Total Environ 351(352):57–93
Garen A, Levinthal CA (1960) Fine-structure genetic and chemical study of the enzyme alkaline phosphatase of E. coli. l. Purification and characterization of alkaline phosphatase. Biochem Biophys Acta 38:470–483
Hendy E, HA, Yousef MI, Abo El-Naga NI (2001) Effect of dietary zinc deficiency on hematological and biochemical parameters and concentrations of zinc, copper, and iron in growing rats. Toxicology 167:163–170
Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, Oxford
Hyun S, Lee T, Lee CH, Park YH (2006) The effects of metal distribution and anthropogenic effluents on the benthic environment of Gwangyang Bay, Korea. Mar Pollut Bull 52:113–120
Jurss K, Bastrop R (1995) Amino acid metabolism in fish (chapter 7). In: W.H.A.T. P (ed) Biochemistry and molecular biology of fishes. Elsevier, In, pp 159–189
Kletzien RF, Harris PKW, Foellmi LA (1994) Glucose-6-phosphate dehydrogenase: a “housekeeping” enzyme subject to tissue specific regulation by hormones, nutrients, and oxidant stress. FASEB J 8(2):174–181
Kumar N, Jadhao SB, Chandan NK, Rana RS (2011a) Dietary choline, betaine and lecithin mitigates endosulfan induced stress in Labeo rohita fingerlings. Fish Physiol Biochem 38:989–1000
Kumar N, Prabhu AJ, Pal AK, Remya S, Aklakur M, Rana RS, Gupta S, Raman RP, Jadhao SB (2011b) Anti-oxidative and immuno-hematological status of Tilapia (Oreochromis mossambicus) during acute toxicity test of endosulfan. Pestic Biochem Physiol 99:45–52
Kumar N, Jadhao S.B, Chandan NK, Akhlak MD, Rana RS (2012) Methyl donors potentiates growth, metabolic status and neurotransmitter enzyme in Labeo rohita fingerlings exposed to endosulfan and temperature. Fish Physiol Biochem 38(5), 1343–1353
Kumar N, Sharma R, Tripathi G, Kumar K, Dalvi RS, Krishna G (2014a) Cellular metabolic, stress and histological response on exposure to acute toxicity of endosulfan in Tilapia (Oreochromis mossambicus). Environ Toxicol 31(1):106–115
Kumar N, Gupta S, Chandan NK, Aklakur M, Pal AK, Jadhao SB (2014b) Lipotropes protect against pathogen-aggravated stress and mortality in low dose pesticide-exposed fish. PLoS One 9(4):e93499
Kumar N, Ambasankar K, Krishnani KK, Gupta SK, Bhushan S, Minhas PS (2016a) Acute toxicity, biochemical and histopathological responses of endosulfan in Chanos chanos. Ecotoxicol Environ Saf 131:79–88
Kumar N, Ambasankar K, Krishnani KK, Bhushan S, Minhas PS (2016b) Dietary pyridoxine protects against stress and maintains immune-hematological status in Chanos chanos exposed to endosulfan. Basic Clin Pharmacol Toxicol 119:297–308
Kumar N, Ambasankar K, Krishnani KK, Kumar P, Akhtar MS, Bhushan S, Minhas PS (2016c) Dietary pyridoxine potentiates thermal tolerance, heat shock protein and protect against cellular stress of milk fish (Chanos chanos) under endosulfan-induced stress. Fish Shellfish Immunol 55:407–414
Kumar N, Krishnani KK, Meena KK, Gupta SK, Singh NP (2017a) Oxidative and cellular metabolic stress of Oreochromis mossambicus as biomarkers indicators of trace element contaminants. Chemosphere 171:265–274
Kumar N, Krishnani KK, Gupta SK, Singh NP (2017b) Selenium nanoparticles enhanced thermal tolerance and maintain cellular stress protection of Pangasius hypophthalmus reared under lead and high temperature. Respir Physiol Neurobiol 246:107–116
Kumar N, Ambasankar K, Krishnani KK, Gupta S, Minhas PS (2017c) Dietary pyridoxine promotes growth and cellular metabolic plasticity of Chanos chanos fingerlings exposed to endosulfan induced stress. Aquac Res 48(5):2074–2087
Kumar N, Krishnani KK, Brahmane MP, Gupta SK, Kumar P, Singh NP (2018a) Temperature induces lead toxicity in Pangasius hypophthalmus: an acute test, antioxidative status and cellular metabolic stress. Int J Environ Sci Technol 15(1):57–68
Kumar N, Krishnani KK, Kumar P, Sharma R, Baitha R, Singh DK, Singh NP (2018b) Dietary nano-silver: does support or discourage thermal tolerance and biochemical status in air-breathing fish reared under multiple stressors? J Therm Biol 77:111–121
Kumar N, Gupta SK, Bhushan S, Singh NP (2019) Impacts of acute toxicity of arsenic (III) alone and with high temperature on stress biomarkers, immunological status and cellular metabolism in fish. Aquat Toxicol 4:214 105233
Lakshmi R, Kundu R, Thomas E, Mansuri AP (1991) Mercuric chloride induced inhibition of acid and alkaline phosphatase activity in the kidney of mudskipper; Boleophthalmus dentatus. Acta Hydrochim Hydrobiol 19(3):341–344
Lefevre S, Jensen FB, Huong do TT, Wang T, Phuong NT, Bayley M (2011) Effects of nitrite exposure on functional haemoglobin levels, bimodal respiration, and swimming performance in the facultative air-breathing fish Pangasianodon hypophthalmus. Aquat Toxicol 104(1–2):86–93
Lefevre S, Bayley M, Wang T, Malate H, Do Thanh H, Van Cong N (2008) Critical oxygen tension and the effect of hypoxia on the oxygen consumption of the striped catfish, Pangasius hypophthalmus (Pangasiidae). Comp Biochem Physiol A Mol Integr Physiol 150(3):S119–S120
Legendre M, Pouyaud L, Slembrouck J, Gustiano, R, Kristanto, AH, Subagja J, Komuradin O, Maskur (2000) Pangasius djambal: a new candidate species for fish culture in Indonesia. IARD J 22: 7–19
Lemieux H, Blier P, Dutil JD (1999) Do digestive enzymes set a physiological limit on growth rate and food conversion efficiency in the Atlantic cod (Gadus morhua)? Fish Physiol Biochem 20:293–303
Lowry OH, Ronebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Lozano I, Devoy RJN, May W, Andersen U (2004) Storminess and vulnerability along the Atlantic coastlines of Europe: analysis of storm records and of a greenhouse gases induced climate scenario. Mar Geol 210:205–225
Metz JR, van den Burg EH, Bonga SE, Flik G (2003) Regulation of branchial Na+/K+-ATPase in common carp Cyprinus carpio L. acclimated to different temperatures. J Exp Biol 206:2273–2280
Murray HM, Gallant JW, Perez-Casanova JC, Johnson SC, Douglas SE (2003) Ontogeny of lipase expression in winter flounder. J Fish Biol 62:816–833
Muthappa NA, Gupta S, Yengkokpam S, Debnath D, Kumar N, Pal AK, Jadhao SB (2014) Lipotropes promote immunobiochemical plasticity and protect fish against low-dose pesticide-induced oxidative stress. Cell Stress Chaperones 19(1):61–81
Ochoa S (1955) Malic dehydrogenase and ‘malic’ enzyme. In: Coloric SP, Kaplan N (eds) Methods of enzymology, vol I. Academic, New York, pp 735–745
Pelletier D, Dutil JD, Blier P, Guderley H (1994) Relation between growth rate and metabolic organisation of white muscle, liver and digestive tract in cod, Gadus morhua. J Comp Physiol 164B(179):190
Pfaff MW, Gerstmayer B, Bosio A, Windisch W (2003) Effect of zinc deficiency on the mRNA expression pattern in liver and jejunum of adult rats: monitoring gene expression using cDNA microarrays combined with real-time RT-PCR. J Nutr Biochem 14:691–702
Post RL, Sen AK (1967) Sodium and potassium stimulated ATPase. In: Colowick SP, Kaplan NO (eds) Methods in enzymology, vol 10. Academic, New York, pp 762–768
Powell SR (2000) The antioxidant properties of zinc. J Nutr 130(5S Suppl):1447S–1454S
Ren X, McHale CM, Skibola CF, Smith AH, Smith MT, Zhang L (2011) An emerging role for epigenetic dysregulation in arsenic toxicity and carcinogenesis. Environ Health Perspect 119:11–19
Rick W, Stegbauer HP (1974) Amylase measurement of reducing groups. In: Bergmeyer HV (ed) Methods of enzymatic analysis, vol 2, 2nd edn. Academic, New York, pp 885–889
Sa MVC, Pezzato LE, Lima MMBF, Padilha PM (2004) Optimum zinc supplementation level in Nile tilapia Oreochromis niloticus juveniles diets. Aquaculture 238(1–4):385–401
Sa MVC, Pezzato LE, Lima MMBF, Padilha PM (2005) Relative bioavailability of zinc in supplemental inorganic and organic sources for Nile tilapia Oreochromis niloticus fingerlings. Aquac Nutr 11(4):273–281
Salgueiro MJ, Zubillaga M, Lysionek A, Sarabia MI, Caro R, Paoli DT, Hager A, Weill R, Boccio J (2000) Zinc as an essential micronutrient: a review. Nutr Res 20:737–755
Sanfey H, Sar MG, Bulkley GB, Cameron JL (1986) Oxygen-derived free radicals and acute pancreatitis: a review. Acta Physiol Scand Supl 548:109–118
Sardella BA, Kültz D, Cech J Jr, Brauner C (2008) Salinity-dependent changes in Na+/K+-ATPase content of mitochondria-rich cells contribute to differences in thermal tolerance of Mozambique tilapia. J Comp Physiol B 178:249–256 Salinity-dependent changes in Na(+)/K (+)-ATPase content of mitochondria-rich cells contribute to differences in thermal tolerance of Mozambique tilapia
Shay NF, Manigan HF (2000) Neurobiology of zinc-influenced eating behaviour. J Nutr 130:1493S–1499S
Singh AK, Lakra WS (2012) Culture of Pangasianodon hypophthalmus into India: impacts and present scenario. Pak J Biol Sci 15(1):19–26
Skou JC (1975) The Na+−K+ activated enzyme system its relationship to transport of sodium and potassium. Q Rev Biophys 7:401–434
Trenberth KE, Jones PD, Ambenje P, Bojariu R and others (2007) Observations: surface and atmospheric climate change. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M Miller HL (eds) Climate change 2007: the physical science basis. Contribution of Working Group I to the 4th Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp. 235–336
Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39(1):44–84
Verma AK, Pal AK, Manush SM, Das T, Dalvi RS, Chandrachoodan PP, Ravi PM, Apte SK (2007) Persistent sub-lethal chlorine exposure elicits the temperature induced stress responses in Cyprinus carpio early fingerlings. Pestic Biochem Physiol 87:229–237
Willmer P, Stone G, Johnston I (2000) Environmental physiology of animals. Blackwell Science, Oxford, p 768. isbn:978-1-405-10724-2
Wootton IDP (1964) Microanalysis. In: Churchill J (ed) Medical biochemistry, 4th edn, London, pp 101–107
Wroblewski L, LaDue JS (1955) Lactic dehydrogenase activity in blood. Proc Soc Exp Biol Med 90:210–213
Yadav A, Gopesh A, Pandey RS, Rai DK, Sharma B (2007) Fertilizers industry effluent induced biochemical changes in fresh water teleost Channa staiatus (Bolch). Bull Environ Contam Toxicol 79:588–595
Yousef MI, El-Hendy HA, El-Demerdash FM, Elagamy EI (2002) Dietary zinc deficiency induced changes in the activity of enzymes and levels of free radicals, lipids and protein electrophoretic behaviour in growing rats. Toxicology 175(1–3):223–234
Yuen BB, Au DW (2006) Temporal changes of ethoxyresorufin-o-deethylase (EROD) activities and lysosome accumulation in intestine of fish on chronic exposure to dietary benzo[a]pyrene: linking erode induction to cytological effects. Environ Toxicol Chem 25:2593–2600
Yuen BB, Wong CK, Woo NY, Au DW (2007) Induction and recovery of morph functional changes in the intestine of juvenile carnivorous fish (Epinephelus coioides) upon exposure to foodborne benzo[a]pyrene. Aquat Toxicol 82(3):181–194
Acknowledgments
The authors express their sincere gratitude to the Director of ICAR-National Institute of abiotic Stress Management, Baramati, Pune, for providing all the facilities to conduct the present study.
Funding
The study was supported with financial assistance provided by the Indian Council of Agricultural Research (ICAR), New Delhi, India, as institutional project (no. IXX09673).
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Kumar, N., Krishnani, K.K. & Singh, N.P. Effect of zinc on growth performance and cellular metabolic stress of fish exposed to multiple stresses. Fish Physiol Biochem 46, 315–329 (2020). https://doi.org/10.1007/s10695-019-00719-1
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DOI: https://doi.org/10.1007/s10695-019-00719-1