Skip to main content
SpringerLink
Log in

Effect of zinc on growth performance and cellular metabolic stress of fish exposed to multiple stresses

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alayash AI (1989) Zinc and some zinc dependent enzymes in sickle cell anemia. Int J Vitam Nutr Res 59(4):388–389

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Cherry IS, Crandell LA Jr (1932) The specificity of pancreatic lipase: its appearance in blood after pancreatic injury. Am J Phys 100:266–273

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Drapeau GR (1976) Protease from Staphylococcus aureus. Methods Enzymol 45:469–475

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, Oxford

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Lowry OH, Ronebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Powell SR (2000) The antioxidant properties of zinc. J Nutr 130(5S Suppl):1447S–1454S

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Shay NF, Manigan HF (2000) Neurobiology of zinc-influenced eating behaviour. J Nutr 130:1493S–1499S

    CAS  PubMed  Google Scholar 

  • Singh AK, Lakra WS (2012) Culture of Pangasianodon hypophthalmus into India: impacts and present scenario. Pak J Biol Sci 15(1):19–26

    CAS  PubMed  Google Scholar 

  • Skou JC (1975) The Na+−K+ activated enzyme system its relationship to transport of sodium and potassium. Q Rev Biophys 7:401–434

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Willmer P, Stone G, Johnston I (2000) Environmental physiology of animals. Blackwell Science, Oxford, p 768. isbn:978-1-405-10724-2

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

  1. ICAR-National Institute of Abiotic Stress Management, Malegaon, Baramati, Pune, 413115, India

    Neeraj Kumar, Kishore Kumar Krishnani & Narendra Pratap Singh

Authors
  1. Neeraj Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kishore Kumar Krishnani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Narendra Pratap Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Neeraj Kumar.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOC 37 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-019-00719-1

Keywords

Search

Navigation