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Fish Physiology and Biochemistry

, Volume 44, Issue 2, pp 629–637 | Cite as

Alterations in the activity of certain enzymes in the gills of a carp Labeo rohita exposed to an azo dye, Eriochrome black T: a biochemical investigation

  • Ayan Srivastava
  • Usha Kumari
  • Ashwini Kumar Nigam
  • Swati Mittal
  • Ajay Kumar Mittal
Article

Abstract

In Labeo rohita exposed to sub-lethal concentrations of an azo dye, Eriochrome black T for 4 days, gills show considerable alterations in the activity of certain metabolic enzymes—alkaline phosphatase, acid phosphatase, carboxylesterase, lactate dehydrogenase, and succinate dehydrogenase; and antioxidant enzymes—catalase and peroxidase. The activities of alkaline phosphatase, acid phosphatase, carboxylesterase, succinate dehydrogenase, catalase, and peroxidase decline significantly. This has been associated with impaired metabolic function of the gills due to azo dye toxicity. The activity of lactate dehydrogenase, in contrast, shows a gradual increase, reflecting a shift from aerobic to anaerobic metabolism. In the fish kept for recovery for 8 days, after exposing the fish to the dye for 4 days, activity of succinate dehydrogenase, alkaline phosphatase, and lactate dehydrogenase gradually become similar to control. Nevertheless, activity of acid phosphatase, catalase, peroxidase, and carboxylesterase, although recover gradually, remained significantly low as compared to that of control. This study signifies that the dye is highly toxic to Labeo rohita and suggests that the activity of metabolic and antioxidant enzymes can be used as biomarker for fish toxicity.

Keywords

Azo Dye Enzymes Exposure Gills Labeo rohita 

Notes

Author contributions

Ayan Srivastava designed and conducted the experiments and drafted the manuscript. Usha Kumari and Ashwini Kumar Nigam assisted in execution of experiments and data interpretation. Swati Mittal and Ajay Kumar Mittal were involved in critical analysis of data and reading and editing of the manuscript. All authors discussed the results and approved the final version of the manuscript.

Funding information

Present work was conducted under the project P-01/651 sponsored by University Grant Commission, Government of India. Mr. Ayan Srivastava was supported by Banaras Hindu University Fellowship (Scheme No. 5012) sponsored by the University Grants Commission, Government of India.

Compliance with ethical standards

All experiments were performed following the approval of the Ethics Committee of the institution as per ethical guidelines for the treatment and maintenance of animals (Ref No. F.Sc./88/IAEC/2016-2017/228). We hereby declare that the experiments comply with the current laws of the country (India) in which they were performed.

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. Abdel-Hameid NAH (2009) A protective effect of calcium carbonate against arsenic toxicity of the Nile catfish, Clarias gariepinus. Turk J Fish Aquat Sci 9:191–200CrossRefGoogle Scholar
  2. Adams SM, Greeley MS (2000) Ecotoxicological indicators of water quality: using multi-response indicators to assess the health of aquatic ecosystems. J Water Air Soil Pollut 123(1/4):103–115.  https://doi.org/10.1023/A:1005217622959 CrossRefGoogle Scholar
  3. Altinok I, Capkin E (2007) Histopathology of rainbow trout exposed to sublethal concentrations of methiocarb or endosulfan. Toxicol Pathol 35:405–410Google Scholar
  4. American Public Health Association (APHA), American Water Works Association (AWWA) and Water Pollution Control Federation (WPCF) (1985) Standard methods for the examination of water and wastewater, 16th edn. American Public Health Association, WashingtonGoogle Scholar
  5. Ayadi I, Monteiro SM, Regaya I, Coimbra A, Fernandes F, Oliveira MM, Peixoto F, Mnif W (2015) Biochemical and histological changes in the liver and gill of Nile tilapia Oreochromis niloticus exposed to Red 195 Dye. RSC Adv 5(106):87168–87178.  https://doi.org/10.1039/C5RA13127H CrossRefGoogle Scholar
  6. Ballesteros ML, Wunderlin DA, Bistoni MA (2009) Oxidative stress responses in different organs of Jenynsia multidentata exposed to endosulfan. Ecotoxicol Environ Saf 72(1):199–205.  https://doi.org/10.1016/j.ecoenv.2008.01.008 CrossRefPubMedGoogle Scholar
  7. Barot J (2015) Evaluation of azo dye toxicity using some haematological and histopathological alterations in fish Catla catla. Int J Biol Biomol Agric Food Biotechnol Eng 9(5):415–418Google Scholar
  8. Barot J, Bahadur A (2015) Toxic impacts of C.I. Acid Orange 7 on behavioural, haematological and some biochemical parameters of Labeo rohita fingerlings. IJSRES 3(8):284–290.  https://doi.org/10.12983/ijsres-2015-p0284-0290 CrossRefGoogle Scholar
  9. Cazenave J, Bistoni MDA, Pesce SF et al (2006) Differential detoxification and antioxidant response in diverse organs of Corydoras paleatus experimentally exposed to microcystin-RR. Aquat Toxicol 76(1):1–12.  https://doi.org/10.1016/j.aquatox.2005.08.011 CrossRefPubMedGoogle Scholar
  10. Chen QL, Luo Z, Zheng JL, Li XD, Liu CX, Zhao YH, Gong Y (2012) Protective effects of calcium on copper toxicity in Pelteobagrus fulvidraco: copper accumulation, enzymatic activities, histology. Ecotox Environ Saf 76(2):126–134.  https://doi.org/10.1016/j.ecoenv.2011.10.007 CrossRefGoogle Scholar
  11. Cinar K, Aksoy A, Emre Y, Aşti RN (2009) The histology and histochemical aspects of gills of the flower fish, Pseudophoxinus antalyae. Vet Res Commun 33(5):453–460.  https://doi.org/10.1007/s11259-008-9191-2 CrossRefPubMedGoogle Scholar
  12. David M, Ramesh H, Patil VK, Marigoudar SR, Chebbi SG (2010) Sodium cyanide induced modulations in the activities of some oxidative enzymes and metabolites in the fingerlings of Cyprinus carpio (Linnaeus). Toxicol Environ Chem 92(10):1841–1849.  https://doi.org/10.1080/02772248.2010.498374 CrossRefGoogle Scholar
  13. de Lima D, Roque GM, de Almeida EA (2013) In vitro and in vivo inhibition of acetylcholinesterase and carboxylesterase by metals in zebrafish (Danio rerio). Mar Environ Res 91:45–51.  https://doi.org/10.1016/j.marenvres.2012.11.005 CrossRefPubMedGoogle Scholar
  14. Denton DL, Wheelock CE, Murry SA et al (2003) Joint acute toxicity of esfenvalerate and diazinon to larval fathead minnows (Pimephales promelas). Environ Toxicol Chem 22(2):336–341.  https://doi.org/10.1002/etc.5620220214 CrossRefPubMedGoogle Scholar
  15. Evans DH, Cameron JN (1986) Gill ammonia transport. J Exp Zoo 239(1):17–23.  https://doi.org/10.1002/jez.1402390104 CrossRefGoogle Scholar
  16. Evans DH, Claiborne JB, Farmer L et al (1982) Fish gill ionic transport: methods and models. Biol Bull 163(1):108–130.  https://doi.org/10.2307/1541502 CrossRefGoogle Scholar
  17. Fernandes MN, Mazon AF (2003) Environmental pollution and fish gill morphology. In: Val AL, Kapoor BG (ed) Fish adaptations. Science Publishers, Enfield, 203–231Google Scholar
  18. Flik G, Verbost PM (1993) Calcium transport in fish gills and intestine. J Exp Biol 184:17–29Google Scholar
  19. Goldstein L (1982) Gill nitrogen excretion. In: Gills. Cambridge University Press, pp 193–206Google Scholar
  20. Gonzales RJ, McDonald DG (1992) The relationship between oxygen consumption and ion loss in a freshwater fish. J Exp Biol 163:317–332Google Scholar
  21. Goss GG, Perry SF, Wood CM, Laurent P (1992) Mechanisms of ion and acid-base regulation at the gills of freshwater fish. J Exp Zool 263(2):143–159.  https://doi.org/10.1002/jez.1402630205 CrossRefPubMedGoogle Scholar
  22. Gül S, Belge-Kurutas E, Yıldıza E et al (2004) Pollution correlated modifications of liver antioxidant systems and histopathology of fish (Cyprinidae) living in Seyhan Dam Lake, Turkey. Environ Int 30(5):605–609.  https://doi.org/10.1016/S0160-4120(03)00059-X CrossRefPubMedGoogle Scholar
  23. Hughes GM (1966) The dimensions of fish gills in relation to their function. J Exp Biol 45(1):177–195PubMedGoogle Scholar
  24. Hughes GM (1982) An introduction to the study of gills. In: Houlihan DF, Rankin JC, Shuttleworth TJ (eds) Gills. Cambridge University Press, Cambridge, UK, pp 1–24Google Scholar
  25. Kaur S, Kaur A (2015) Variability in antioxidant/detoxification enzymes of Labeo rohita exposed to an azo dye, acid black (AB). Comp Biochem Physiol C 167:108–116Google Scholar
  26. Kaur K, Kaur S, Kaur A (2016) Scanning electron microscopic observations of Basic Violet-1 induced changes in the gill morphology of Labeo rohita. Environ Sci Pollut Res 23(16):16579–16588.  https://doi.org/10.1007/s11356-016-6764-4 CrossRefGoogle Scholar
  27. Korndat J, Braunbeck T (2001) Alterations of selected metabolic enzymes in fish following long-term exposure to contaminated streams. J Aquat Ecosys Stres Recov 8:299–318CrossRefGoogle Scholar
  28. Leticia AG, Gerardo GB (2008) Determination of esterase activity and characterization of cholinesterases in the reef fish Haemulon plumieri. Ecotox Environ Saf 71(3):787–797.  https://doi.org/10.1016/j.ecoenv.2008.01.024 CrossRefGoogle Scholar
  29. Manjunatha B, Tirado JO, Selvanayagam (2015) Sub-lethal toxicity of potassium cyanide on nile tilapia (Oreochromis niloticus): biochemical response. Int J Pharm Sci 7(3):379–382Google Scholar
  30. Mauceri A, Fossi MC, Leonzio C, Ancora S, Minniti F, Maisano M, Lo Cascio P, Ferrando S, Fasulo S (2005) Stress factors in the gills of Liza aurata (Perciformes, Mugilidae) living in polluted environments. Ital J Zool 72(4):285–292.  https://doi.org/10.1080/11250000509356687 CrossRefGoogle Scholar
  31. McDonald DG, Wood CM, Rhem RG, Mueller ME, Mount DR, Bergman HL (1991) Nature and time course of acclimation to aluminium in juvenile brook trout (Salvelinus fontinalis) I Physiology. Can J Fish Aquat Sci 48(10):2006–2015.  https://doi.org/10.1139/f91-239 CrossRefGoogle Scholar
  32. Mittal AK, Whitear M (1978) A note on cold anaesthesia of poikilotherms. J Fish Biol 13(4):519–520.  https://doi.org/10.1111/j.1095-8649.1978.tb03462.x CrossRefGoogle Scholar
  33. Neff JM (1985) Use of biochemical measurements to detect pollutant mediated damage to fish. In: Aquatic toxicology and hazard assessment: seventh symposium. Cardwell RD, Purdy R, Bahner RC (eds) ASTM STP 854, ASTM, Philadelphia, 155–83, DOI:  https://doi.org/10.1520/STP36266S
  34. Nigam AK, Kumari U, Mittal S, Mittal AK (2014) Characterization of carboxylesterase in skin mucus of Cirrhinus mrigala and its assessment as biomarker of organophosphate exposure. Fish Physiol Biochem 40(3):635–644.  https://doi.org/10.1007/s10695-013-9872-9 CrossRefPubMedGoogle Scholar
  35. Olson KR (2002) Vascular anatomy of the fish gill. J Exp Zool 293(3):214–231.  https://doi.org/10.1002/jez.10131 CrossRefPubMedGoogle Scholar
  36. Padh H (1992) Organelle isolation and marker enzyme assay. Tested studies for laboratory teaching. Goldman CA (ed) Proceedings of the 13th Workshop/Conference of the Association for Biology Laboratory Education (ABLE), 13:129–146Google Scholar
  37. Parthasarathi K, Karuppasamy R (1998) Fenvalerate impact on tissue acid and alkaline phosphatase activity of the fish, Channa punctatus (Bloch.) Pollut Res 17(3):281–285Google Scholar
  38. Perry SF, Laurent P (1993) Environmental effects on fish gill structure and function, in Fish ecophysiology, Rankin JC, Jensen FB (eds) vol. 9 of Chapman & Hall Fish and Fisheries Series. Springer, London, UK, 231–264Google Scholar
  39. Petersen CE, Anderson BA (2005) Investigations in the Biology. 1151 Laboratory, Stipes Publishing L.L.C. Champaign, IL, USA 45Google Scholar
  40. Poleksic V, Mitrovic-Tutundzic V (1994) Fish gills as a monitor of sublethal and chronic effects of pollution. In: Mulle R, Llyod R (eds) Sublethal and chronic effects of pollutants on freshwater fish. Fishing News Books, Oxford, London, pp 339–352Google Scholar
  41. Rani AS, Sudharsan R, Reddy TN et al (2000) Alternations in the levels of dehydrogenases in a freshwater fish, Tilapia mossambica (Peters) exposed to arsenic toxicity. Indian J Environ Health 42:130–133Google Scholar
  42. Romão S, Freire CA, Fanta E (2001) Ionic regulation and Na, K-ATPase activity in gills and kidney of the aglomerular Antarctic fish Notothenia neglecta upon exposure to seawater dilution. J Fish Biol 55:119–130Google Scholar
  43. Sayer MD, Davenport J (1987) The relative importance of the gills to ammonia and urea excretion in five seawater and one freshwater teleost species. J Fish Biol 31(4):561–570.  https://doi.org/10.1111/j.1095-8649.1987.tb05258.x CrossRefGoogle Scholar
  44. Sekar P, Hariprasad S, Deccaraman M (2008) Impact of textile dye industry effluent on the neurosecretory cells in fresh water female crab Spiralothelphusa hydrodroma (Herbst). J Appl Sci Res 4(11):1526–1533Google Scholar
  45. Shen B, Liu HC, WB O et al (2014) Toxicity induced by Basic Violet 14, Direct Red 28 and Acid Red 26 in zebrafish larvae. J Appl Toxicol 35(12):1473–1480CrossRefGoogle Scholar
  46. Solé M, Sanchez-Hernandez JC (2015) An in vitro screening with emerging contaminants reveals inhibition of carboxylesterase activity in aquatic organisms. Aquat Toxicol 169:215–222.  https://doi.org/10.1016/j.aquatox.2015.11.001 CrossRefPubMedGoogle Scholar
  47. Srivastava S, Sinha R, Roy D (2004) Toxicological effects of malachite green. Aquat Toxicol 66(3):319–329.  https://doi.org/10.1016/j.aquatox.2003.09.008 CrossRefPubMedGoogle Scholar
  48. Sudova E, Machova J, Svobodova Z et al (2007) Negative effects of malachite green and possibilities of its replacement in the treatment of fish eggs and fish: a review. Vet Med 52(12):527–539CrossRefGoogle Scholar
  49. Thompson HM (1999) Esterases as markers of exposure to organophosphates and carbamates. Ecotoxicology 8(5):369–384.  https://doi.org/10.1023/A:1008934505370 CrossRefGoogle Scholar
  50. Tridico CM, Rodrigues ACF, Nogueira L, Silva DCS, Moreira AB, de Almeida EA (2010) Biochemical biomarkers in Oreochromis niloticus exposed to mixtures of benzo[a]pyrene and diazinon. Ecotox Environ Saf 73(5):858–863.  https://doi.org/10.1016/j.ecoenv.2010.01.016 CrossRefGoogle Scholar
  51. Tripathi G, Shasmal J (2011) Concentration related responses of chlorpyriphos in antioxidant, anaerobic and protein synthesizing machinery of the freshwater fish, Heteropneustes fossilis. Pest Biochem Physiol 99(3):215–220.  https://doi.org/10.1016/j.pestbp.2010.12.006 CrossRefGoogle Scholar
  52. van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol.Pharmacol 13(2):57–149.  https://doi.org/10.1016/S1382-6689(02)00126-6 CrossRefPubMedGoogle Scholar
  53. Verbost PM, Schoenmakers TJM, Flik G et al (1994) Kinetics of ATP and Na+-gradient driven Ca+2 transport in basolateral membranes from gills of freshwater and seawater-adapted tilapia. J Exp Biol 186:95–108PubMedGoogle Scholar
  54. Worthington Enzyme Manual, Worthington K, Worthington V (2011a) Worthington Biochemical Corporation. Cited July, 2014 (http://www.worthington-biochem.com/CTL/default.html)
  55. Worthington Enzyme Manual, Worthington K, Worthington V (2011b) Worthington Biochemical Corporation. Cited July, 2014 (http://www.worthington-biochem.com/HPO/default.html)
  56. Worthington Enzyme Manual, Worthington K, Worthington V (2011c) Worthington Biochemical Corporation. Cited July, 2014 (http://www.worthington-biochem.com/LDH/default.html)
  57. Xing H, Wanga J, Li J et al (2010) Effects of atrazine and chlorpyrifos on acetylcholinesterase and carboxylesterase in brain and muscle of common carp. Environ Toxicol Pharmacol 30(1):26–30.  https://doi.org/10.1016/j.etap.2010.03.009 CrossRefPubMedGoogle Scholar
  58. Zheng JL, Luo Z, Chen QL, Liu X, Liu CX, Zhao YH, Gong Y (2011) Effect of water borne zinc exposure on metal accumulation, enzymatic activities and histology of Synechogobius hasta. Ecotoxicol Environ Saf 74(7):1864–1873.  https://doi.org/10.1016/j.ecoenv.2011.06.018 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2017

Authors and Affiliations

  • Ayan Srivastava
    • 1
  • Usha Kumari
    • 1
    • 2
  • Ashwini Kumar Nigam
    • 1
  • Swati Mittal
    • 1
  • Ajay Kumar Mittal
    • 1
    • 3
  1. 1.Skin Physiology Laboratory, Centre of Advanced Study, Department of Zoology, Institute of ScienceBanaras Hindu UniversityVaranasiIndia
  2. 2.Zoology Section, Mahila MahavidyalayaBanaras Hindu UniversityVaranasiIndia
  3. 3.Department of ZoologyBanaras Hindu UniversityVaranasiIndia

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