Metal bioaccumulation, oxidative stress, and biochemical alterations in the freshwater snail (Galba truncatula) exposed to municipal sewage

Document Type: Original Article

Authors

Aquaculture Department, Faculty of Natural Resources and Environment, Behbahan Khatam Alanbia University of Technology, Iran

Abstract

Urban wastewater contains various detergents, pesticides, pharmaceutical medications, cosmetics, hygiene products, and heavy metals. Discharge of municipal sewage into surface water affects the health of aquatic organisms through altering biochemical markers and accumulating heavy metals in various tissues. The present study aimed to evaluate the toxic effects of municipal sewage on the biochemical markers and bioaccumulation of cadmium and lead in freshwater snail (Galba truncatula) during 14 days. Concentrations of toxic metals in the snails were determined using ICP-OES-PerkinElmer, and biochemical parameters were measured via UV-Vis spectroscopy. The results indicated significantly lower levels of glycogen and total antioxidant in the cells, as well as the significantly lower activities of aspartate aminotransferase, alanine aminotransferase, alkaline phosphatase, acetylcholine esterase, catalase, and glucose-6-phosphate dehydrogenase in the Galba truncatula exposed to sewage compared to the control. However, the activities of lactate dehydrogenase ,glutathione peroxidase, and malondialdehyde were significantly higher in the snails exposed to sewage compared to the control. Moreover, bioaccumulation of cadmium and lead was observed to increase in the experimental groups exposed to sewage. Alterations in biochemical parameters in the G. truncatula exposed to sewage could be due to the toxic effects of various environmental pollutants in municipal wastewater. According to the findings, oxidative damage to the vital tissues of G. truncatula was associated with the bioaccumulation of cadmium and lead, depletion of total antioxidant levels, changes in biochemical parameters, and lipid peroxidation in soft tissues.

Keywords


1. Pérez M R, Rossi A S, Bacchetta C, Elorriaga Y, Carriquiriborde P, Cazenave J. In situ evaluation of the toxicological impact of a wastewater effluent on the fish Prochilodus lineatus: biochemical and histological assessment. Ecol Indic 2018; 84: 345–353.

2.  Archer E, Petrie B, Kasprzyk-Hordern B, Wolfaardt GM. The fate of pharmaceuticals and personal care products (PPCPs), endocrine disrupting contaminants (EDCs), metabolites and illicit drugs in a WWTW and environmental waters. Chemosphere 2017; 174: 437-446.

3. Banaee M, Mohammadipour S, Madhani S. Effects of sublethal concentrations of permethrin on bioaccumulation of cadmium in zebra cichlid (Cichlasoma nigrofasciatum). Toxicol  Environ Chem 2015; 97 (2):200-207.

4. Nematdoost Haghi B, Banaee M. Effects of micro-plastic particles on paraquat toxicity to common carp (Cyprinus carpio): biochemical changes. Int J Environ Sci Technol 2017; 14 (3): 521-530.

5. Banaee M, Shahafve S, VaziriyanM, Taheri S, Nemadoost Haghi B. Effects of sewage effluent on blood biochemical parameters of common carp (Cyprinus carpio): A case study of Behbahan, Khuzestan Province. J Chem Health Risks 2016; 6 (3): 161-173.

6. Mosavi Dehmord L, Shoukat P, Banaee M, Nematdoust Haghi B. Limnological investigation and biological assessment of Maroon River. J Animal Environ 2017; 9 (2): 259-266.

7.  Macías-Mayorga D, Laiz I, Moreno-Garrido I, Blasco J. Is oxidative stress related to cadmium accumulation in the Mollusc Crassostrea angulate?. Aquat Toxicol 2015; 161: 231-241.

8. Zheng S, Zhou Q, Gao J, Xiong H, Chen C. Behavioral alteration and DNA damage of freshwater snail Bellamya aeruginosa stressed by ethylbenzene and its tissue residue. Ecotoxicol Environ Saf 2012; 81: 43-8.

9. Bhattacharya P, Swarnakar S, Mukhopadhyay A, Ghosh S. Exposure of composite tannery effluent on snail, Pila globosa: A comparative assessment of toxic impacts of the untreated and membrane treated effluents. Ecotoxicol Environ Saf 2016; 126: 45-55.

10. Wan R, Meng F, Fu W, Wang Q, Su E. Biochemical responses in the gills of Meretrix meretrix after exposure to treated municipal effluent. Ecotoxicol Environ Saf 2015; 111: 78-85.

11. Barky FA, Abdelsalam H A, Mahmoud M B, Hamdi SAH. Influence of Atrazine and Roundup pesticides on biochemical and molecular aspects of Biomphalaria alexandrina snails. Pestici Biochem Physiol 2012;104 (1): 9-18.

12. Ali D, Alarifi S, Kumar S, Ahamed M, Siddiqui MA. Oxidative stress and genotoxic effect of zinc oxide nanoparticles in freshwater snail Lymnaea luteola L. Aquat Toxicol 2012; 125: 83-90.

13. Abdel-Halim KY, Abo El-Saad  AM, Talha M M, Hussein AA, Bakry NM. Oxidative stress on land snail Helix aspersa as a sentinel organism for ecotoxicological effects of urban pollution with heavy metals. Chemosphere 2013; 93 (6): 1131-1138.

14. Radwan MA, El-Gendy KS, Gad  A F. Biomarkers of oxidative stress in the land snail, Theba pisana for assessing ecotoxicological effects of urban metal pollution. Chemosphere 2010; 79 (1): 40-46.

15. De Silva NA L, Marsden I D, Gaw S, Glover C N. Acute waterborne cadmium toxicity in the estuarine pulmonate mud snail, Amphibola crenata. Ecotoxicol Environ Saf 2018; 158: 274-283.

16. Placer Z, Cushman L, Johnson B. Estimation of product of lipid peroxidation (malonyl dialdehyde) in biochemical systems. Analytic Biochem 1996; 16 (2): 359-364.

17. Benzie I, Strain J. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”, the FRAP assay. Analytic Biochem. 1996; 239 (1): 70-76.

18. Zhang P. Analysis of Mouse Liver Glycogen Content. Bio-protocol 2012; 2 (10): e186.

19. Góth LA. Simple method for determination of serum catalase and revision of reference range. Clin Chim Acta 1991; 196: 143-152.

20. Moss DV, Henderson AR. Clinical enzymology. In Tietz Textbook of Clinical Chemistry. 3rd ed.; W.B. Saunders Company: Philadelphia 1999; pp 617-721.

21. Knedel M, Boetteger R. Kinetic method for determination of pseudocholinesterase (acylcholine acylhydrolase) activity. Klin. Wochenschr 1967; 45(6): 325-327.

22. Gómez-Milán E, Lozano MJSM. Daily and annual variations of the hepatic glucose 6-phosphate dehydrogenase activity and seasonal changes in the body fats of the gilthead seabream Sparus aurata. J Exp Zool A Ecol Genet Physiol 2007; 307(9): 516–526.

23. Johnson AM, Rohlfs EM, Silverman L M. Proteins. In Tietz Textbook of Clinical Chemistry. 3rd ed.; W.B. Saunders Company: Philadelphia, 1999; pp 477-540.

24. Silva CO, Simões T, Novais SC, Pimparel I, Granada L, Soares AM, et al. Fatty acid profile of the sea snail Gibbula umbilicalis as a biomarker for coastal metal pollution. Sci Total Environ 2017; 586: 542-550.

25. Al-Ghais S M. Acetylcholinesterase, glutathione and hepatosomatic index as potential biomarkers of sewage pollution and depuration in fish. Mar Pollut Bull 2013; 74 (1): 183-186.

26. Ma J, Zhou C, Li Y, Li X. Biochemical responses to the toxicity of the biocide abamectin on the freshwater snail Physa acuta. Ecotoxicol Environ Saf 2014;101: 31-35.

27. Khalil AM. Impact of methomyl lannate on physiological parameters of the land snail Eobania vermiculata. J Basic  App Zool 2016; 74: 1-7.

28. Ellinger JJ, Lewis IA, Markley JL. Role of aminotransferases in glutamate metabolism of human erythrocytes. J Biomol NMR 2011; 49 (3): 221-229.

29. Chen Y Q, Xu QM, Liu YL, Li XR, Yang SL, Zhuge H X. Laboratory evaluation of the molluscicidal activity of Pulsatilla chinensis (Bunge) Regel saponins against the snail Oncomelania hupensis. Biomed Environ Sci 2012; 25 (2): 224-229.

30. Tunholi VM, Tunholi-Alves VM, Monteiro CO, Silva LCD, Dolinski CM, Castro RN, et al. Biological, biochemical and histological features of Bradybaena similaris (Gastropoda: Pulmonata) infected by Heterorabditis indica (Rhabditida: Heterorhabditidae) strain LPP1. Exp Parasitol 2017; 179: 28-35.

31. Sharma U, Pal D, Prasad R. Alkaline Phosphatase: An Overview. Indian J Clin Biochem 2014; 29 (3): 269-278.

32. Lama JL, Bell RAV, Storey KB. Glucose-6-phosphate dehydrogenase regulation in the hepatopancreas of the anoxia-tolerant marine mollusc, Littorina littorea. Peerj 2013; 1: e21.

33. Rezaei Shadegan M, Banaee M. Effects of dimethoate alone and in combination with Bacilar fertilizer on oxidative stress in common carp, Cyprinus carpio. Chemosphere 2018; 208: 101-107.

34. Banaee M, Sureda A, Mirvaghefi A R, Ahmadi K. Biochemical and histological changes in the liver tissue of Rainbow trout (Oncorhynchus mykiss) exposed to sub-lethal concentrations of diazinon. Fish Physiol Biochem 2013; 39 (3): 489-501.

35. Hillar A, Nicholls P. A mechanism for NADPH inhibition of catalase compound II formation. FEBS Lett 1992; 314 (2); 179-182.

36. Pedrini-Martha V, SchneggR, Baurand PE,de Vaufleury A, Dallinger R. The physiological role and toxicological significance of the non-metal-selective cadmium/copper-metallothionein isoform differ between embryonic and adult helicid snails. Comp Biochem Physiol C Toxicol  Pharmaco 2017; 199: 38-47.

37. Hosseini M H, Khodadadi M, Dorri H. Evaluation of heavy metals (Cd, Cr, Zn, Pb) concentration in effluent & sludge of a tile factory in Birjand 2011. J Birjand Univ Med Sci 2013; 20 (1) :85-93.