Effect of sodium chloride on oxidative stress biomarkers of the freshwater bivalve Anodonta cygnea

  • D. S. Pesnya Papanin Institute for Biology of Inland Waters
  • A. V. Romanovsky Papanin Institute for Biology of Inland Waters
  • Y. S. Klimova Papanin Institute for Biology of Inland Waters
  • R. A. Fedorov Papanin Institute for Biology of Inland Waters
  • E. S. Ivanova Cherepovets State University
Keywords: antioxidant; catalase; glutathione-s-transferase; glutathione reductase; reduced glutathione; malonic dialdehyde

Abstract

For the first time a study was conducted of the effects of the change in the concentration of sodium chloride in water on the biomarkers of oxidative stress (enzymes: catalase (CAT), glutathione reductase (GR), glutathione-S-transferase (GST), and the levels of reduced glutathione (GSH), and a marker of peroxidation lipids (LPO) – malonic dialdehyde (MDA)) in the gills of the freshwater mollusc Anodonta cygnea. Adult specimens of A. cygnea of both sexes with a shell length of 70–100 mm were selected for the study, a total of 36 individuals. The molluscs were collected in one of the bays on the southwestern coast of the Volga reaches of the Rybinsk Reservoir (reservoir of the cascade of the upper Volga). The molluscs were kept in the laboratory in aquariums with river water and sand collected from the place of the molluscs' collection. During the experiment, a solution of NaCl 3 g/l in river water was introduced into the container with molluscs. Samples of molluscs’ tissues were taken before application of the saline solution, 40 and 120 min after changing the salt concentration to 3 g/l, and 20 and 60 min after changing the NaCl solution to river water. The change in the concentration of NaCl in water (0–3 g/l) did not affect the content of water-soluble protein in the gills of molluscs during short-term exposure. The change in NaCl concentration in water caused the intensification of LPO processes in the gills of A. cygnea. The change in the activity of the enzymes of the antioxidant system and the increase in the concentration of GSH in A. cygnea gills, indicates their involvement in protecting freshwater molluscs from NaCl-induced oxidative stress. The change in the functioning of the glutathione system may be a compensatory mechanism for changing the NaCl concentration in water. Such biomarkers of oxidative stress as malonic dialdehyde and enzymes of the antioxidant system are sensitive indicators of changes in NaCl concentration in water in freshwater bivalve molluscs, for example A. cygnea.

References

Baysoy, E., Atli, G., Gürler, C. Ö., Dogan, Z., Eroglu, A., Kocalar, K., & Canli, M. (2012). The effects of increased freshwater salinity in the biodisponibility of metals (Cr, Pb) and effects on antioxidant systems of Oreochromis niloticus. Ecotoxicology and Environmental Safety, 34(84), 249–253.


Beggel, S., & Geist, J. (2015). Acute effects of salinity exposure on glochidia viability and host infection of the freshwater mussel Anodonta anatina (Linnaeus, 1758). Science of the Total Environment, 502, 659–665.


Binelli, A., Torre, C. D., Magni, S., & Parolini, M. (2015). Does zebra mussel (Dreissena polymorpha) represent the freshwater counterpart of Mytilus in ecotoxicological studies? A critical review. Environmental Pollution, 196, 386–403.


Blakeslee, C. J., Galbraith, H. S., Robertson, L. S., & White, B. S. J. (2013). The effects of salinity exposure on multiple life stages of a common freshwater mussel, Elliptio complanata. Environmental Toxicology and Chemistry, 32(12), 2849–2854.


Canesi, L., Viarengo, A., Leonzio, C., Filippelli, M., & Gallo, G. (1999). Heavy metals and glutathione metabolism in mussel tissues. Aquatic Toxicology, 46(1), 67–76.


Charissou, A. M., Cossu-Leguille, C., & Vasseur, P. (2004). Relationship between two oxidative stress biomarkers, malondialdehyde and 8-oxo-7,8-dihydro-2′-deoxyguanosine, in the freshwater bivalve Unio tumidus. Science of The Total Environment, 322, 109–122.


Choi, C. Y., An, K. W., & An, M. I. (2008). Molecular characterization and mRNA expression of glutathione peroxidase and glutathione S-transferase during osmotic stress in olive flounder (Paralichthys olivaceus). Comparative Biochemistry and Physiology, Part A, 149, 330–337.


Doucet-Beaupre, H., Dubé, C., Breton, S., Pörtner, H. O., & Blier, P. U. (2010). Thermal sensitivity of metabolic enzymes in subarctic and temperate freshwater mussels (Bivalvia: Unionoida). Journal of Thermal Biology, 35(1), 11–20.


Falfushynska, H. I., Gnatyshyna, L. L., Farkas, A., Vehovszky, A., Gyori, J., & Stoliar, O. B. (2010). Vulnerability of biomarkers in the indigenous mollusk Anodonta cygnea to spontaneous pollution in a transition country. Chemo sphere, 81(10), 1342–1351.


Falfushynska, H. I., Gnatyshyna, L. L., Golubev, A. P., & Stoliar, O. B. (2012). Main partitioning criteria for the characterization of the health status in the freshwater mussel Anodonta cygnea from spontaneously polluted area in Western Ukraine. Environmental Toxicology, 27(8), 485–494.


Faria, M., Carrasco, L., Diez, S., Riva, M. C., Bayona, J. M., & Barata, C. (2009). Multibiomarker responses in the freshwater mussel Dreissena polymorpha exposed to polychlorobiphenyls and metals. Comparative Biochemistry and Physiology, Part C, 149, 281– 288.


Fernandez, B., Campillo, J. A., Martinez-Gomez, C., & Benedicto, J. (2010). An tioxidant responses in gills of mussel (Mytilus galloprovincialis) as biomar kers of environmental stress along the Spanish Mediterranean coast. Aquatic Toxicology, 99, 186–197.


Fritts, A. K., Barnhart, C., Bradley, M., Liu, N., Cope, W. G., Hammer, E., & Brin golf, R. B. (2014). Assessment of toxicity test endpoints for freshwater mussel larvae (glochidia). Environmental Toxicology and Chemistry, 33(1), 199–207.


Gama-Flores, J. L., Sarma, S. S. S., & Nandini, S. (2005). Interaction among copper toxicity, temperature and salinity on the population dynamics of Brachionus rotundiformis (Rotifera). Hydrobiologia, 546, 559–568.


Geist, J. (2010). Strategies for the conservation of endangered freshwater pearl mussels (Margaritifera margaritifera L.): A synthesis of conservation gene tics and ecology. Hydrobiologia, 644, 69–88.


Gillis, P. (2011). Assessing the toxicity of sodium chloride to the glochidia of freshwater mussels: Implications for salinization of surface waters. Environ mental Pollution, 159, 1702–1708.


Guidi, P., Frenzilli, G., Benedetti, M., Bernardeschi, M., Falleni, A., Fattorini, D., Regoli, F., Scarcelli, V., & Nigroa, M. (2010). Antioxidant, genotoxic and lysosomal biomarkers in the freshwater bivalve (Unio pictorum) transplanted in a metal polluted river basin. Aquatic Toxicology, 100, 75–83.


Halliwell, B., & Gutteridge, J. M. C. (1999). Free radicals in biology and medi cine. Oxford University Press, Oxford.


Keller, E. A., & Zam, S. G. (1999). The acute toxicity of selected metals to the freshwater mussel, Anodonta imbecilis. Toxicology and Chemistry, 10(4), 539–546.


Khlebovich, V. V. (2013). Kriticheskaya solenost’ – gomeostaz – ustoichivoe raz vitie [Critical salinity – homeostasis – sustainable development]. Trudy Zoo logicheskogo Instituta RAN, Prilojenie, 3, 3–6 (in Russian).


Klimova, Y. S., Chuiko, G. M., Gapeeva, M. V., & Pesnya, D. S. (2017). The use of biomarkers of oxidative stress in zebra mussel Dreissena polymorpha (Pallas, 1771) for chronic anthropogenic pollution assessment of the Rybinsk Reservoir. Contemporary Problems of Ecology, 24(2), 210–217.


Koprucu, S. S., Yonar, E., & Seker, E. (2008). Effects of deltamethrin on antioxi dant status and oxidative stress biomarkers in freshwater mussel, Unio elon gatulus eucirrus. Bulletin of Environmental Contamination and Toxicology, 81, 253–257.


Koryak, M., Stafford, L. J., Reilly, R. J., & Magnuson, P. M. (2001). Highway deicing salt runoff events and major ion concentrations along a small urban stream. Journal of Freshwater Ecology, 16(1), 125–134.


Limón-Pacheco, J., & Gonsebatt, M. E. (2009). The role of antioxidants and anti oxidant-related enzymes in protective responses to environmentally induced oxidative stress. Mutation Research, 674, 137–147.


Liu, Q., Shang, X., Ma, Y., Xia, X., Xue, S., Hua, C., Liang, G., Yao, L., & Guo, L. (2017). Isolation and characterization of two glutathione S-transferases from freshwater bivalve Anodonta woodiana: Chronic effects of pentachlorophe nol on gene expression profiles. Fish and Shellfish Immunology, 64, 339–351.


Lushchak, V. I. (2011). Environmentally induced oxidative stress in aquatic animals. Aquatic Toxicology, 101, 13–30.


Martemyanov, V. I. (2011). Influence of environmental mineral composition on the indices of water-salt metabolism in Dreissena polymorpha Pallas introdu ced to Rybinsk Reservoir. Russian Journal of Biological Invasions, 2, 120–134.


Martínez-Álvarez, R. M., Hidalgo, M. C., Domezain, A., Morales, A. E., García-Gallego, M., & Sanz, A. (2002). Physiological changes of sturgeon Acipenser naccarii caused by increasing environmental salinity. The Journal of Experi mental Biology, 205, 3699–3706.


Morozov, A. A., Chuiko, G. M., & Brodskii, E. S. (2012). Functional state of the liver antioxidant system of the Bream Abramis brama (L.) from Rybinsk reservoir regions with different anthropogenic loads. Inland Water Biology, 5(1), 147–152.


Norrstrom, A. C. (2005). Metal mobility by de-icing salt from an infiltration trench for highway runoff. Applied Geochemistry, 20(10), 1907–1919.


Novotny, E. V., Murphy, D., & Stefan, H. G. (2008). Increase of urban lake sali nity by road deicing salt. Science of the Total Environment, 406, 131–144.


Paital, B., & Chainy, G. B. N. (2010). Antioxidant defenses and oxidative stress parameters in tissues of mud crab (Scylla serrata) with reference to changing salinity. Comparative Biochemistry and Physiology, Part C, 151, 142–151.


Pandolfo, T. J., Cope, W. G., Young, G. B., Jones, J. W., Hua, D., & Lingenfelser, S. F. (2012). Acute effects of road salts and associated cyanide compounds on the early life stages of the unionid mussel Villosa iris. Environmental Toxicology and Chemistry, 31(8), 1801–1806.


Prevodnik, A., Gardestrom, J., Lilja, K., Elfwing, T., McDonagh, B., Petrovi, N., Tedengren, M., Sheehan, D., & Bollner, T. (2007). Oxidative stress in res ponse to xenobiotics in the blue mussel Mytilus edulis L.: Evidence for varia tion along a natural salinity gradient of the Baltic Sea. Aquatic Toxicology, 82, 63–71.


Regoli, F., Frenzilli, G., Bocchetti, R., Annarumma, F., Scarcelli, V., Fattorini, D., & Nigro, M. (2004). Time-course variations of oxyradical metabolism, DNA integrity and lysosomal stability in mussels, Mytilus galloprovincialis, during a field translocation experiment. Aquatic Toxicology, 68, 167–178.


Robillard, S., Beauchamp, G., & Laulier, M. (2003). The role of abiotic factors and pesticide levels on enzymatic activity in the freshwater mussel Anodonta cygnea at three different exposure sites. Comparative Biochemistry and Phy siology, Part C, 135(1), 49–59.


Sharov, A. N., & Kholodkevich, S. V. (2015). O nekotoryh osobennostyah ispol’ zovaniya presnovodnyh dvustvorchatyh molluskov pri provedenii ecotoksi kologicheskih issledovaniy na osnove monitoringa ih kardioritma volokon no-opticheskim metodom [Some features of using heart rate monitoring of freshwater bivalve mollusсs with a fiber-optical method for ecotoxicological research]. Principy Ecologii, 2, 21–28 (in Russian).


Shkorbatov, G. L., & Starobogatov, Y. I. (1990). Metody izucheniya dvustvorcha tyh molluskov [Method of investigation of bivalves]. Trudy Zoologichesko go Insituta AN SSSR, 219, 208 (in Russian).


Strayer, D. L., Downing, J. A., Haag, W. R., King, T. L., Layzer, J. B., Newton, T. J., & Nichols, J. S. (2004). Changing perspectives on pearly mussels, North America’s most imperiled animals. Bioscience, 54(1), 429–439.


Tu, H. T., Silvestre, F., Meulder, B. D., Thome, J.-P., Phuong, N. T., & Kestemont, P. (2012). Combined effects of deltamethrin, temperature and salinity on oxi dative stress biomarkers and acetylcholinesterase activity in the black tiger shrimp (Penaeus monodon). Chemosphere, 86, 83–91.


Valavanidis, A., Vlahogianni, T., Dassenakis, M., & Scoullos, M. (2006). Mole cular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicology and Environmental Safety, 64, 178–189.


Vaughn, C. C. (2010). Biodiversity losses and ecosystem function in freshwaters: Emerging conclusions and research directions. Bioscience, 60, 25–35.


Viarengo, A., Bettella, E., Fabbri, R., Burlando, B., & Lafaurie, M. (1997). Heavy metal inhibition of EROD activity in liver micomes from the Bass Dicentrarchus fabrax exposed to organic xenobiotics: Role of GSH in the reduction of heavy metal effects. Marine Environmental Research, 44(1), 1–11.


Winston, G. W., & Di Giulio, R. T. (1991). Prooxidant and antioxidant mecha nisms in aquatic organisms. Aquatic Toxicology, 19, 137–161.

Published
2018-03-09
How to Cite
Pesnya, D. S., Romanovsky, A. V., Klimova, Y. S., Fedorov, R. A., & Ivanova, E. S. (2018). Effect of sodium chloride on oxidative stress biomarkers of the freshwater bivalve Anodonta cygnea. Regulatory Mechanisms in Biosystems, 9(2), 135-140. https://doi.org/10.15421/021820