Alterations in Some Biochemical Responses of Freshwater Mussels in Acute Imidacloprid Exposure

Öz

Imidacloprid is a widely used systemic neonicotinoid insecticide. The aim of this study is to identify potential harmful effects of imidacloprid in freshwater mussels (Unio mancus) which were exposed to sub-lethal concentrations (1, 10, 100, and 1000 µg AI L^-1) for 96 h. For this aim, glutathione s-transferase (GST) activity, carboxylesterase (CaE) activity, acetylcholinesterase (AChE) activity, glutathione reductase (GR) activity, reduced glutathione (GSH) level, and malondialdehyde (MDA) level were evaluated as biochemical markers of exposure in the gills and digestive glands. The actual imidacloprid concentrations in the test waters were determined by LC-MS/MS analysis. The results showed that the AChE, GR, and CaE activities in the digestive glands significantly decreased at different exposure concentrations, while the MDA level significantly increased at the highest exposure concentration (p < 0.05). Considering the results in the gills, the lowest exposure concentration caused inhibition in AChE activity, while the highest exposure concentration caused significant induction in GST activity, GSH level and MDA level (p < 0.05). In addition, the measured imidacloprid concentrations were determined to be about 80% of the nominal imidacloprid concentrations. The data obtained from this study indicated that acute imidacloprid exposure caused biochemical alterations related to oxidative stress in mussels.

Anahtar Kelimeler

• Imidacloprid,Oxidative stress,Freshwater mussel,Neurotoxicity,LC-MS/MS

Akut İmidacloprid Maruziyetinde Tatlı Su Midyelerinin Bazı Biyokimyasal Yanıtlarındaki Değişimler

Öz

İmidacloprid yaygın olarak kullanılan bir sistemik neonikotinoid insektisittir. Bu çalışmanın amacı 96 saat süre ile imidaclopridin öldürücü olmayan konsantrasyonlarına (1, 10, 100 ve 1000 µg AI L^-1) maruz kalan tatlı su midyelerinde (Unio mancus) bu insektisitin potansiyel zararlı etkilerini belirlemektir. Bu amaçla, tatlı su midyelerinin solungaçlarında ve sindirim bezlerinde biyokimyasal belirteçler olarak glutatyon s-transferaz (GST) aktivitesi, karboksilesteraz (CaE) aktivitesi, asetilkolinesteraz (AChE) aktivitesi, glutatyon redüktaz (GR) aktivitesi, redükte glutatyon (GSH) seviyesi ve malondialdehit (MDA) seviyesi değerlendirilmiştir. Test sularındaki gerçek imidacloprid konsantrasyonları LC-MS/MS analizi ile belirlenmiştir. Sonuçlar, sindirim bezlerindeki AChE, GR ve CaE aktivitelerinin farklı maruziyet konsantrasyonlarında anlamlı olarak azaldığını, MDA seviyesinin en yüksek maruziyet konsantrasyonunda anlamlı şekilde arttığını göstermiştir (p < 0.05). Solungaçlardaki sonuçlar göz önüne alındığında, en düşük maruziyet konsantrasyonu AChE aktivitesinde inhibisyona neden olurken, en yüksek maruziyet konsantrasyonu GST aktivitesinde, GSH seviyesinde ve MDA seviyesinde önemli indüksiyona neden olmuştur (p < 0.05). Ayrıca, ölçülen imidacloprid konsantrasyonlarının nominal imidacloprid konsantrasyonlarının yaklaşık % 80'i düzeyinde olduğu belirlenmiştir. Bu çalışmadan elde edilen veriler, akut imidacloprid maruziyetinin midyelerde oksidatif stres ile ilgili biyokimyasal değişikliklere neden olduğunu göstermiştir.

Anahtar Kelimeler

• İmidacloprid,Oksidatif stres,Tatlı su midyesi,Nörotoksisite,LC-MS/MS

Kaynakça

1. [1] Arrighetti, F., Ambrosio, E., Astiz, M., Capítulo, A.R., Lavarías, S., Differential response between histological and biochemical biomarkers in the apple snail Pomacea canaliculata (Gasteropoda: Amullariidae) exposed to cypermethrin, Aquatic Toxicology, 194, 140-151, 2018.
2. [2] Iummato, M.M., Sabatini, S.E., Cacciatore, L.C., Cochón, A.C., Cataldo, D., D., de Molina, M. D. C. R., Juárez, Á. B., Biochemical responses of the golden mussel Limnoperna fortunei under dietary glyphosate exposure, Ecotoxicology and Environmental Safety, 163, 69-75, 2018.
3. [3] Vieira, C.E.D., Pérez, M.R., Acayaba, R.D.A., Raimundo, C.C.M., dos Reis Martinez, C.B., DNA damage and oxidative stress induced by imidacloprid exposure in different tissues of the Neotropical fish Prochilodus lineatus, Chemosphere, 195, 125- 134, 2018.
4. [4] Prosser, R.S., De Solla, S.R., Holman, E.A.M., Osborne, R., Robinson, S.A., Bartlett, A.J., Maisonneuve, F.J., Gillis, P.L., Sensitivity of the early-life stages of freshwater mollusks to neonicotinoid and butenolide insecticides, Environmental Pollution, 218, 428-435, 2016.
5. [5] Vehovszky, Á., Farkas, A., Csikós, V., Székács, A., Mörtl, M., Győri, J., Neonicotinoid insecticides are potential substrates of the multixenobiotic resistance (MXR) mechanism in the non-target invertebrate, Dreissena sp, Aquatic Toxicology, 205, 148-155, 2018.
6. [6] Miranda, G.R., Raetano, C.G., Silva, E., Daam, M.A., Cerejeira, M.J., Environmental fate of neonicotinoids and classification of their potential risks to hypogean, epygean, and surface water ecosystems in Brazil, Human and Ecological Risk Assessment, An International Journal, 17(4), 981-995, 2011.
7. [7] Hanana, H., Turcotte, P., André, C., Gagnon, C., Gagné, F., Comparative study of the effects of gadolinium chloride and gadolinium–based magnetic resonance imaging contrast agent on freshwater mussel, Dreissena polymorpha, Chemosphere, 181, 197-207, 2017.
8. [8] Güngördü, A., Comparative toxicity of methidathion and glyphosate on early life stages of three amphibian species: Pelophylax ridibundus, Pseudepidalea viridis, and Xenopus laevis, Aquatic Toxicology, 140, 220-228, 2013.

9. [9] Solé, M., Bonsignore, M., Rivera-Ingraham, G., Freitas, R., Exploring alternative biomarkers of pesticide pollution in clams, Marine Pollution Bulletin, 136, 61-67, 2018. [10] Pereira, P., Pablo, H., Vale, C., Pacheco, M., Combined use of environmental data and biomarkers in fish (Liza aurata) inhabiting a eutrophic and metal- contaminated coastal system–Gills reflect environmental contamination, Marine Environmental Research, 69, 53–62, 2010.
10. [11] Yang, X., Song, Y., Kai, J., Cao, X., Enzymatic biomarkers of earthworms Eisenia fetida in response to individual and combined cadmium and pyrene, Ecotoxicology and Environmental Safety, 86, 162–167, 2012.
11. [12] Khazri, A., Sellami, B., Hanachi, A., Dellali, M., Eljarrat, E., Beyrem, H., Mahmoudi, E., Neurotoxicity and oxidative stress induced by permethrin in gills of the freshwater mussel Unio ravoisieri, Chemistry and Ecology, 33(1), 88-101, 2017.
12. [13] Çekiç, F.Ö., Ekinci, S., İnal, M.S., Ünal, D., Silver nanoparticles induced genotoxicity and oxidative stress in tomato plants, Turkish Journal of Biology, 41(5), 700-707, 2017.
13. [14] USEPA, Aquatic Life Benchmarks and Ecological Risk Assessments for Registered Pesticides; OPP Aquatic Life Benchmarks, 2017, Link: https://www.epa.gov/pesticide-science-and-assessing-pesticide-risks/aquatic-life benchmarks-and-ecological-risk#benchmarks [accessed 10 April 2019].
14. [15] Bradford, M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Analytical Biochemistry, 72, 248–254, 1976.
15. [16] Jollow, D.J., Mitchell, J.R., Zampaglione, N.A., Gillette, J.R., Bromobenzene-induced liver necrosis. Protective role of glutathione and evidence for 3, 4-bromobenzene oxide as the hepatotoxic metabolite, Pharmacology, 11(3), 151-169, 1974.
16. [17] Ohkawa, H., Ohishi, N., Yagi, K., Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction, Analytical Biochemistry, 95(2), 351-358, 1979.
17. [18] Habig, W.H., Pabst, M.J., Jacoby, W.B., Glutathione S-transferases. The first enzymatic step in mercapturic acid formation, Journal of Biological Chemistry, 249, 7130–7139, 1974.
18. [19] Santhoshkumar, P., Shivanandappa, T., In vitro sequestration of two organophosphorus homologs by the rat liver, Chemico-Biological Interactions, 119- 120, 277-282, 1999.
19. [20] Elman, G.L., Courtney, K.D., Andres, J.V., Featherstone, R.M., New and rapid colorimetric determination of acetylcholinesterase activity, Biochemical Pharmacology, 7, 88–95, 1961.
20. [21] Cribb, A., Leeder, J., Spielberg, S.P., Use of a microplate reader in an assay of glutathione reductase using 5,5′-dithiobis(2-nitrobenzoic acid), Analytical Biochemistry, 183, 195-196, 1989.
21. [22] Korkmaz, V., Güngördü, A., Ozmen, M., Comparative evaluation of toxicological effects and recovery patterns in zebrafish (Danio rerio) after exposure to phosalone-based and cypermethrin-based pesticides, Ecotoxicology and Environmental Safety, 160, 265-272, 2018.
22. [23] Wu, S., Li, X., Liu, X., Yang, G., An, X., Wang, Q., Wang, Y., Joint toxic effects of triazophos and imidacloprid on zebra fish (Danio rerio), Environmental Pollution, 235, 470-481, 2018.
23. [24] Qi, S., Wang, D., Zhu, L., Teng, M., Wang, C., Xue, X., Wu, L., Neonicotinoid insecticides imidacloprid, guadipyr, and cycloxaprid induce acute oxidative stress in Daphnia magna, Ecotoxicology and Environmental Safety, 148, 352-358, 2018.
24. [25] Dondero, F., Negri, A., Boatti, L., Marsano, F., Mignone, F., Viarengo, A., Transcriptomic and proteomic effects of a neonicotinoid insecticide mixture in the marine mussel (Mytilus galloprovincialis, Lam.), Science of the Total Environment, 408(18), 3775-3786, 2010.
25. [26] Azevedo-Pereira, H.M.V.S., Lemos, M.F.L., Soares, A.M., Effects of imidacloprid exposure on Chironomus riparius Meigen larvae: linking acetylcholinesterase activity to behaviour, Ecotoxicology and Environmental Safety, 74(5), 1210-1215, 2011.
26. [27] Jemec, A., Tišler, T., Drobne, D., Sepčić, K., Fournier, D., Trebše, P., Comparative toxicity of imidacloprid, of its commercial liquid formulation and of diazinon to a non-target arthropod, the microcrustacean Daphnia magna, Chemosphere, 68(8), 1408-1418, 2007.
27. [28] Sobjak, T.M., Romão, S., Cazarolli, L.H., Sampaio, S.C., Remor, M.B., Guimarães, A.T.B., Evaluation of the antioxidant system and neurotoxic effects observed in Rhamdia branneri (Teleostei: Heptapteridae) sampled from streams of the lower Iguazu River basin, Ecotoxicology and Environmental Safety, 155, 162-170, 2018.
28. [29] Mahajan, L., Verma, P.K., Raina, R., Pankaj, N.K., Sood, S., Singh, M., Alteration in thiols homeostasis, protein and lipid peroxidation in renal tissue following subacute oral exposure of imidacloprid and arsenic in Wistar rats, Toxicology Reports, 5, 1114-1119, 2018.
29. [30] Iturburu, F.G., Zömisch, M., Panzeri, A.M., Crupkin, A.C., Contardo-Jara, V., Pflugmacher, S., Menone, M.L., Uptake, distribution in different tissues, and genotoxicity of imidacloprid in the freshwater fish Australoheros facetus, Environmental Toxicology and Chemistry, 36(3), 699-708, 2017.
30. [31] Velisek, J., Stara, A., Effect of thiacloprid on early life stages of common carp (Cyprinus carpio), Chemosphere, 194, 481-487, 2018.
31. [32] Topal, A., Alak, G., Ozkaraca, M., Yeltekin, A.C., Comaklı, S., Acıl, G., Kokturk, M., Atamanalp, M., Neurotoxic responses in brain tissues of rainbow trout exposed to imidacloprid pesticide: assessment of 8-hydroxy-2-deoxyguanosine activity, oxidative stress and acetylcholinesterase activity, Chemosphere, 175, 186-191, 2017.
32. [33] Köprücü, K., Yonar, S.M., Şeker, E., Effects of cypermethrin on antioxidant status, oxidative stress biomarkers, behavior, and mortality in the freshwater mussel Unio elongatulus eucirrus, Fisheries Science, 76(6), 1007-1013, 2010.
33. [34] Lunardelli, B., Cabral, M.T., Vieira, C.E., Oliveira, L.F., Risso, W.E., Meletti, P.C., Martinez, C.B., Chromium accumulation and biomarker responses in the Neotropical fish Prochilodus lineatus caged in a river under the influence of tannery activities, Ecotoxicology and Environmental Safety, 153, 188-194, 2018.
34. [35] Faria, M., Soares, A.M., Caiola, N., Barata, C., Effects of Camellia sinensis crude saponin on survival and biochemical markers of oxidative stress and multixenobiotic resistance of the Mediterranean mussel, Mytilus galloprovincialis, Science of the Total Environment, 625, 1467-1475, 2018.
35. [36] Shukla, S., Jhamtani, R.C., Dahiya, M.S., Agarwal, R., Oxidative injury caused by individual and combined exposure of neonicotinoid, organophosphate and herbicide in zebrafish, Toxicology Reports, 4, 240-244, 2017.