Oxidative Damages of Two Neonicotinoid Pesticides to Arthrospira platensis (Gomont)

Öz

In this study, chlorophyll-a amount, OD 560 and antioxidant parameters (total SOD, APX, GR, MDA, H2O2 and Proline) were determined in order to understand the effects of Thiacloprid and Imidacloprid on Arthrospira platensis Gomont. Both Imidacloprid and Thiacloprid applications showed significant reductions in growth rate and chlorophyll-a content of A. platensis cultures with dose-dependent manner when the days and concentrations were compared each other. SOD activity significantly decreased in the Imidacloprid application while Thiacloprid caused a significant increase only at 75 µg mL-1 concentration. APX activity significantly increased in the Imidacloprid and Thiacloprid applications at 50 µg mL-1 and 35 µg mL-1 concentrations, respectively. Imidacloprid treatment increased GR activity at 20 and 30 µg mL-1 concentrations while GR activity increased at 15, 25 and 35 µg mL-1 Thiacloprid concentrations. The MDA content of A. platensis cultures did not change with Imidacloprid or Thiacloprid applications. The H2O2 content did not change at all different Imidacloprid concentrations. However, the H2O2 content decreased at 15 µg mL-1 and increased at 45 and 75 µg mL-1 Thiacloprid concentrations. Free proline content increased in the Imidacloprid and Thiacloprid applications at 100 µg mL-1 and 75 µg mL-1 concentrations, respectively. These neonicotinoid pesticides cause oxidative stress in A. platensis cells.

Anahtar Kelimeler

• Arthrospira platensis
• oxidative stess
• antioxidant
• thiacloprid
• imidacloprid

Kaynakça

1. Aiba S and Ogawa T. 1977. Assessment of Growth Yield of a Bluegreen Alga, Spirulina platensis, in Axenic and Continuous Culture. Microbiol. 102: 179-182. doi:10.1099/00221287-102-1-179
2. Akbaş D, Askın A, Çömelekoglu U. 2014. Influence of neurotransmission in frog peripheral nerve by the neonicotinoid insecticide imidacloprid: an electrophysiological study. Fresenius Environ Bull. 23(8): 1816-1823.
3. Asada K. 1984. Chloroplasts: formation of active oxygen and its scavenging. Methods Enzymol. 10: 422-429. doi:10.1016/S0076-6879(84)05059-X
4. Bartosz G. 1997. Oxidative stress in plants. Acta Physiol Plant. 19:7-64
5. Beketov MA, Liess M. 2008. Acute and delayed effects of the neonicotinoid insecticide thiacloprid on seven freshwater arthropods. Environ Toxicol Chem Inter. J 27(2): 461-470. doi:10.1897/07-322R.1
6. Beketov MA, Schäfer RB, Marwitz A, Paschke A, Liess M. 2008. Long-term stream invertebrate community alterations induced by the insecticide thiacloprid: effect concentrations and recovery Dynamics. Sci Total Environ. 405(1-3): 96-108. doi: 10.1016/j.scitotenv.2008.07.001
7. Beyer WF, and Fridovich I. 1987. Assaying for superoxide dismutase activity: Some large consequences of minor changes in conditions. Anal Biochem. 161: 559-566. doi:10.1016/0003-2697(87)90489-1
8. Bolboaca SD, Jaentschi L. 2005. Molecular descriptors family on structure activity relationships. 2. Insecticidal activity of neonicotinoid compounds. J Pest Sci. 4: 78–85.

9. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72: 248-254. doi:10.1016/0003-2697(76)90527-3
10. Bray EA, Bailey-Serres J, Weretilnyk E. 2000. Responses to abiotic stress Biochemistry and Molecular Biology of Plants. American Society of Plant Biologists, Waldorf, 1158-1203 s.
11. British Crop Protection Council (BCPC). 2004. the e-Pesticide Manual, Version 3.1- 2004–05, 13th ed.
12. Casida JE, Durkin K. 2013. Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annu Rev Entomol. 58: 99-117. doi:10.1146/annurev-ento-120811-153645
13. Chen S, Wang L, Feng W, Yuan M., Li J, Xu H, Zhang Z, Zhang W. 2020. Sulfonamides-induced oxidative stress in freshwater microalga Chlorella vulgaris: Evaluation of growth, photosynthesis, antioxidants, ultrastructure, and nucleic acids- Sci Rep. 10(1): 1-11. doi:10.1038/s41598-020-65219-2
14. Choudhary M, Kumar U, Mohammed J, Khan A, Zutshi S, Fatma T. 2007. Effect of heavy metal stress on proline, malondialdehyde, and superoxide dismutase activity in the cyanobacterium Spirulina platensis-S5. Ecotox Environ Safe. 66 (2): 204-209. doi: 10.1016/j.ecoenv.2006.02.002
15. Daneshvar N, Khataee AR, Ghadim AA, Rasoulifard MH. 2007. Decolorization of CI Acid Yellow 23 solution by electrocoagulation process: Investigation of operational parameters and evaluation of specific electrical energy consumption (SEEC). J Hazar Mater. 148(3): 566-572. doi: 10.1016/j.jhazmat.2007.03.028
16. Del Vos CH, Vonk MJ, Schat H. 1992. Glutathione depletion due to copper induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. Plan Physiol. 98: 853-858. doi:10.1104/pp.98.3.853
17. Del-Rio LA, Sevilla F, Sandalio LM, Palma JM. 1991. Nutritional effect and expression of superoxide dismutase; induction and gene expression, diagnostics, prospective protection against oxygen toxicity. Free Radic Res Commun. 12(13): 819-828 doi:10.3109/10715769109145863
18. Durner J, Klessig DF. 1995. Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses. Proc Natl Acad Sci. U S A, 92(24): 11312–11316 s. doi:10.1073/pnas.92.24.11312
19. Duval B, Shetty K, Thomas WH. 1999. Phenolic compounds and antioxidant properties in the snow alga Chlamydomonas nivalis after exposure to UV light. J Appl Phycol. 11: 559-565.
20. EPA. 2003. US EPA. Pesticides; Thiacloprid, Washington United States
21. EPA, U. Environmental Protection Agency. 2008. Mercury Human Exposure: http://www. epa. gov/hg/exposure. Html
22. Fatma T, Khan A, Choudhary M. 2007. Impact of environmental pollution on cyanobacterial proline content. J Appl Phycol. 19(6): 625–629. doi:10.1007/s10811-007-9195-2
23. Franco JC, Zada A, Mendel Z. 2009. Novel approaches for the management of mealybug pests. In: Ishaaya I, Horowitz AR, editors. Bioration-al Control of Arthropod Pests Application and Resistance Management. Netherlands: Springer. s 233–278.
24. Galhano V, Laranjo JG, Peixoto F. 2011. Exposure of the cyanobacterium Nostoc muscorum from Portuguese rice fields to Molinate (Ordram®): Effects on the antioxidant system and fatty acid profile. Aquat Toxicol. 101(2): 367-376. doi: 10.1016/j.aquatox.2010.11.011
25. Galhano V, Peixoto F, Gomes J. 2010. Bentazon triggers the promotion of oxidative damage in the Portuguese ricefield cyanobacterium Anabaena cylindrica: Response of the antioxidant system. Environ Toxicol. 25(5): 517–526. doi:10.1002/tox.20597
26. Halliwell B. 1987. Oxidative damage, lipid peroxidation and antioxidant protection in chloroplasts. Chem Phys Lipid. 44(2-4): 327-340. doi:10.1016/0009-3084(87)90056-9
27. Heath RL, Packer L. 1968. Photoperoxidation in isolated Chloroplasts. I. Stoichiometry of fatty acid peroxidation. Arch Biochem Biophys. 125: 189-198. doi:10.1016/0003-9861(68)90654-1
28. Hendry GAF. 1994. Oxygen and environmental stress in plants: an evolutionary context. Proc R Soc Edinb, 102B: 155-165. doi:10.1017/S026972700001407X
29. Jeschke P, Nauen R, Schindler M, Elbert A. 2011. Overview of the status and global strategy for neonicotinoids. J Agric Food Chem. 59(7): 2897-2908.
30. Jiménez A, Hernández JA, Pastori GM, Del Río LA, Sevilla F. 1998. The role of the ascorbate–glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol. 118: 1327-1335. doi:10.1104/pp.118.4.1327
31. Karahan A, Kutlu MA, Gül A, Karaca İ. 2018. The Effect of Pesticides on Honey Bees. 6th International Muğla Beekeeping and Pine Honey Congress; Muğla Turkiye.
32. Kocaman AY, Rencüzoğulları E, Topaktaş M. 2014. In vitro investigation of the genotoxic and cytotoxic effects of thiacloprid in cultured human peripheral blood lymphocytes. Environ Toxicol. 29(6): 631-641. doi:10.1002/tox.21790
33. Kumar S, Habib K, Fatma T. 2008. Endosulfan induced biochemical changes in nitrogen-fixing cyanobacteria. Sci The Total Environ. 403(1–3): 130-138. doi: 10.1016/j.scitotenv.2008.05.026
34. Kumar S, Praveenkumar R, Jeon BH, Thajuddin N. 2014. Chlorpyrifos-induced changes in the antioxidants and fatty acid compositions of Chroococcus turgidus NTMS12. Lett Appl Microbiol. 59(5): 535–541. doi:10.1111/lam.12311
35. Li X., Ping X., Xiumei S., Zhenbin W., Liqiang X. 2005. Toxicity of cypermethrin on growth, pigments, and superoxide dismutase of Scenedesmus obliquus. Ecotoxicol Environ Saf. 60(2): 188-92. doi:10.1016/j.ecoenv.2004.01.012
36. Liu L, Zhu B, Wang GX. 2015. Azoxystrobin-induced excessive reactive oxygen species (ROS) production and inhibition of photosynthesis in the unicellular green algae Chlorella vulgaris. Environ Sci Poll Res. 22(10): 7766-7775. doi:10.1007/s11356-015-4121-7
37. MacKinney G. 1941. Absorption of light by chlorophyll solution. J Biol Chem. 140: 315-322.
38. Malato S, Caceres J, Agüera A, Mezcua M, Hernando D, Vial J, Fernández-Alba AR. 2001. Degradation of imidacloprid in water by photo-Fenton and TiO2 photocatalysis at a solar pilot plant: a comparative study. Environ Sci Tech. 5(21): 4359-4366. doi:10.1021/es000289k
39. Malev O, Klobučar RS, Fabbretti E, Trebše P. 2012. Comparative toxicity of imidacloprid and its transformation product 6-chloronicotinic acid to non-target aquatic organisms: Microalgae Desmodesmus subspicatus and amphipod Gammarus fossarum. Pestic Biochem Physiol. 104(3): 178-186. doi: 10.1016/j.pestbp.2012.07.008
40. Matsuda K, Kanaoka S, Akamatsu M, Sattelle DB. 2009. Diverse actions and target-site selectivity of neonicotinoids: structural insights. Mol Pharm. 76(1): 1-10. doi:10.1124/mol.109.055186
41. Matsuda K, Shimomura M, Ihara M, Akamatsu M, Sattelle DB. 2005. Neonicotinoids show selective and diverse actions on their nicotinic receptor targets: electrophysiology, molecular biology, and receptor modeling studies. Biosci Biotechnol Biochem. 69(8): 1442-1452. doi:10.1271/bbb.69.1442
42. Mofeed J, Mosleh YY. 2013. Toxic responses and antioxidative enzymes activity of Scenedesmus obliquus exposed to fenhexamid and atrazine, alone and in mixture. Ecotoxicol Environ Safe. 95: 234-240. doi: 10.1016/j.ecoenv.2013.05.023
43. Morrissey CA, Mineau P, Devries JH, Sanchez-Bayo F, Liess M, Cavallaro MC, Liber K. 2015. Neonicotinoid contamination of global surface waters and associated risk to aquatic invertebrates: a review. Environment Inter. 74: 291-303. doi: 10.1016/j.envint.2014.10.024
44. Olga B, Eija V, Kurt VF. 2003. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot. 91: 179-194. doi:10.1093/aob/mcf118
45. Prasad SM, Kumar D, Zeeshan M. 2005. Growth, photosynthesis, active oxygen species and antioxidants responses of paddy field cyanobacterium Plectonema boryanum to endosulfan stress. J Gen Appl Microbiol. 51(2): 115-23. doi:10.2323/jgam.51.115
46. Qian H, Chen W, Sheng GD, Sun L, Jin Y, Liu W, Fu Z. 2009. Inhibitory effects of paraquat on photosynthesis and the response to oxidative stress in Chlorella vulgaris. Ecotoxicol. 18 (5): 537–543. doi:10.1007/s10646-009-0311-8
47. Qian H, Chen W, Sheng GD, Xu X, Liu W, Fu Z. 2008. Effects of glufosinate on antioxidant enzymes, subcellular structure, and gene expression in the unicellular green alga Chlorella vulgaris. Aquatic Toxicol. 88(4): 01-307. doi: 10.1016/j.aquatox.2008.05.009
48. Rabinowich HD, Fridovich I. 1985. Cell content of superoxide dismutase and resistance to paraquat in Chlorella sorokiniana. Planta. 164: 524.
49. Salman JM, Abdul-Adel E, AlKaim AFA. 2016. Effect of pesticide Glyphosate on some biochemical features in cyanophyta algae Oscillatoria limnetica. Int J PharmTech Res. 9(8): 355-365.
50. Schmuck R, Schöning R, Stork A, Schramel O. 2001. Risk posed to honeybees (Apis mellifera L, Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Management Science: formerly Pest Sci. 57(3): 225-238. doi:10.1002/ps.270
51. Schuld M, Schmuck R. 2000. Effects of Thiacloprid, a new chloronicotinyl insecticide, on the egg parasitoid Trichogramma cacaoeciae. Ecotoxicol. 9(3): 197-205.
52. Sebaugh JL. 2011. Guidelines for accurate EC50/IC50 estimation. Pharmaceutical statistics, 10(2): 128-134. doi:10.1002/pst.426
53. Sgherri CLM, Loggini B, Puliga S, Navari-Izzo F. 1994. Antioxidant system in Sporobolus stapfianus: changes in response to desiccation and rehydration. Phytochem. 35: 561-565. doi:10.1016/S0031-9422(00)90561-2
54. Siripornadulsil S, Traina S, Verma DPS, Sayre RT. 2002. Molecular Mechanisms of Proline-Mediated Tolerance to Toxic Heavy Metals in Transgenic Microalgae. Plant Cell. 14(11): 2837–2847. doi:10.1105/tpc.004853
55. Smirnoff N. 1993. The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol. 125: 27-58.
56. Starner K, Goh KS. 2012. Detections of the neonicotinoid insecticide imidacloprid in surface waters of three agricultural regions of California, USA- 2010–2011. Bull Environ Contam Toxicol. 88(3): 316-321. DOI 10.1007/s00128-011-0515-5
57. Tankiewicz M, Fenik J, Biziuk M. 2010. Determination of organophosphorus and organonitrogen pesticides in water samples. TrAC Trend Anal Chem. 29(9): 1050-1063. doi: 10.1016/j.trac.2010.05.008
58. Tišler T, Jemec A, Mozetič B, Trebše P. 2009. Hazard identification of imidacloprid to aquatic environment. Chemosphere. 76(7): 907-914. doi: 10.1016/j.chemosphere.2009.05.002
59. Tunca H. 2020. Determination of changes in Arthrospira platensis antioxidant activity and growth parameters due to oxidative stress arising from Lambda cyhalothrin. Ann Limnol. 56: 1. doi:10.1051/limn/2020024
60. Verma S, Dubey RS. 2003. Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci. 164: 645–65. doi:10.1016/S0168-9452(03)00022-0
61. Wang SY, Jiao H, Faust M. 1991. Changes in ascorbate, glutathione and related enzyme activity during thidiazuron-induced bud break of apple. Physiol Plant. 82: 231-236. doi:10.1111/j.1399-3054.1991.tb00086.x
62. Weckx JEJ, Clijsters MM. 1996. Oxidative damage and defense mechanisms in primary leaves of Phaseolus vulgaris as a result of root assimilation of toxic amounts of copper. Physiol Plant. 96(3): 506–512. doi:10.1111/j.1399-3054.1996.tb00465.x
63. Weimberg R. 1987. Solute adjustments in leaves of two species of wheat at two different stages of growth in response to salinity. Physiol Plant. 70: 381-388. doi:10.1111/j.1399-3054.1987.tb02832.x
64. Wood TJ, Goulson D. 2017. The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013. Environ Sci Poll Res. 24(21): 17285-17325. doi: 10.1007/s11356-017-9240-x