Biochemical response of earthworm, Eisenia fetida to heavy metals toxicity
Article Main
Abstract
Soil heavy metal pollution is widespread and has severe adverse effects on soil organisms. Earthworms are the major soil organisms which perform several beneficial ecological functions butare vulnerable to damage from heavy metal pollution of soil. The present study was conducted to evaluate the potential toxicity of arsenic (As) and chromium (Cr) on the biochemical response of the earthworm, Eisenia fetida. Following exposure to various sub-lethal concentrations ofAs (34, 68, 102 and 136 mg/kg) and Cr(26, 51, 77 and 102 mg/kg ) for 28 days, the levels of several biochemical markers, including superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), Glutathione-S-transferase (GST) and malondialdehyde (MDA) content were assessed. The results showed that both heavy metals significantly (p<0.05) impacted the antioxidant enzyme activities and MDA content during the entire exposure period. Compared with the control, SOD, CAT, POD and GST activities increased significantly (p<0.05) by (6.21-23.23, 6.32-18.6, 15.87-34.18 and 0.84-5.45% respectively) at14th day, but after prolonged exposure, these activities were significantly (p<0.05) decreased (9.58-38.13, 10.09-30.03, 19.05-53.16 and 2.26-9.36% respectively) at 28th day. The contents of MDA showed significant (p<0.05) increase (17.84-45.59%) in all exposure groups for entire exposure period. Therefore, it can be concluded that antioxidants play a direct role in the adaptive response of E. fetida for survival in heavy metal contaminated soil. This adaptive antioxidant response can be used as an important biomarker to assess the toxicity of heavy metals in the soil ecosystems.
Article Details
Article Details
Antioxidant enzymes, Biomarker, Earthworms, Eisenia fetida, Heavy metals toxicity
Asada, K., Takahashi, M. & Nagate, M. (1974). Assay and inhibitors of spinach superoxide dismutase. Agriculural and Biological Chemistry, 38, 471-473.https://doi.org/10.1080/00021369.1974.10861178
Basha, P.M. & Latha, V. (2016). Evaluation of sublethal toxicity of zinc and chromium in Eudriluseugeniae using biochemical and reproductive parameters. Ecotoxicology, 25(4), 802-813.https://doi.org/10.10 07/s10646-016-1637-7
Chao, G., Jingbo, X., Ji, L. & Zhengtao, L. (2016). Biological responses in the earthworm Eisenia fetida exposed to soils near a typical lead acid battery plant. Soil and Sediment Contamination: An International Journal, 25(5), 573-585.https://doi.org/10.1080/15320383.2016.1184619
Chen, J., Saleem, M., Wang, C., Liang, W. & Zhang, Q. (2018). Individual and combined effects of herbicide tribenuron-methyl and fungicide tebuconazole on soil earthworm Eisenia fetida. Scientific Reports, 8, 2967.https://doi.org/10.1038/s41598-018-21288-y
Datta, S., Singh, J., Singh, S. & Singh, J. (2016). Earthworms, pesticides and sustainable agriculture: a review. Environmental Science and Pollution Research, 23 (9), 8227-8243.https://doi.org/10.1007/s11356-016-6375-0
El-Demerdash, F.M., Yousef, M. I. & Radwan, F. M.(2009). Ameliorating effect of curcumin on sodium arsenite-induced oxidative damage and lipid peroxidation in different rat organs. Food and Chemical Toxicology, 47, 249-254.https://doi.org/10.1016/j.fct.2008.11.013
Ezemonye, L. & Tongo, I.(2010). Sublethal effects of endosulfan and diazinon pesticides on glutathione-S-transferase (GST) in various tissues of adult amphibians (Bufo regularis). Chemosphere, 81, 214-217.https://doi.org/10.1016/j.chemosphere.2010.06.039
Giannopolitis, C.N. & Ries, S. K. (1977). Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology, 59, 309-314.https://doi.org/10.1104/pp.59.2.309
Habig, W.H., Pabst, M.J. & Jacoby, W. B. (1974). Glutathione s-transferases: the first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 249, 7130-7139.https://doi.org/10.1016/S0021-9258(19)42083-8
Heath, R.L. & Packer, L. (1968). Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics, 125, 189-198.https://doi.org/10.1016/0003-9861(68)90654-1
Ighodaro, O.M. & Akinloye, O.A. (2018). First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alexandria Journal of Medicine, 54(4), 287-293.DOI: 10.1016/j.ajme.2017.0 9.0 01
Jeyanthi, V., Paul, J. A. J., Selvi, B. K. & Karmegam, N. (2016). Comparative Study of Biochemical Responses in Three Species of Earthworms Exposed to Pesticide and Metal Contaminated Soil. Environmental Processes, 3, 167-178.https://doi.org/10.1007/s40710-016-0131-9
Li, Y., Zhang, F., Ai, X., Wang, X., Robin, P., Cavanagh, J., Matthew, C. & Qiu, J. (2015). Antioxidant and behavior responses of earthworms after introduction to a simulated vermifilter environment. Ecological Engineering, 81, 218-227.https://doi.org/10.1016/j.ecoleng.2015.04.045
Liang, X., Zhou, D., Wang, J., Li, Y., Liu, Y. & Ning, Y.(2022). Evaluation of the toxicity effects of microplastics and cadmium on earthworms. Science of The Total Environment, 836, 155747.https://doi.org/10.1016/j.scitoten v.2022.155747
Lin, D., Zhou, Q., Xie, X. & Liu, Y. (2010). Potential biochemical and genetic toxicity of triclosan as an emerging pollutant on earthworms (Eisenia fetida). Chemosphere, 81, 1328-1333.https://doi.org/10.1016/j.chemosphere.20 10.08.027
Liu, K., Chen, L., Zhang, W., Lin, K. F. & Zhao, L. (2015). EPR detection of hydroxyl radical generation and oxidative perturbations in lead-exposed earthworms (Eisenia fetida) in the presence of decabromodiphenyl ether. Ecotoxicology, 24, 301-308.https://doi.org/10.1007/s10646-014-1378-4
Liu, S., Zhou, Q.X. & Chen, C. (2012). Antioxidant enzyme activities and lipid peroxidation in earthworm Eisenia fetida exposed to 1,3,4,6,7,8-hexahydro4,6,6,7,8,8-hexamethyl-cyclopenta-c-2-benzopyran. Environmental Toxicology, 27, 472-479. https://doi.org/10.1002/tox.20661
Liu, S., Zhou, Q. X. & Wang, Y.Y. (2011). Ecotoxicological responses of the earthworm Eisenia fetida exposed to soil contaminated with HHCB. Chemosphere, 83, 1080-1086.https://doi.org/10.1016/j.chemosphere.2011.01.046
Liu, T., Wang, X., You, X., Chen, D., Li, Y. & Wang, F. (2017). Oxidative stress and gene expression of earthworm (Eisenia fetida) to clothianidin. Ecotoxicology and environmental safety, 142, 489-496. https://doi.org/10.10 16/j.ecoenv.2017.04.012
Liu, T., Wang, X., Chen, D., Li, Y. & Wang, F. (2018). Growth, reproduction and biochemical toxicity of chlorantraniliprole in soil on earthworms (Eisenia fetida). Ecotoxicology and Environmental Safety, 150, 18-25. https://doi.org/10.1016/j.ecoenv.2017.12.010
Ma, T., Chen, L.W., Zhang, H. & Luo, Y. (2016). Oxidative stress, cytotoxicity and genotoxicity in earthworm Eisenia fetida at different di-n-butyl phthalate exposure levels. PLoS One, 11(3), e0151128. https://doi.org/10.1371/journal.pone.0151128.
Maity, S., Poracova, J., Dey, P., Vaskova, J., Vasko, L., Sedlak, V. & Mydlarova Blascakova, M. (2018). Antioxidant responses in the earthworm Aporrectodea caliginosa of eastern Slovakia: application of principal component analysis as a tool to identify metal contaminated areas. Environmental monitoring and assessment, 190(1), 1-16.https://doi.org/10.1007/s10661-017-6377-5
Maity, S., Roy, S., Chaudhury, S. & Bhattacharya, S.(2008). Antioxidant responses of the earthworm Lampitomauritii exposed to Pb and Zn contaminated soil. Environmental Pollution, 151, 1-7.https://doi.org/10.1016/j.envpol.2007.03.005
Markad, V. L., Gaupale, T. C., Bhargava, S., Kodam, K. M. & Ghole, V. S. (2015). Biomarker responses in the earthworm, Dichogaster curgensis exposed to fly ash polluted soils. Ecotoxicology and Environmental Safety, 118, 62-70.https://doi.org/10.1016/j.ecoenv.2015.04.011
OECD, (1984). Earthworm, acute toxicity tests. Guideline for Testing Chemicals 207. OECD, Paris, France.
Otmani, H., Tadjine, A., Moumeni, O., Zeriri, I., Amamra, R., Samira, D.B., Djebar, M.R. & Berrebbah, H. (2018). Biochemical responses of the earthworm Allolobophoracaliginosa exposed to cadmium contaminated soil in the Northeast of Algeria. Bulletin de la Societe Royale des Sciences de Liege. DOI: 10.25518/0037-9565.7331
Pratviel, G. (2012). Oxidative DNA damage mediated by transition metal ions and their complexes. In: Sigel, Astrid, Sigel, Helmut, Roland, K.O. Sigel (Eds.), Interplay between Metal Ions and Nucleic Acids. Metals Ions in Life Sciences 10. Springer, 201-216 Chapter 7.https://doi.org/10.1007/978-94-007-2172-2_7
Ray, S., Gautam, A., Ray, A., Das, S. & Ray, M. (2019). Analysis of oxidative stress and cellular aggregation in the coelomocytes of earthworms collected from metal contaminated sites of industrial and agricultural soils of West Bengal, India. Environmental Science and Pollution Research, 26(22), 22625-22640.https://doi.org/10.1007/s11356-019-05438-x
Roubalova, R., Prochazkova, P., Dvorak, J., Skanta, F. & Bilej, M. (2015). The role of earthworm defense mechanisms in ecotoxicity studies. Invertebrate Survival Journal, 12, 203-213.
Saleeb, N., Robinson, B., Cavanagh, J., Ross, J., Munir, K. & Gooneratne, R. (2020). Antioxidant enzyme activity and lipid peroxidation in Aporrectodea caliginosa earthworms exposed to silver nanoparticles and silver nitrate in spiked soil. Environmental Toxicology and Chemistry, 39(6), 1257-1266.https://doi.org/10.1002/etc.4713
Shi, Y.J., Xu, X.B., Zheng, X. Q. & Lu, Y.L. (2015). Responses of growth inhibition and antioxidant gene expression in earthworms (Eisenia fetida) exposed to tetrabromobisphenol A, hexabromocyclododecane and decabromodiphenyl ether. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 174, 32-38.https://doi.org/10.1016/j.cbpc.2015.06.005
Song, Y., Zhu, L.S., Wang, J., Wang, J.H., Liu, W. & Xie, H. (2009). DNA damage and effects on antioxidative enzymes in earthworm (Eisenia foetida) induced by atrazine. Soil Biology and Biochemistry, 41, 905-909.https://doi.org/10.1016/j.soilbio.2008.09.009
Sun, Y. Y., Yin, Y., Zhang, J. F., Yu, H. X. & Wang, X. R. (2007). Bioaccumulation and ROS generation in liver of freshwater fish, goldfish Carassius auratus under HC Orange No. 1 exposure. Environmental Toxicology, 22, 256-263.https://doi.org/10.1002/tox.20262
Tiwari, R.K., Singh, S. & Pandey, R.S. (2019). Assessment of acute toxicity and biochemical responses to chlorpyrifos, cypermethrin and their combination exposed earthworm, Eudrilus eugeniae. Toxicology reports, 6,288-297.https://doi.org/10.1016/j.toxrep.2019.03.007
Vlahogianni, T.H. & Valavanidis, A. (2007). Heavy-metal effects on lipid peroxidation and antioxidant defence enzymes in mussels Mytilus galloprovincialis. Chemistry and Ecology, 23(5), 361-371.https://doi.org/10.1080/02757540 701653285
Wang, H. & Xie, X. Y. (2014). Effects of combined pollution of Cd, Cu and Pb on antioxidant enzyme activities of earthworm in soils. Environmental Science, 35 (7), 2748-2754. https://doi.org/10.13227/j.hjkx.2014.07.044.
Wang, Y., Wu, Y., Cavanagh, J., Yiming, A., Wang, X., Gao, W., Matthew, C., Qiu, J. & Li, Y. (2018). Toxicity of arsenite to earthworms and subsequent effects on soil properties. Soil Biology and Biochemistry, 117, 36-47.https://doi.org/10.1016/j.soilbio.2017.11.007
Wang, Z., Cui, Z., Liu, L., Ma, Q. & Xu, X. (2016). Toxicological and biochemical responses of the earthworm Eisenia fetida exposed to contaminated soil: effects of arsenic species. Chemosphere, 154, 161-170.https://doi.org/1 0.1016/j.chemosphere.2016.03.070
Wen, S., Liu, C., Wang, Y., Xue, Y., Wang, X., Wang, J., Xia, X. & Kim, Y.M. (2021). Oxidative stress and DNA damage in earthworm (Eisenia fetida) induced by triflumezopyrim exposure. Chemosphere, 264, 128499. https://doi.org/10.1016/j.chemosphere.2020.128499
Wu, B., Liu, Z., Xu, Y., Li, D. & Li, M. (2012). Combined toxicity of cadmium and lead on the earthworm Eisenia fetida (Annelida, Oligochaeta). Ecotoxicology and Environmental Safety, 81, 122-126.https://doi.org/10.1016/j.ecoenv.2012.05.003
Wu, D., Liu, M., Song, X., Jiao, J., Li, H. & Hu, F. (2015). Earthworm ecosystem service and dis-service in an N-enriched agroecosystem: increase of plant production leads to no effects on yield-scaled N2O emissions. Soil Biology and Biochemistry, 82, 1-8.https://doi.org/10.1016/j.soilbio.2014.12.009
Xu, D. M., Li, C. D., Wen, Y. Z. & Liu, W. P. (2013). Antioxidant defense system responses and DNA damage of earthworms exposed to perfluorooctane sulfonate (PFOS). Environmental Pollution, 174:121-1.https://doi.org/10.1016/j.envpol.2012.10.030
Xu, J. B., Yuan, X. F. & Lang, P. Z. (1997). Determination of catalase activity and catalase inhibition by ultraviolet spectrophotometry. Environmental Chemistry, 16, 73-76.
Xu, Z., Yang, Z., Shu, W. & Zhu, T. (2021). Combined toxicity of soil antimony and cadmium on earthworm Eisenia fetida: accumulation, biomarker responses and joint effect. Journal of Hazardous Materials Letters, 2, 100018.https://doi.org/10.1016/j.hazl.2021.100018
Xue Y., Gu X., Wang X., Sun C., Xu X., Sun J & Zhang B. (2009). The hydroxyl radical generation and oxidative stress for the earthworm Eisenia fetida exposed to tetrabromobisphenol A. Ecotoxicology, 18, 693-699.https://doi.org/10.1007/s10646-009-0333-2
Yao, X., Zhang, F., Qiao, Z., Yu, H., Sun, S., Li, X., Zhang, J. & Jiang, X. (2020). Toxicity of thifluzamide in earthworm (Eisenia fetida). Ecotoxicology and Environmental Safety, 188, 109880. https://doi.org/10.1016/j.ecoenv.2019.109880
Zhang, Q. M., Zhang, B. H. & Wang, C. X. (2014). Ecotoxicological effects on the earthworm Eisenia fetida following exposure to soil contaminated with imidacloprid. Environmental Science and Pollution Research, 21, 12345-12353.https://doi.org/10.1007/s11356-014-3178-z
Zhang, Q., Zhu, L., Wang, J., Xie, H., Wang, J., Han, Y. & Yang, J. (2013). Oxidative stress and lipid peroxidation in the earthworm Eisenia fetida induced by low doses of fomesafen. Environmental Science and Pollution Research, 20(1), 201-208. https://doi.org/10.1007/s11356-012-0962-5
Zheng, K., Liu, Z., Li, Y., Cui, Y. & Li, M. (2013). Toxicological responses of earthworm (Eisenia fetida) exposed to metal-contaminated soils. Environmental Science and Pollution Research, 20(12), 8382-8390.https://doi.org/1 0.1007/s11356-013-1689-7
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
This work is licensed under Attribution-NonCommercial 4.0 International (CC BY-NC 4.0) © Author (s)