Heavy Metal Pollution and Temperature Stress Induced Changes in Acetyl Choline Esterase Activity in Two Ecologically Different Earthworm Species
Abstract
Acetyl choline esterase is an enzyme participating in cholinergic system and breaks down acetylcholine into choline and acetate, terminating the neurotransmission process. The study highlights the influence of temperature on AChE activity in two ecologically different earthworm species viz., epigeic- Eudrilus eugeniae and aneic- Lampito mauritii when exposed to metal stress and temperature co-exposure. In Eudrilus eugeniae, an augmentation in the level of AChE was observed upon exposure to both metals (Zn2+ and Cr6+) while Zn2+ co-exposures carried at 18oC and 28oC found to inhibit the activity on day 21 and 28 highlighting the modulatory effect of temperature in augmenting the toxic potential of Zn2+. Chromium exposures carried out at 18oC caused a significant (p<0.05) augmentation in AChE activity on day 7, 14 and 21 and the observed % change found to be +95.75, +27.71 and +32.99 respectively; while a considerable suppression in its activity was evident on day 28 (-29.17 %). Whereas, in Lampito mauritii, a considerable augmentation in AChE activity was evident upon exposure to both metals, while a significant (p<0.05) inhibition in enzyme activity levels was evident in Zn2+ exposure at 18oC and 28oC explaining the influence of temperature in augmenting the toxicity. Likewise, Cr6+ co-exposures carried out at 18oC found to inhibit AChE activity on day 21 and 28 and similar, inhibition was evident in exposures made at 28oC on day 7 and 28 with exception on day 21 wherein increased AChE activity levels were observed. Thus emphasising significant role of temperature in routine toxicological assessments.
Keywords:
AChE Activity, Eudrilus Eugeniae, Hexavalent Chromium, Lampito Mauritii, Temperature Toxicity, Zinc
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References
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Bednarska, A. J., Choczyński, M., Laskowski, R., & Walczak, M. (2017). Combined effects of chlorpyriphos, copper and temperature on acetylcholinesterase activity and toxicokinetics of the chemicals in the earthworm Eisenia fetida. Environmental Pollution, 220, 567-576. https://doi.org/10.1016/j.envpol.2016.10.004
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Booth, L. H., & O'Halloran, K. (2001). A comparison of biomarker responses in the earthworm Aporrectodea caliginosa to the organophosphorus insecticides diazinon and chlorpyrifos. Environmental Toxicology and Chemistry: An International Journal, 20(11), 2494-2502. https://doi.org/10.1897/1551-5028(2001)020%3C2494:acobri%3E2.0.co;2
Brown, R. J., Galloway, T. S., Lowe, D., Browne, M. A., Dissanayake, A., Jones, M. B., & Depledge, M. H. (2004). Differential sensitivity of three marine invertebrates to copper assessed using multiple biomarkers. Aquatic Toxicology, 66(3), 267-278. https://doi.org/10.1016/j.aquatox.2003.10.001
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Calisi, A., Lionetto, M.G., & Schettino, T. (2009). Pollutant-induced alterations of granulocyte morphology in the earthworm Eisenia foetida. Ecotoxicology and Environmental Safety. 72(5), 1369-1377. https://doi.org/10.1016/j.ecoenv.2009.03.010
Caselli, F., Gastaldi, L., Gambi, N., & Fabbri, E. (2006). In vitro characterization of cholinesterases in the earthworm Eisenia andrei. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 143(4), 416-421. https://doi.org/10.1016/j.cbpc.2006.04.003
Diamantino, T. C., Almeida, E., Soares, A. M. V. M., & Guilhermino, L. (2003). Characterization of cholinesterases from Daphnia magna straus and their inhibition by zinc. Bulletin of Environmental Contamination & Toxicology, 71(2), 0219–0225. https://doi.org/10.1007/s00128-003-0153-7
Ducros V. (1992). Chromium Metabolism. Biological Trace Element Research, 32(1-3), 65-77. https://doi.org/10.1007/bf02784589
Dzul-Caamal, R., Vega-López, A., & Osten, J. R. V. (2024). Integrated evaluation of the biological response of the earthworm Eisenia fetida using two glyphosate exposure strategies: soil enriched and soils collected from crops in Southeastern Mexico. Environmental Science and Pollution Research, 1-16. Available at: https://ui.adsabs.harvard.edu/abs/2024ESPR...3132152D/abstract
Ellman, G. L., Courtney, K. D., Andres Jr, V., & Featherstone, R. M. (1961). A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology, 7(2), 88-95. https://doi.org/10.1016/0006-2952(61)90145-9
Grisaru, D., Pick, M., Perry, C., Sklan, E. H., Almog, R., Goldberg, I., ... & Deutsch, V. (2006). Hydrolytic and nonenzymatic functions of acetylcholinesterase comodulate hemopoietic stress responses. The Journal of Immunology, 176(1), 27-35. https://doi.org/10.4049/jimmunol.176.1.27
Gudeta, K., Kumar, V., Bhagat, A., Julka, J. M., Bhat, S. A., Ameen, F., & Amarowicz, R. (2023). Ecological adaptation of earthworms for coping with plant polyphenols, heavy metals, and microplastics in the soil: A review. Heliyon, 9(3). https://doi.org/10.1016/j.heliyon.2023.e14572
Hagger, J. A., Jones, M. B., Leonard, D. P., Owen, R., & Galloway, T. S. (2006). Biomarkers and integrated environmental risk assessment: are there more questions than answers? Integrated Environmental Assessment and Management: an International Journal, 2(4), 312-329. https://doi.org/10.1002/ieam.5630020403
Kammenga, J. E., Dallinger, R., Donker, M. H., Köhler, H. R., Simonsen, V., Triebskorn, R., & Weeks, J. M. (2000). Biomarkers in terrestrial invertebrates for ecotoxicological soil risk assessment. Reviews of Environmental Contamination and Toxicology, 164, 93-147.
Latha, V., & Basha, P. M. (2016). Extent of heavy metal accumulation in sewage irrigated soils and their impact on distribution of earthworm communities: linking Chromium and Zinc toxicity on growth and reproduction in selected earthworm species. Current World Environment, 11(1), 279-290. https://doi.org/10.12944/cwe.11.1.34
Najimi, S., Bouhaimi, A., Daubeze, M., Zekhnini, A., Pellerin, J., Narbonne, J. F., & Moukrim, A. (1997). Use of acetylcholinesterase in Perna perna and Mytilus galloprovincialis as a biomarker of pollution in Agadir Marine Bay (South of Morocco). Bulletin of Environmental Contamination and Toxicology, 58, 901-908. https://doi.org/10.1007/s001289900419
Narváez, C., Sabat, P., & Sanchez-Hernandez, J. C. (2022). Synergistic effects of pesticides and environmental variables on earthworm standard metabolic rate. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 260. https://doi.org/10.1016/j.cbpc.2022.109404
Park, S. E., Kim, N. D., & Yoo, Y. H. (2004). Acetylcholinesterase plays a pivotal role in apoptosome formation. Cancer Research, 64(8), 2652-2655. https://doi.org/10.1158/0008-5472.can-04-0649
Pelaez-Sanchez, S., Schmidt, O., Frouz, J., Čápová, K. & Courtney, R., (2024). Effects of earthworms on microbial community structure, functionality and soil properties in soil cover treatments for mine tailings rehabilitation. European Journal of Soil Biology, 120, 1-7. https://doi.org/10.1016/j.ejsobi.2024.103603
Rao, J. V., & Kavitha, P. (2004). Toxicity of azodrin on the morphology and acetylcholinesterase activity of the earthworm Eisenia foetida. Environmental Research, 96(3), 323-327. https://doi.org/10.1016/j.envres.2004.02.014
Ribera, D., Narbonne, J. F., Arnaud, C., & Saint-Denis, M. (2001). Biochemical responses of the earthworm Eisenia fetida andrei exposed to contaminated artificial soil, effects of carbaryl. Soil Biology and Biochemistry, 33(7-8), 1123-1130. https://doi.org/10.1016/s0038-0717(01)00035-9
Sanchez-Hernandez, J. C., Del Pino, J. N., Capowiez, Y., Mazzia, C., & Rault, M. (2018). Soil enzyme dynamics in chlorpyrifos-treated soils under the influence of earthworms. Science of the Total Environment, 612, 1407-1416. https://doi.org/10.1016/j.scitotenv.2017.09.043
Singh, K., & Fatima, N. (2022). The efficiency of earthworms as a biomarker for environmental pollution. International Journal of Biological Innovations, 4(1), 104-112. https://doi.org/10.46505/ijbi.2022.4111
Sternfeld, M., Ming, G. L., Song, H. J., Sela, K., Timberg, R., Poo, M. M., & Soreq, H. (1998). Acetylcholinesterase enhances neurite growth and synapse development through alternative contributions of its hydrolytic capacity, core protein, and variable C termini. Journal of Neuroscience, 18(4), 1240-1249. https://doi.org/10.1523/jneurosci.18-04-01240.1998
Basha, P. M., & Latha, V. (2016). Evaluation of sublethal toxicity of zinc and chromium in Eudrilus eugeniae using biochemical and reproductive parameters. Ecotoxicology, 25, 802-813. https://doi.org/10.1007/s10646-016-1637-7
Bednarska, A. J., Choczyński, M., Laskowski, R., & Walczak, M. (2017). Combined effects of chlorpyriphos, copper and temperature on acetylcholinesterase activity and toxicokinetics of the chemicals in the earthworm Eisenia fetida. Environmental Pollution, 220, 567-576. https://doi.org/10.1016/j.envpol.2016.10.004
Bigbee, J. W., & Sharma, K. V. (2004). The adhesive role of acetylcholinesterase (AChE): detection of AChE binding proteins in developing rat spinal cord. Neurochemical Research, 29, 2043-2050. https://doi.org/10.1007/s11064-004-6877-x
Bigbee, J. W., Sharma, K. V., Chan, E. L. P., & Bögler, O. (2000). Evidence for the direct role of acetylcholinesterase in neurite outgrowth in primary dorsal root ganglion neurons. Brain Research, 861(2), 354-362. https://doi.org/10.1016/s0006-8993(00)02046-1
Booth, L. H., & O'Halloran, K. (2001). A comparison of biomarker responses in the earthworm Aporrectodea caliginosa to the organophosphorus insecticides diazinon and chlorpyrifos. Environmental Toxicology and Chemistry: An International Journal, 20(11), 2494-2502. https://doi.org/10.1897/1551-5028(2001)020%3C2494:acobri%3E2.0.co;2
Brown, R. J., Galloway, T. S., Lowe, D., Browne, M. A., Dissanayake, A., Jones, M. B., & Depledge, M. H. (2004). Differential sensitivity of three marine invertebrates to copper assessed using multiple biomarkers. Aquatic Toxicology, 66(3), 267-278. https://doi.org/10.1016/j.aquatox.2003.10.001
Calisi, A., Lionetto, M. G., & Schettino, T. (2011). Biomarker response in the earthworm Lumbricus terrestris exposed to chemical pollutants. Science of the Total Environment, 409(20), 4456-4464.https://doi.org/10.1016/j.scitotenv.2011.06.058
Calisi, A., Lionetto, M.G., & Schettino, T. (2009). Pollutant-induced alterations of granulocyte morphology in the earthworm Eisenia foetida. Ecotoxicology and Environmental Safety. 72(5), 1369-1377. https://doi.org/10.1016/j.ecoenv.2009.03.010
Caselli, F., Gastaldi, L., Gambi, N., & Fabbri, E. (2006). In vitro characterization of cholinesterases in the earthworm Eisenia andrei. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 143(4), 416-421. https://doi.org/10.1016/j.cbpc.2006.04.003
Diamantino, T. C., Almeida, E., Soares, A. M. V. M., & Guilhermino, L. (2003). Characterization of cholinesterases from Daphnia magna straus and their inhibition by zinc. Bulletin of Environmental Contamination & Toxicology, 71(2), 0219–0225. https://doi.org/10.1007/s00128-003-0153-7
Ducros V. (1992). Chromium Metabolism. Biological Trace Element Research, 32(1-3), 65-77. https://doi.org/10.1007/bf02784589
Dzul-Caamal, R., Vega-López, A., & Osten, J. R. V. (2024). Integrated evaluation of the biological response of the earthworm Eisenia fetida using two glyphosate exposure strategies: soil enriched and soils collected from crops in Southeastern Mexico. Environmental Science and Pollution Research, 1-16. Available at: https://ui.adsabs.harvard.edu/abs/2024ESPR...3132152D/abstract
Ellman, G. L., Courtney, K. D., Andres Jr, V., & Featherstone, R. M. (1961). A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology, 7(2), 88-95. https://doi.org/10.1016/0006-2952(61)90145-9
Grisaru, D., Pick, M., Perry, C., Sklan, E. H., Almog, R., Goldberg, I., ... & Deutsch, V. (2006). Hydrolytic and nonenzymatic functions of acetylcholinesterase comodulate hemopoietic stress responses. The Journal of Immunology, 176(1), 27-35. https://doi.org/10.4049/jimmunol.176.1.27
Gudeta, K., Kumar, V., Bhagat, A., Julka, J. M., Bhat, S. A., Ameen, F., & Amarowicz, R. (2023). Ecological adaptation of earthworms for coping with plant polyphenols, heavy metals, and microplastics in the soil: A review. Heliyon, 9(3). https://doi.org/10.1016/j.heliyon.2023.e14572
Hagger, J. A., Jones, M. B., Leonard, D. P., Owen, R., & Galloway, T. S. (2006). Biomarkers and integrated environmental risk assessment: are there more questions than answers? Integrated Environmental Assessment and Management: an International Journal, 2(4), 312-329. https://doi.org/10.1002/ieam.5630020403
Kammenga, J. E., Dallinger, R., Donker, M. H., Köhler, H. R., Simonsen, V., Triebskorn, R., & Weeks, J. M. (2000). Biomarkers in terrestrial invertebrates for ecotoxicological soil risk assessment. Reviews of Environmental Contamination and Toxicology, 164, 93-147.
Latha, V., & Basha, P. M. (2016). Extent of heavy metal accumulation in sewage irrigated soils and their impact on distribution of earthworm communities: linking Chromium and Zinc toxicity on growth and reproduction in selected earthworm species. Current World Environment, 11(1), 279-290. https://doi.org/10.12944/cwe.11.1.34
Najimi, S., Bouhaimi, A., Daubeze, M., Zekhnini, A., Pellerin, J., Narbonne, J. F., & Moukrim, A. (1997). Use of acetylcholinesterase in Perna perna and Mytilus galloprovincialis as a biomarker of pollution in Agadir Marine Bay (South of Morocco). Bulletin of Environmental Contamination and Toxicology, 58, 901-908. https://doi.org/10.1007/s001289900419
Narváez, C., Sabat, P., & Sanchez-Hernandez, J. C. (2022). Synergistic effects of pesticides and environmental variables on earthworm standard metabolic rate. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 260. https://doi.org/10.1016/j.cbpc.2022.109404
Park, S. E., Kim, N. D., & Yoo, Y. H. (2004). Acetylcholinesterase plays a pivotal role in apoptosome formation. Cancer Research, 64(8), 2652-2655. https://doi.org/10.1158/0008-5472.can-04-0649
Pelaez-Sanchez, S., Schmidt, O., Frouz, J., Čápová, K. & Courtney, R., (2024). Effects of earthworms on microbial community structure, functionality and soil properties in soil cover treatments for mine tailings rehabilitation. European Journal of Soil Biology, 120, 1-7. https://doi.org/10.1016/j.ejsobi.2024.103603
Rao, J. V., & Kavitha, P. (2004). Toxicity of azodrin on the morphology and acetylcholinesterase activity of the earthworm Eisenia foetida. Environmental Research, 96(3), 323-327. https://doi.org/10.1016/j.envres.2004.02.014
Ribera, D., Narbonne, J. F., Arnaud, C., & Saint-Denis, M. (2001). Biochemical responses of the earthworm Eisenia fetida andrei exposed to contaminated artificial soil, effects of carbaryl. Soil Biology and Biochemistry, 33(7-8), 1123-1130. https://doi.org/10.1016/s0038-0717(01)00035-9
Sanchez-Hernandez, J. C., Del Pino, J. N., Capowiez, Y., Mazzia, C., & Rault, M. (2018). Soil enzyme dynamics in chlorpyrifos-treated soils under the influence of earthworms. Science of the Total Environment, 612, 1407-1416. https://doi.org/10.1016/j.scitotenv.2017.09.043
Singh, K., & Fatima, N. (2022). The efficiency of earthworms as a biomarker for environmental pollution. International Journal of Biological Innovations, 4(1), 104-112. https://doi.org/10.46505/ijbi.2022.4111
Sternfeld, M., Ming, G. L., Song, H. J., Sela, K., Timberg, R., Poo, M. M., & Soreq, H. (1998). Acetylcholinesterase enhances neurite growth and synapse development through alternative contributions of its hydrolytic capacity, core protein, and variable C termini. Journal of Neuroscience, 18(4), 1240-1249. https://doi.org/10.1523/jneurosci.18-04-01240.1998
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V, L., & P., M. (2025). Heavy Metal Pollution and Temperature Stress Induced Changes in Acetyl Choline Esterase Activity in Two Ecologically Different Earthworm Species. International Journal of Advancement in Life Sciences Research, 8(1), 100-107. https://doi.org/https://doi.org/10.31632/ijalsr.2025.v08i01.009
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