Low-density polyethylene microplastics partially alleviate the ecotoxicological effects induced by cadmium exposure on the earthworm Eisenia fetida

Highlights

● LDPE had no effect on the mortality, growth, and reproduction of earthworms.

● LDPE did not alter the mortality, growth, and reproduction of earthworm caused by Cd.

● LDPE alleviated histopathological damage to earthworms caused by Cd.

● LDPE alleviated DNA damage in earthworm coelomocytes caused by Cd.

● LDPE did not affect the accumulation of Cd in earthworms.

Abstract

Cadmium (Cd) can accumulate in the food chain, with serious impacts on human health and safety. Microplastics (MPs) such as low-density polyethylene (LDPE) should be considered not only as a single pollutant but also as a carrier of other pollutants. In this study, we investigated the joint effects of 30% LDPE and 313 mg kg⁻¹ Cd on mortality, growth, reproduction, microstructure, DNA damage, oxidative stress, and mRNA levels in the earthworm Eisenia fetida. We found that 313 mg kg⁻¹ Cd inhibited growth and reproduction and damaged the microstructures of the skin and intestine. Meanwhile, LDPE had no effect on the mortality, growth, or cocoon production of earthworms. Moreover, it did not increase the mortality, growth, or inhibition of cocoon production caused by Cd and instead alleviated the DNA damage in coelomocytes caused by Cd treatment. Finally, it did not alter the accumulation of Cd in the worms. These indicators can be used for toxicity safety assessment and soil ecological risk assessment of LDPE and Cd cooccurrence in soil.

Graphical abstract

Keywords

microplastics / Eisenia fetida / DNA damage / histopathological damage / heavy metals

References

[1] Alimba, C.G., Faggio, C., 2019. Microplastics in the marine environment: Current trends in environmental pollution and mechanisms of toxicological profile. Environmental Toxicology and Pharmacology68, 61–74.

[2] Bradford, M.M., 1976. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Analytical Biochemistry72, 248–254.

[3] Cao, J., Wang, Q., Lei, Y., Jiang, X., Li, M., 2022. Accumulation of microplastics and Tcep pollutants in agricultural soil: Exploring the links between metabolites and gut microbiota in earthworm homeostasis. Environment International170, 107590.

[4] Chia, R.W., Lee, J.Y., Kim, H., Jang, J., 2021. Microplastic pollution in soil and groundwater: a review. Environmental Chemistry Letters19, 4211–4224.

[5] Dedeke, G.A., Owagboriaye, F.O., Adebambo, A.O., Ademolu, K.O., 2016. Earthworm metallothionein production as biomarker of heavy metal pollution in abattoir soil. Applied Soil Ecology104, 42–47.

[6] Diepens, N.J., Koelmans, A.A., 2018. Accumulation of plastic debris and associated contaminants in aquatic food webs. Environmental Science & Technology52, 8510–8520.

[7] Du, Y., Shang, G., Zhai, J., Wang, X., 2023. Effects of soybean oil exposure on the survival, reproduction, biochemical responses, and gut microbiome of the earthworm Eisenia fetida. Journal of Environmental Sciences (China)133, 23–36.

[8] Farrell, P., Nelson, K., 2013. Trophic level transfer of microplastic: Mytilus edulis (L.) to Carcinus maenas (L.). Environmental Pollution177, 1–3.

[9] Fleury, J.B., Baulin, V.A., 2021. Microplastics destabilize lipid membranes by mechanical stretching. Proceedings of the National Academy of Sciences of the United States of America118, 118.

[10] Gajski, G., Žegura, B., Ladeira, C., Pourrut, B., Del Bo’, C., Novak, M., Sramkova, M., Milić, M., Gutzkow, K.B., Costa, S., Dusinska, M., Brunborg, G., Collins, A., 2019. The comet assay in animal models: From bugs to whales - (Part 1 Invertebrates). Mutation Research/Reviews in Mutation Research779, 82–113.

[11] Goswami, L., Pratihar, S., Dasgupta, S., Bhattacharyya, P., Mudoi, P., Bora, J., Bhattacharya, S.S., Kim, K.H., 2016. Exploring metal detoxification and accumulation potential during vermicomposting of Tea factory coal ash: sequential extraction and fluorescence probe analysis. Scientific Reports6, 30402.

[12] Gu, X., Liu, Z., Wang, X., Luo, J., Zhang, H., Davison, W., Ma, L.Q., Xue, Y., 2017. Coupling biological assays with diffusive gradients in thin-films technique to study the biological responses of Eisenia fetida to cadmium in soil. Journal of Hazardous Materials339, 340–346.

[13] Hodson, M.E., Duffus-Hodson, C.A., Clark, A., Prendergast-Miller, M.T., Thorpe, K.L., 2017. Plastic bag derived-microplastics as a vector for metal exposure in terrestrial invertebrates. Environmental Science & Technology51, 4714–4721.

[14] Holmes, L.A., Turner, A., Thompson, R.C., 2014. Interactions between trace metals and plastic production pellets under estuarine conditions. Marine Chemistry167, 25–32.

[15] Huang, C., Ge, Y., Yue, S., Zhao, L., Qiao, Y., 2021. Microplastics aggravate the joint toxicity to earthworm Eisenia fetida with cadmium by altering its availability. Science of the Total Environment753, 142042.

[16] Huerta Lwanga, E., Gertsen, H., Gooren, H., Peters, P., Salánki, T., van der Ploeg, M., Besseling, E., Koelmans, A.A., Geissen, V., 2016. Microplastics in the terrestrial ecosystem: Implications for Lumbricus terrestris (Oligochaeta, Lumbricidae). Environmental Science & Technology50, 2685–2691.

[17] Huerta Lwanga, E., Thapa, B., Yang, X., Gertsen, H., Salánki, T., Geissen, V., Garbeva, P., 2018. Decay of low-density polyethylene by bacteria extracted from earthworm’s guts: A potential for soil restoration. Science of the Total Environment624, 753–757.

[18] Ivar do Sul, J.A., Costa, M.F., 2014. The present and future of microplastic pollution in the marine environment. Environmental Pollution185, 352–364.

[19] Jiang, X., Chang, Y., Zhang, T., Qiao, Y., Klobučar, G., Li, M., 2020. Toxicological effects of polystyrene microplastics on earthworm (Eisenia fetida). Environmental Pollution259, 113896.

[20] Jiang, X., Yang, Y., Wang, Q., Liu, N., Li, M., 2022. Seasonal variations and feedback from microplastics and cadmium on soil organisms in agricultural fields. Environment International161, 107096.

[21] Kirkham, M.B., 2006. Cadmium in plants on polluted soils: Effects of soil factors, hyperaccumulation, and amendments. Geoderma137, 19–32.

[22] Koelmans, A.A., Besseling, E., Wegner, A., Foekema, E.M., 2013. Plastic as a carrier of POPs to aquatic organisms: A model analysis. Environmental Science & Technology47, 8992–8993.

[23] Li, X., Wang, M., Jiang, R., Zheng, L., Chen, W., 2020a. Evaluation of joint toxicity of heavy metals and herbicide mixtures in soils to earthworms (Eisenia fetida). Journal of Environmental Sciences (China)94, 137–146.

[24] Li, Y., Wang, X., Sun, Z., 2020b. Ecotoxicological effects of petroleum-contaminated soil on the earthworm Eisenia fetida. Journal of Hazardous Materials393, 122384.

[25] 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 Environment836, 155747.

[26] Liu, J., Qin, J., Zhu, L., Zhu, K., Liu, Z., Jia, H., Lichtfouse, E., 2022. The protective layer formed by soil particles on plastics decreases the toxicity of polystyrene microplastics to earthworms (Eisenia fetida). Environment International162, 107158.

[27] Liu, P., Lu, K., Li, J., Wu, X., Qian, L., Wang, M., Gao, S., 2020. Effect of aging on adsorption behavior of polystyrene microplastics for pharmaceuticals: Adsorption mechanism and role of aging intermediates. Journal of Hazardous Materials384, 121193.

[28] Lourenco, J., Silva, A., Carvalho, F., Oliveira, J., Malta, M., Mendo, S., Gonçalves, F., Pereira, R., 2011. Histopathological changes in the earthworm Eisenia andrei associated with the exposure to metals and radionuclides. Chemosphere85, 1630–1634.

[29] Meharg, A.A., Norton, G., Deacon, C., Williams, P., Adomako, E.E., Price, A., Zhu, Y., Li, G., Zhao, F.J., McGrath, S., Villada, A., Sommella, A., De Silva, P.M.C.S., Brammer, H., Dasgupta, T., Islam, M.R., 2013. Variation in rice cadmium related to human exposure. Environmental Science & Technology47, 5613–5618.

[30] OECD, 2004. Guideline for Testing of Chemicals No. 222, Earthworm Reproduction Test (Eisenia fetida/Eisenia andrei). OECD, Paris, France

[31] Phillips, H.R.P., Guerra, C.A., Bartz, M.L.C., Briones, M.J.I., Brown, G., Crowther, T.W., Ferlian, O., Gongalsky, K.B., van den Hoogen, J., Krebs, J., Orgiazzi, A., Routh, D., Schwarz, B., Bach, E.M., Bennett, J.M., Brose, U., Decaëns, T., König-Ries, B., Loreau, M., Mathieu, J., Mulder, C., van der Putten, W.H., Ramirez, K.S., Rillig, M.C., Russell, D., Rutgers, M., Thakur, M.P., de Vries, F.T., Wall, D.H., Wardle, D.A., Arai, M., Ayuke, F.O., Baker, G.H., Beauséjour, R., Bedano, J.C., Birkhofer, K., Blanchart, E., Blossey, B., Bolger, T., Bradley, R.L., Callaham, M.A., Capowiez, Y., Caulfield, M.E., Choi, A., Crotty, F.V., Crumsey, J.M., Dávalos, A., Diaz Cosin, D.J., Dominguez, A., Duhour, A.E., van Eekeren, N., Emmerling, C., Falco, L.B., Fernández, R., Fonte, S.J., Fragoso, C., Franco, A.L.C., Fugère, M., Fusilero, A.T., Gholami, S., Gundale, M.J., López, M.G., Hackenberger, D.K., Hernández, L.M., Hishi, T., Holdsworth, A.R., Holmstrup, M., Hopfensperger, K.N., Lwanga, E.H., Huhta, V., Hurisso, T.T., Iannone, B.V. III, Iordache, M., Joschko, M., Kaneko, N., Kanianska, R., Keith, A.M., Kelly, C.A., Kernecker, M.L., Klaminder, J., Koné, A.W., Kooch, Y., Kukkonen, S.T., Lalthanzara, H., Lammel, D.R., Lebedev, I.M., Li, Y., Jesus Lidon, J.B., Lincoln, N.K., Loss, S.R., Marichal, R., Matula, R., Moos, J.H., Moreno, G., Morón-Ríos, A., Muys, B., Neirynck, J., Norgrove, L., Novo, M., Nuutinen, V., Nuzzo, V., Pansu, J., Paudel, S., Pérès, G., Pérez-Camacho, L., Piñeiro, R., Ponge, J.F., Rashid, M.I., Rebollo, S., Rodeiro-Iglesias, J., Rodríguez, M.Á., Roth, A.M., Rousseau, G.X., Rozen, A., Sayad, E., van Schaik, L., Scharenbroch, B.C., Schirrmann, M., Schmidt, O., Schröder, B., Seeber, J., Shashkov, M.P., Singh, J., Smith, S.M., Steinwandter, M., Talavera, J.A., Trigo, D., Tsukamoto, J., de Valença, A.W., Vanek, S.J., Virto, I., Wackett, A.A., Warren, M.W., Wehr, N.H., Whalen, J.K., Wironen, M.B., Wolters, V., Zenkova, I.V., Zhang, W., Cameron, E.K., Eisenhauer, N., 2019. Global distribution of earthworm diversity. Science366, 480–485.

[32] Piola, L., Fuchs, J., Oneto, M.L., Basack, S., Kesten, E., Casabé, N., 2013. Comparative toxicity of two glyphosate-based formulations to Eisenia andrei under laboratory conditions. Chemosphere91, 545–551.

[33] Rinklebe, J., Antoniadis, V., Shaheen, S.M., Rosche, O., Altermann, M., 2019. Health risk assessment of potentially toxic elements in soils along the Central Elbe River, Germany. Environment International126, 76–88.

[34] Rodriguez-Seijo, A., Lourenço, J., Rocha-Santos, T.A.P., da Costa, J., Duarte, A.C., Vala, H., Pereira, R., 2017. Histopathological and molecular effects of microplastics in Eisenia andrei Bouche. Environmental Pollution220, 495–503.

[35] Santadino, M., Coviella, C., Momo, F., 2014. Glyphosate sublethal effects on the population dynamics of the earthworm Eisenia fetida (Savigny, 1826). Water, Air, and Soil Pollution225, 2207.

[36] Satarug, S., Garrett, S.H., Sens, M.A., Sens, D.A., 2010. Cadmium, environmental exposure, and health outcomes. Environmental Health Perspectives118, 182–190.

[37] Sheng, Y.F., Liu, Y., Wang, K., Cizdziel, J.V., Wu, Y., Zhou, Y., 2021. Ecotoxicological effects of micronized car tire wear particles and their heavy metals on the earthworm (Eisenia fetida) in soil. Science of the Total Environment793, 793.

[38] Shi, Z., Zhang, F., Wang, C., 2018. Adsorption of phenanthrene by earthworms — A pathway for understanding the fate of hydrophobic organic contaminants in soil-earthworm systems. Journal of Environmental Management212, 115–120.

[39] Song, X., Liu, M., Wu, D., Qi, L., Ye, C., Jiao, J., Hu, F., 2014. Heavy metal and nutrient changes during vermicomposting animal manure spiked with mushroom residues. Waste Management (New York, N.Y.)34, 1977–1983.

[40] 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 & Biochemistry41, 905–909.

[41] Stuerzenbaum, S.R., Höckner, M., Panneerselvam, A., Levitt, J., Bouillard, J-S., Taniguchi, S., Dailey, L-A., Ahmad Khanbeigi, R., Rosca, E.V., Thanou, M., Suhling, K., Zayats, A.V., Green, M., 2013. Biosynthesis of luminescent quantum dots in an earthworm. Nature Nanotechnology8, 57–60.

[42] Sun, Y., Li, H., Guo, G., Semple, K.T., Jones, K.C., 2019. Soil contamination in China: Current priorities, defining background levels and standards for heavy metals. Journal of Environmental Management251, 109512.

[43] Tian, L., Jinjin, C., Ji, R., Ma, Y., Yu, X., 2022. Microplastics in agricultural soils: sources, effects, and their fate. Current Opinion in Environmental Science & Health25, 100311.

[44] Wang, C., Rong, H., Liu, H., Wang, X., Gao, Y., Deng, R., Liu, R., Liu, Y., Zhang, D., 2018a. Detoxification mechanisms, defense responses, and toxicity threshold in the earthworm Eisenia foetida exposed to ciprofloxacin-polluted soils. Science of the Total Environment612, 442–449.

[45] Wang, G., Xia, X., Yang, J., Tariq, M., Zhao, J., Zhang, M., Huang, K., Lin, K., Zhang, W., 2020. Exploring the bioavailability of nickel in a soil system: Physiological and histopathological toxicity study to the earthworms (Eisenia fetida). Journal of Hazardous Materials383, 121169.

[46] Wang, J., Coffin, S., Sun, C., Schlenk, D., Gan, J., 2019a. Negligible effects of microplastics on animal fitness and HOC bioaccumulation in earthworm Eisenia fetida in soil. Environmental Pollution249, 776–784.

[47] Wang, J., Wang, J., Wang, G., Zhu, L., Wang, J., 2016. DNA damage and oxidative stress induced by imidacloprid exposure in the earthworm Eisenia fetida. Chemosphere144, 510–517.

[48] Wang, K., Qiao, Y., Zhang, H., Yue, S., Li, H., Ji, X., Liu, L., 2018b. Bioaccumulation of heavy metals in earthworms from field contaminated soil in a subtropical area of China. Ecotoxicology and Environmental Safety148, 876–883.

[49] Wang, X., Chang, L., Sun, Z., Zhang, Y., Yao, L., 2010. Analysis of earthworm Eisenia fetida proteomes during cadmium exposure: An ecotoxicoproteomics approach. Proteomics10, 4476–4490.

[50] Wang, X., Zhu, X., Peng, Q., Wang, Y., Ge, J., Yang, G., Wang, X., Cai, L., Shen, W., 2019b. Multi-level ecotoxicological effects of imidacloprid on earthworm (Eisenia fetida). Chemosphere219, 923–932.

[51] Wang, Y., Li, Y., Geng, H., Zuo, Q., Thunders, M., Qiu, J., 2022. Effect of arsenite on the proteome of earthworms Eisenia fetida. Soil Ecology Letters5, 181–194.

[52] Wang, Z.D., Zhang, L., Wang, X., 2023. Molecular toxicity and defense mechanisms induced by silver nanoparticles in Drosophila melanogaster. Journal of Environmental Sciences (China)125, 616–629.

[53] 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 Safety81, 122–126.

[54] Yan, X., Wang, J., Zhu, L., Wang, J., Li, S., Kim, Y.M., 2021. Oxidative stress, growth inhibition, and DNA damage in earthworms induced by the combined pollution of typical neonicotinoid insecticides and heavy metals. Science of the Total Environment754, 141873.

[55] Yang, X., Li, Y., Wang, X., 2020. Effects of ciprofloxacin exposure on the earthworm Eisenia fetida. Environmental Pollution262, 114287.

[56] Yang, X., Shang, G., Wang, X., 2022. Biochemical, transcriptomic, gut microbiome responses and defense mechanisms of the earthworm Eisenia fetida to salt stress. Ecotoxicology and Environmental Safety239, 113684.

[57] Zhang, H., Yuan, X., Xiong, T., Wang, H., Jiang, L., 2020. Bioremediation of co-contaminated soil with heavy metals and pesticides: Influence factors, mechanisms and evaluation methods. Chemical Engineering Journal398, 125657.

[58] Zhao, S., He, L., Lu, Y., Duo, L., 2017. The impact of modified nano-carbon black on the earthworm Eisenia fetida under turfgrass growing conditions: Assessment of survival, biomass, and antioxidant enzymatic activities. Journal of Hazardous Materials338, 218–223.

[59] Zhou, Y., Liu, X., Wang, J., 2020. Ecotoxicological effects of microplastics and cadmium on the earthworm Eisenia foetida. Journal of Hazardous Materials392, 122273.

[60] Zhu, M.L.J.F.Y.S.B., 2023. Microplastics effects on soil biota are dependent on their properties: A meta-analysis. Soil Biology & Biochemistry178, 108940.

Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 31172091), the National Key Research and Development Program of China (No. 2018YFC0507204) and The 2115 Talent Development Program of China Agricultural University.

Author contributions

Song Zhang: Investigation, Formal analysis, Data curation, Methodology, Software, Validation, Writing-original draft. Yating Du: Data curation, Methodology, Validation, Software, Writing-original draft. Guangshen Shang: Data curation, Methodology, Validation, Writing-original draft. Kejiao Hu: Writing-original draft. Xing Wang: Project administration, Funding acquisition, Supervision, Conceptualization, Writing-review and editing.

Conflict of interest

The authors declare no competing of interest.

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