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| Metabolic toxicity of polyethylene microplastics with different sizes to earthworms Eisenia fetida |
| YANG Xiao-xia, ZHANG Xue-mei, SHU Xiao, XIE Man-li, MENG Xia, ZHANG Wei, YANG Jun-ying, GONG Jiu-ping, LI Bi-quan |
| Institute of Agricultural Quality Standard and Testing Technology, Chongqing Academy of Agricultural Sciences, Chongqing 401329, China |
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Abstract By using Eisenia fetida as the test object, the growth and reproduction, cytochrome P450 (CYP) sub-enzymes activity, and small molecule metabolites were measured to investigate the metabolic toxicity of polyethylene microplastics with different particle sizes (small, 30~50μm; large, 125μm) at different concentrations (0.5, 2.5, 10, 20g/kg). The results showed that small particles of polyethylene were more likely to retain and accumulate in earthworms, and their harm to earthworms were greater. And large particle polyethylene microplastics could inhibit the reproduction of earthworms to some extent. The top twelve most important metabolites identified by metabolomics responded differently under the stress of different sizes of polyethylene, and the particle size of polyethylene had a significant effect on the toxic effect. The stress of small-size polyethylene with low concentrations (0.5, 2.5g/kg) had no significant effect on the CYP2B6 and CYP3A4 activities and the concentrations of important metabolites in earthworms; under the stress of small-size polyethylene with high concentrations (10, 20g/kg), the levels in seven important metabolites (L-formylkynurenine, androstanedione, androstenedione, docosapentaenoic acid, (5Z, 8Z, 14Z) -11, 12-dihydroxyicosa-5, 8, 14-dienoic acid (11, 12-DHET), inositol, and all-trans-retinoic acid) significantly increased by 20.5% to 70.2% compared to the control. Small-size polyethylene could cause the inflammation and neuro-metabolic disorders in earthworms, and damage their osmotic regulation metabolism. The significant induction of CYP2B6 and CY2C9 activity revealed that earthworms had certain detoxification functions. Under the stress of large-size polyethylene with the concentration of 0.5~20g/kg, no significant change in the activities of CYP2B6 and CYP3A4 in earthworms in comparison to the control was observed. However, the levels in majority of important metabolites, including L-formylkynurenine, androstanedione, androstenedione, adenosine 3'-phosphate, inosine, and xanthine, were all significantly lower than the control by 20.0% to 77.3%, which suppressed the hormone production of the earthworms, thus affecting their reproduction and metabolism.
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Received: 05 July 2023
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[1] 陈钦威,王 鹏,丁明军,等.中国地表水环境微塑料赋存特征及驱动因素 [J]. 中国环境科学, 2024,44(8):4599-4609.Chen Q W, Wang P, Ding M J, et al. Characteristics and driving factors of microplastics in surface water environment of China [J]. China Environmental Science, 2024,44(8):4599-4609.
[2] Dong X, Liu X, Hou Q, et al. From natural environment to animal tissues: A review of microplastics (nanoplastics) translocation and hazards studies [J] . Science of the Total Environment, 2023,855:158686.
[3] Mueller N C, Nowack B. Exposure modeling of engineered nanoparticles in the environment [J] . Environmental Science and Technology, 2008,42:4447-4453.
[4] Bueks F, Kaupenjohann M. Global concentrations of microplastics in soils-a review [J]. Soil, 2020,6:649-662.
[5] Yin L Y, Chen B J, Xia B, et al. Polystyrene microplastics alter the behavior, energy reserve and nutritional composition of marine jacopever (Sebastes schlegelii) [J]. Journal of Hazardous Materials, 2018,360:97-105.
[6] Lu K, Qiao R X, An H, et al. Influence of microplastics on the accumulation and chronic toxic effects of cadmium in zebrafish Danio rerio [J]. Chemosphere, 2018,202:514-520.
[7] Huang W, Wang X H, Chen D Y, et al. Toxicity mechanisms of polystyrene microplastics in marine mussels revealed by high-coverage quantitative metabolomics using chemical isotope labeling liquid chromatography mass spectrometry [J]. Journal of Hazardous Materials, 2021,417:126003.
[8] 侯晨丽,于 越,于玲红,等.微塑料与双酚A联合下鲤鱼生物积累及氧化应激效应 [J]. 中国环境科学, 2023,43(8):4334-4342.Hou C L, Yu Y, Yu L H, et al. Interactive effects of polystyrene microplastics and bisphenol A on bioaccumulation and oxidative stress in the Yellow River carp (Cyprinus carpio haematopterus) [J]. China Environmental Science, 2023,43(8):4334-4342.
[9] Lwanga E H, Gertsen H, Gooren H, et al. Microplastics in the terrestrial ecosystem: Implications for Lumbricus terrestris (Oligochaeta, Lumbricidae) [J]. Environmental Science and Technology, 2016,50:2685-2691.
[10] Hoseini M, Bond T. Predicting the global environmental distribution of plastic polymers [J]. Environmental Pollution, 2022,300:118966.
[11] Li B, Song W H, Cheng Y L, et al. Ecotoxicological effects of different size ranges of industrial-grade polyethylene and polypropylene microplastics on earthworms Eisenia fetida [J]. Science of the Total Environment, 2021,783:147007.
[12] Hodson M E, Duffus-Hodson C A, Clark A, et al. Plastic bag berived-microplastics as a vector for metal exposure in terrestrial invertebrates [J]. Environmental Science and Technology, 2017,51: 4714-4721.
[13] Zhang L, Sintim H Y, Bary A I, et al. Interaction of Lumbricus terrestris with macroscopic polyethylene and biodegradable plastic mulch [J] . Science of the Total Environment, 2018,635:1600-1608.
[14] Rodriguez-Seijo A, Lourenco J, Rocha-Santos TAP, et al. Histopathological and molecular effects of microplastics in Eisenia andrei Bouche [J] . Environmental Pollution, 2017,220:495-503.
[15] Wang J, Coffin S, Sun CL, et al. Negligible effects of microplastics on animal fitness and HOC bioaccumulation in earthworm Eisenia fetida in soil [J] . Environmental Pollution, 2019,249:776-784.
[16] Xu G H, Yang Y, Yu Y. Size effects of polystyrene microplastics on the accumulation and toxicity of (semi-)metals in earthworms [J] . Environmental Pollution, 2021,291:118194.
[17] Li M, Ruan L Y, Dang F, et al. Metabolic response of earthworms (Pheretima guillemi) to silver nanoparticles in sludge-amended soil [J] . Environment Pollution, 2022,300:118594.
[18] Yang X, Zhang X, Shu X, et al. The effects of polyethylene microplastics on the growth, reproduction, metabolic enzymes, and metabolomics of earthworms Eisenia fetida [J] . Ecotoxicology and Environmental Safety, 2023,263:115390.
[19] Boots B, Russell C W, Green DS. Effects of microplastics in soil ecosystems: Above and below ground [J] . Environmental Science and Technology, 2019,53:11496-11506.
[20] Van den Berg P, Huerta-Lwanga E, Corradini F, et al. Sewage sludge application as a vehicle for microplastics in eastern Spanish agricultural soils [J] . Environmental Pollution, 2020,261:114198.
[21] Machado A A, Lau C W, Till J, et al. Impacts of microplastics on the soil biophysical environment [J] . Environmental Science and Technology, 2018,52:9656-9665.
[22] Teng J, Zhao J M, Zhu X P, et al. Toxic effects of exposure to microplastics with environmentally relevant shapes and concentrations: Accumulation, energy metabolism and tissue damage in oyster Crassostrea gigas [J] . Environmental Pollution, 2021,269:116169.
[23] 杨晓霞,龚久平,张雪梅,等.亚致死剂量乙草胺对蚯蚓的毒性效应及敏感生物标记物 [J] . 应用生态学报, 2021,32(9):3327-3334.Yang X X, Gong J P, Zhang X M, et al. Toxic effects of sublethal acetochlor with sublethal doses on earthworms in soil using multiendpoints system [J]. Chinese Journal of Applied Ecology, 2021, 32(9):3327-3334.
[24] 杨晓霞,张雪梅,张 伟,等.蚯蚓细胞色素P450亚酶及代谢组学对土壤亚致死剂量草甘膦除草剂的响应 [J]. 环境科学学报, 2021, 41(3):1091-1100.Yang X X, Zhang X M, Zhang W, et al. Responses of cytochrome P450 subenzymes and metabolomics in earthworms exposed to sublethal of glyphosate-based herbicide in soil [J]. Acta Scientiae Circumstantiae, 41(3):1091-1100.
[25] Yang X, Zhang X, Shu X, et al. Effects of multi-walled carbon nanotubes in soil on earthworm growth and reproduction, enzymatic activities, and metabolomics [J]. Ecotoxicology and Environmental Safety, 2022,246:114158.
[26] Rendic S, Guengerich F P. Survey of human oxidoreductases and cytochrome P450enzymes involved in the metabolism of xenobiotic and natural chemicals [J]. Chemical Research in Toxicology, 2015, 28:38-42.
[27] Bradford M M. A rapid and sensitive method for the quantitation of microgram quantities of protein Utilizing the principle of protein-pye binding [J]. Analytical Chemistry, 1976,72:248-254.
[28] Lu S B, Qiu R, Hu J N, et al. Prevalence of microplastics in animal-based traditional medicinal materials: Widespread pollution in terrestrial environments [J]. Science of the Total Environment, 2020, 709:136214.
[29] Lahive E, Cross R, Saarloos A I, et al. Earthworms ingest microplastic fibres and nanoplastics with effects on egestion rate and long-term retention [J]. Science of the Total Environment, 2022,807:1151022.
[30] Jager T, Fleuren R, Roelofs W, et al. Feeding activity of the earthworm Eisenia andrei in artificial soil [J]. Soil Biology and Biochemistry, 2003,35:313-322.
[31] Besseling E, Wegner A, Foekema E M, et al. Effects of microplastic on fitness and PCB bioaccumulation by the Lugworm Arenicola marina (L.) [J]. Environmental Science and Technology, 2013,47:593-600.
[32] Khalid W, Gill P, Arshad MS, et al. Functional behavior of DHA and EPA in the formation of babies brain at different stages of age, and protect from different brain-related diseases [J]. International Journal of Food Properties, 2022,25:1021-1044.
[33] Pousinis P. Evaluation of rodent models of osteoarthritis using lipidomic profiling and behavioral studies. Ph.D. dissertation [D]. Nottingham: The University of Nottingham (United Kingdom), 2017.
[34] Zhang J, Zhang M, Zhang W, et al. Total flavonoids of Inula japonica alleviated the inflammatory response and oxidative stress in LPS-induced acute lung injury via inhibiting the sEH activity: Insights from lipid metabolomics [J]. Phytomedicine, 2022,107:154380.
[35] Hessel S, Lampen A. All-trans retinoic acid enhances the transport of phase II metabolites of benzo [a] pyrene by inducing the Breast Cancer Resistance Protein expression in Caco-2cells [J]. Toxicology Letters, 2010,197:151-155.
[36] Lampen A, Meyer S, Nau H. Effects of receptor-selective retinoids on CYP26gene expression and metabolism of all-trans-retinoic acid in intestinal cells [J]. Drug Metabolism and Disposition, 2001,29:742-747.
[37] Wood PL, Smith T, Pelzer L, et al. Targeted metabolomic analyses of cellular models of pelizaeus-merzbacher disease reveal plasmalogen and myo-inositol solute carrier dysfunction [J]. Lipids in Health and Disease, 2011,10:102.
[38] Tang R G, Ying M S, Luo YM, et al. Microplastic pollution destabilized the osmoregulatory metabolism but did not affect intestinal microbial biodiversity of earthworms in soil [J]. Environmental Pollution, 2023,320:1121020.
[39] Gonsioroski A, Meling D D, Gao L, et al. Iodoacetic acid affects estrous cyclicity, ovarian gene expression, and hormone levels in mice [J]. Biology of Reproduction, 2021,105:1030-1042.
[40] Gray P B, Straftis A A, Bird B M, et al. Human reproductive behavior, life history, and the challenge hypothesis: A 30-year review, retrospective and future directions [J]. Hormones and Behavior, 2020, 123:104530. |
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