Abstract
The co-occurrence of heavy metals and microplastics (MPs) is an emerging issue that has attracted considerable attention. However, the interaction of nickel oxide nanoparticle (nano-NiO) combined with MPs in soil was poorly researched. Here, experiments were conducted to study the influence of nano-NiO (200 mg/kg) and polyethylene (PE) MPs with different concentrations (0.1, 1, and 10%) and sizes (13, 50, and 500 µm) on earthworms for 28 days. Compared to control, the damage was induced by PE and nano-NiO, which was evaluated by biomarker Integrated Biomarker Response index: version 2 (IBRv2) based on six biomarkers including SOD, POD, CAT, MDA, AChE, Na+/K+-ATPase and cellulase. The majority of the chosen biomarkers showed significant but complicated responses with increasing contaminant concentrations after 28 days of exposure. Moreover, the joint effect was assessed as antagonism by the effect addition index (EAI). Overall, this work expands our understanding of the combined toxicity of PE and nano-NiO in soil ecosystems.
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The data that support the findings of this study are available from the corresponding author (Zaifu Yang) upon reasonable request.
References
Adeel M, Ma CX, Ullah S, Rizwan M, Hao Y, Chen CY, Jilani G, Shakoor N, Li MS, Wang LH, Tsang DCW, Rinklebe J, Rui YK, Xing BS (2019) Exposure to nickel oxide nanoparticles insinuates physiological, ultrastructural and oxidative damage: A life cycle study on Eisenia fetida. Environ Pollut 254:11. https://doi.org/10.1016/j.envpol.2019.113032
Adeel M, Shakoor N, Shafiq M, Pavlicek A, Part F, Zafiu C, Raza A, Ahmad MA, Jilani G, White JC, Ehmoser EK, Lynch I, Ming X, Rui YK (2021) A critical review of the environmental impacts of manufactured nano-objects on earthworm species. Environ Pollut 290:118041. https://doi.org/10.1016/j.envpol.2021.118041
Ahmadpour M, Wang W, Sinkakarimi MH, Ahmadpour M, Hosseini SH (2023) Joint toxicity of cadmium and fenpyroximate on two earthworms: Interspecific differences, subcellular partitioning and biomarker responses. Chemosphere 337:139329. https://doi.org/10.1016/j.chemosphere.2023.139329
Antisari LV, Laudicina VA, Gatti A, Carbone S, Badalucco L, Vianello G (2015) Soil microbial biomass carbon and fatty acid composition of earthworm Lumbricus rubellus after exposure to engineered nanoparticles. Biol Fertil Soils 51:261–269. https://doi.org/10.1007/s00374-014-0972-1
Beliaeff B, Burgeot T (2002) Integrated biomarker response: A useful tool for ecological risk assessment. Environ Toxicol Chem 21:1316–1322. https://doi.org/10.1002/etc.5620210629
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. https://doi.org/10.1006/abio.1976.9999
Chen JQ, Saleem M, Wang CX, Liang WX, Zhang QM (2018) Individual and combined effects of herbicide tribenuron-methyl and fungicide tebuconazole on soil earthworm Eisenia fetida. Sci Rep 8:2967. https://doi.org/10.1038/s41598-018-21288-y
Cui WZ, Gao PP, Zhang MY, Wang L, Sun HW, Liu CG (2022) Adverse effects of microplastics on earthworms: A critical review. Sci Total Environ 850:158041. https://doi.org/10.1016/j.scitotenv.2022.158041
Devin S, Burgeot T, Giamberini L, Minguez L, Pain-Devin S (2014) The integrated biomarker response revisited: optimization to avoid misuse. Environ Sci Pollut Res 21:2448–2454. https://doi.org/10.1007/s11356-013-2169-9
Ding WL, Li Z, Qi RM, Jones DL, Liu QY, Liu Q, Yan CR (2021) Effect thresholds for the earthworm Eisenia fetida: Toxicity comparison between conventional and biodegradable microplastics. Sci Total Environ 781:146884. https://doi.org/10.1016/j.scitotenv.2021.146884
Ellman GL, Courtney KD, Andres V Jr, Feather-Stone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95. https://doi.org/10.1016/0006-2952(61)90145-9
Feng X, Wang Q, Sun Y, Zhang S, Wang F (2022) Microplastics change soil properties, heavy metal availability and bacterial community in a Pb-Zn-contaminated soil. J Hazard Mater 424:127364. https://doi.org/10.1016/j.jhazmat.2021.127364
Gautam K, Anbumani S (2023) Recent trends in analytical measures of microplastic in soil and toxicopathological risk assessment in earthworms. Trac-Trends Anal Chem 168:117292. https://doi.org/10.1016/j.trac.2023.117292
Ghose TK (1987) Measurement of cellulase activities. Pure Appl Chem 59:257–268. https://doi.org/10.1351/pac198759020257
Gudeta K, Kumar V, Bhagat A, Julka JM, Bhat SA, Ameen F, Qadri H, Singh S, Amarowicz R (2023) Ecological adaptation of earthworms for coping with plant polyphenols, heavy metals, and microplastics in the soil: A review. Heliyon 9:e14572. https://doi.org/10.1016/j.heliyon.2023.e14572
Guo S, Wang Q, Li ZS, Chen YH, Li HJ, Zhang JJ, Wang XX, Liu JW, Cao B, Zou GY, Zhang BG, Zhao M (2023) Ecological risk of microplastic toxicity to earthworms in soil: A bibliometric analysis. Front Environ Sci 11:1126847. https://doi.org/10.3389/fenvs.2023.1126847
He FL, Shi HJ, Liu RT, Tian G, Qi YT, Wang TT (2023) Randomly-shaped nanoplastics induced stronger biotoxicity targeted to earthworm Eisenia fetida species: Differential effects and the underlying mechanisms of realistic and commercial polystyrene nanoplastics. Sci Total Environ 877:162854. https://doi.org/10.1016/j.scitotenv.2023.162854
Huang CD, Ge Y, Yue SZ, Zhao L, Qiao YH (2021) Microplastics aggravate the joint toxicity to earthworm Eisenia fetida with cadmium by altering its availability. Sci Total Environ 753. https://doi.org/10.1016/j.scitotenv.2020.142042
Jia L, Liu L, Zhang Y, Fu W, Liu X, Wang Q, Tanveer M, Huang L (2023) Microplastic stress in plants: effects on plant growth and their remediations. Front Plant Sci 14. https://doi.org/10.3389/fpls.2023.1226484
Kanmani S (2022) Enhancement of biological hydrogen production from organic wastes with the application of nanomaterials. Int J Energy Res 46:18929–18946. https://doi.org/10.1002/er.8616
Khalid N, Aqeel M, Noman A, Khan SM, Akhter N (2021) Interactions and effects of microplastics with heavy metals in aquatic and terrestrial environments. Environ Pollut 290. https://doi.org/10.1016/j.envpol.2021.118104
Kwak JI, An YJ (2015) Ecotoxicological Effects of Nanomaterials on Earthworms: A Review. Hum Ecol Risk Assess 21:1566–1575. https://doi.org/10.1080/10807039.2014.960302
Lahive E, Walton A, Horton AA, Spurgeon DJ, Svendsen C (2019) Microplastic particles reduce reproduction in the terrestrial worm Enchytraeus crypticus in a soil exposure. Environ Pollut 255:113174. https://doi.org/10.1016/j.envpol.2019.113174
Li KH, Wang FY (2023) Global hotspots and trends in interactions of microplastics and heavy metals: a bibliometric analysis and literature review. Environ Sci Pollut Res 30:93309–93322. https://doi.org/10.1007/s11356-023-29091-7
Li M, Yang Y, Xie JW, Xu GH, Yu Y (2019a) In-vivo and in-vitro tests to assess toxic mechanisms of nano ZnO to earthworms. Sci Total Environ 687:71–76. https://doi.org/10.1016/j.scitotenv.2019.05.476
Li XZ, Wang ME, Chen WP, Jiang R (2019b) Evaluation of combined toxicity of Siduron and cadmium on earthworm (Eisenia fetida) using Biomarker Response Index. Sci Total Environ 646:893–901. https://doi.org/10.1016/j.scitotenv.2018.07.380
Li M, Jia H, Gao QC, Han S, Yu Y, Sun L (2023) Influence of aged and pristine polyethylene microplastics on bioavailability of three heavy metals in soil: Toxic effects to earthworms (Eisenia fetida). Chemosphere 311. https://doi.org/10.1016/j.chemosphere.2022.136833
Liang X, Zhou D, Wang J, Li Y, Liu Y, Ning Y (2022) Evaluation of the toxicity effects of microplastics and cadmium on earthworms. Sci Total Environ 836:155747. https://doi.org/10.1016/j.scitotenv.2022.155747
Lindsay WL (1978) Development of a DTPA Soil Test for Zinc, Iron, Manganese, and Copper. Soil Sci Soc Am J 42:421–428. https://doi.org/10.2136/sssaj1978.03615995004200030009x
Liu MT, Lu SB, Song Y, Lei LL, Hu JN, Lv WW, Zhou WZ, Cao CJ, Shi HH, Yang XF, He DF (2018) Microplastic and mesoplastic pollution in farmland soils in suburbs of Shanghai, China. Environ Pollut 242:855–862. https://doi.org/10.1016/j.envpol.2018.07.051
Liu GX, Dave PH, Kwong RWM, Wu MJ, Zhong H (2021) Influence of Microplastics on the Mobility, Bioavailability, and Toxicity of Heavy Metals: A Review. Bull Environ Contam Toxicol 107:710–721. https://doi.org/10.1007/s00128-021-03339-9
Luo YR, Wang SH, Yun MX, Li XY, Wang JJ, Sun ZJ (2009) The toxic effects of ionic liquids on the activities of acetylcholinesterase and cellulase in earthworms. Chemosphere 77:313–318. https://doi.org/10.1016/j.chemosphere.2009.07.026
Maehly AC, Chance B (1954) The assay of catalases and peroxidases. Methods Biochem Anal 1:357–424. https://doi.org/10.1002/9780470110171.ch14
Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474. https://doi.org/10.1111/j.1432-1033.1974.tb03714.x
More SL, Kovochich M, Lyons-Darden T, Taylor M, Schulte AM, Madl AK (2021) Review and evaluation of the potential health effects of oxidic nickel nanoparticles. Nanomaterials 11:642. https://doi.org/10.3390/nano11030642
OECD (2016) Test no. 222: earthworm reproduction test (Eisenia fetida/Eisenia andrei) [S]. Paris
Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358. https://doi.org/10.1016/0003-2697(79)90738-3
Ruby MV, Schoof R, Brattin W, Goldade M, Post G, Harnois M, Mosby DE, Casteel SW, Berti W, Carpenter M, Edwards D, Cragin D, Chappell W (1999) Advances in evaluating the oral bioavailability of inorganics in soil for use in human health risk assessment. Environ Sci Technol 33:3697–3705. https://doi.org/10.1021/es990479z
Salam M, Zheng HL, Liu YY, Zaib A, Rehman SAU, Riaz N, Eliw M, Hayat F, Li H, Wang FY (2023) Effects of micro(nano)plastics on soil nutrient cycling: State of the knowledge. J Environ Manag 344:118437. https://doi.org/10.1016/j.jenvman.2023.118437
Sanchez W, Burgeot T, Porcher JM (2013) A novel “Integrated Biomarker Response” calculation based on reference deviation concept. Environ Sci Pollut Res 20:2721–2725. https://doi.org/10.1007/s11356-012-1359-1
Santos FCF, Gomes SIL, Scott-Fordsmand JJ, Amorim MJB (2017) Hazard assessment of nickel nanoparticles in soil—The use of a full life cycle test with Enchytraeus crypticus. Environ Toxicol Chem 36:2934–2941. https://doi.org/10.1002/etc.3853
Shang G, Zhai J, Xu G, Wang L, Wang X (2023) Ecotoxicological effects of co-exposure biodegradable microplastics polylactic acid with cadmium are higher than conventional microplastics polystyrene with cadmium on the earthworm. Sci Total Environ 903:166953. https://doi.org/10.1016/j.scitotenv.2023.166953
Shanmugapriya T, Balavijayalakshmi J (2021) Efficiency Studies of Galinsoga Parviflora Pigments as a Sensitizer in Pt Free Graphene Oxide/Nickel Oxide Counter Electrode: Dye Sensitized Solar Cell Applications. J Cluster Sci 32:1277–1288. https://doi.org/10.1007/s10876-020-01890-9
Shi YJ, Wang X, Lu YL, Yan S (2007) Comparative effects of lindane and deltamethrin on mortality, growth, and cellulase activity in earthworms (Eisenia fetida). Pestic Biochem Physiol 89:31–38. https://doi.org/10.1016/j.pestbp.2007.02.005
Shiosaka T, Okuda H, Fujii S (1971) Mechanism of the phosphorylation of thymidine by the culture filtrate of Clostridium perfringens and rat liver extract. Biochim Biophys Acta 246:171–183. https://doi.org/10.1016/0005-2787(71)90125-0
Singh S, Tiwari RK, Pandey RS (2018) Evaluation of acute toxicity of triazophos and deltamethrin and their inhibitory effect on AChE activity in Channa punctatus. Toxicol Rep 5:85–89. https://doi.org/10.1016/j.toxrep.2017.12.006
Tiwari RK, Singh S, Pandey RS (2019) Assessment of acute toxicity and biochemical responses to chlorpyrifos, cypermethrin and their combination exposed earthworm, Eudrilus eugeniae. Toxicol Rep 6:288–297. https://doi.org/10.1016/j.toxrep.2019.03.007
Wang Y (2018) Experimental techniques for ecological remediation of soil pollution (in Chinese). Science Press of China, Beijing
Wang FY, Zhang XQ, Zhang SQ, Zhang SW, Adams CA, Sun YH (2020) Effects of Co-Contamination of Microplastics and Cd on Plant Growth and Cd Accumulation. Toxics 8:36. https://doi.org/10.3390/toxics8020036
Wang FY, Feng XY, Liu YY, Adams CA, Sun YH, Zhang SW (2022a) Micro(nano)plastics and terrestrial plants: Up-to-date knowledge on uptake, translocation, and phytotoxicity. Resour Conserv Recycl 185:106503. https://doi.org/10.1016/j.resconrec.2022.106503
Wang FY, Zhong LH, Wu YC, He SY (2022b) Editorial: Microbial Interactions With Nanomaterials in the Environment and Their Application. Front Microbiol 13:850141. https://doi.org/10.3389/fmicb.2022.850141
Wang QL, Adams CA, Wang FY, Sun YH, Zhang SW (2022c) Interactions between microplastics and soil fauna: A critical review. Crit Rev Environ Sci Technol 52:3211–3243. https://doi.org/10.1080/10643389.2021.1915035
Wang ZF, Xue WA, Qi FJ, Zhang ZB, Li CA, Cao XF, Cui XW, Wang N, Cui ZJ (2023) How do different arsenic species affect the joint toxicity of perfluorooctanoic acid and arsenic to earthworm Eisenia fetida: A multi-biomarker approach. Ecotoxicol Environ Saf 251:114528. https://doi.org/10.1016/j.ecoenv.2023.114528
Xiao X, He E, Jiang X, Li X, Yang W, Ruan J, Zhao C, Qiu R, Tang Y (2022) Visualizing and assessing the size-dependent oral uptake, tissue distribution, and detrimental effect of polystyrene microplastics in Eisenia fetida. Environ Pollut 306:119436. https://doi.org/10.1016/j.envpol.2022.119436
Xu GH, Liu Y, Song X, Li M, Yu Y (2021a) Size effects of microplastics on accumulation and elimination of phenanthrene in earthworms. J Hazard Mater 403:123966. https://doi.org/10.1016/j.jhazmat.2020.123966
Xu Z, Yang Z, Shu W, Zhu T (2021b) Combined toxicity of soil antimony and cadmium on earthworm Eisenia fetida: Accumulation, biomarker responses and joint effect. J Hazard Mater Lett 2:100018. https://doi.org/10.1016/j.hazl.2021.100018
Yang WW, Cheng P, Adams CA, Zhang SW, Sun YH, Yu HW, Wang FY (2021) Effects of microplastics on plant growth and arbuscular mycorrhizal fungal communities in a soil spiked with ZnO nanoparticles. Soil Biol Biochem 155:108179. https://doi.org/10.1016/j.soilbio.2021.108179
Yang HR, Yan YM, Yu YK, He YL, Fu B, Wang J (2022) Distribution, sources, migration, influence and analytical methods of microplastics in soil ecosystems. Ecotoxicol Environ Saf 243:114009. https://doi.org/10.1016/j.ecoenv.2022.114009
Yuan P, Wang Y, Chen X, Gao P (2023) An overview of microplastic pollution in the environment over the megacity of Shanghai during 2013–2022. Sci Total Environ 912:168986. https://doi.org/10.1016/j.scitotenv.2023.168986
Zahabi P, Zakeri A, Asadrokht M (2023) A facile surfactant-assisted precipitation route to self-assembled 3D flower-shaped NiO nanostructures with enhanced surface area. J Sol-Gel Sci Technol 105:73–84. https://doi.org/10.1007/s10971-022-05980-0
Zaiman N, Shaari N (2023) Review on flower-like structure nickel based catalyst in fuel cell application. J Ind Eng Chem 119:1–76. https://doi.org/10.1016/j.jiec.2022.11.048
Zhang J, Liu S-S, Zhang J, Qin L-T, Deng H-P (2012) Two novel indices for quantitatively characterizing the toxicity interaction between ionic liquid and carbamate pesticides. J Hazard Mater 239:102–109. https://doi.org/10.1016/j.jhazmat.2012.07.063
Zhang SW, Han B, Sun YH, Wang FY (2020) Microplastics influence the adsorption and desorption characteristics of Cd in an agricultural soil. J Hazard Mater 388:121775. https://doi.org/10.1016/j.jhazmat.2019.121775
Zhang SW, Ren S, Pei L, Sun YH, Wang FY (2022) Ecotoxicological effects of polyethylene microplastics and ZnO nanoparticles on earthworm Eisenia fetida. Appl Soil Ecol 176:104469. https://doi.org/10.1016/j.apsoil.2022.104469
Zhou SP, Duan CQ, Michelle WHG, Yang FZ, Wang XH (2011) Individual and combined toxic effects of cypermethrin and chlorpyrifos on earthworm. J Environ Sci 23:676–680. https://doi.org/10.1016/s1001-0742(10)60462-7
Zhou Y, Liu X, Wang J (2019) Characterization of microplastics and the association of heavy metals with microplastics in suburban soil of central China. Sci Total Environ 694:133798. https://doi.org/10.1016/j.scitotenv.2019.133798
Zhou YF, He G, Jiang H, Pan K, Liu WZ (2023) Nanoplastics induces oxidative stress and triggers lysosome-associated immune-defensive cell death in the earthworm Eisenia fetida. Environ Int 174:107899. https://doi.org/10.1016/j.envint.2023.107899
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The authors declare they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. This work was supported by the China Huadian Corporation LTD. (NO: JS-BT-FW/QT-006).
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This work was supported by the China Huadian Corporation LTD. (NO: JS-BT-FW/QT-006).
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Xinyue Tian has drafted the work and revised it critically for important intellectual content. Zaifu Yang has made substantial contributions to the conception or design of the work. Wenjun Shu, Yiran Yang, Jingyao Xu and Simeng Kan provided technical support in chart making and helped prepare the experimental materials. All authors read and approved the final manuscript.
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Yang, Z., Tian, X., Shu, W. et al. Combined toxicity of polyethylene microplastics and nickel oxide nanoparticle on earthworm (Eisenia andrei): oxidative stress responses, bioavailability and joint effect. Environ Sci Pollut Res (2024). https://doi.org/10.1007/s11356-024-33512-6
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DOI: https://doi.org/10.1007/s11356-024-33512-6