Abstract
The effects of mixtures of nanoparticles (NPs) and other chemicals have been poorly studied in terrestrial invertebrates. In this study, we investigated the effects of binary mixtures of goethite (α-FeOOH) NPs and metallic (Cd and Pb) or organic (chlorpyrifos, CPF) contaminants in Eisenia andrei earthworms. We used the filter paper contact test to evaluate (i) the uptake of NPs in organisms exposed to the mixtures of NPs+Metals and NPs+CPF and (ii) the potential effects of the mixture of NPs+CPF on the CPF-induced inhibition of the biomarker enzymes acetylcholinesterase (AChE) and carboxylesterases (CES). We used the artificial soil test to deepen the study on joint effects of NPs+CPF. All compounds were applied separately and in binary mixtures. In the single exposure treatment, Fe levels decreased significantly in organisms exposed to NPs on filter paper, suggesting systemic effects aimed at eliminating Fe incorporated through NPs. Conversely, earthworms exposed to binary mixtures showed Fe levels similar (NPs+Metals) to or higher (NPs+CPF) than controls. The earthworms single exposed to NPs presented no changes in AChE and CES activities. In the artificial soil test, the only treatment that showed AChE inhibition after 72 h was single CPF exposure, while no significant changes were observed in CES activity. However, after 7-day exposure in artificial soil or 72-h exposure on filter paper, the mixture of NPs+CPF induced a similar degree of AChE and CES inhibition as single CPF exposure. All these suggested that NPs did not produce neurotoxic effects, and that the inhibition of the enzymes’ activities in all cases was due to the presence of the pesticide. On the other hand, the differences in the pattern of Fe accumulation in the earthworms indicate that the presence of other contaminants in the exposure media can modify the uptake and/or the excretion of Fe and evidence the interactions that may be found in binary mixtures of metal oxide NPs and other pre-existing contaminants in the soil ecosystem.
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References
Aldridge WN (1953) Serum esterases I: two types of esterase (A and B) hydrolysing p-nitrophenyl acetate, propionate and butyrate, and a method for their determination. Biochem J 53:110–117. https://doi.org/10.1006/eesa.1997.1560
Alloway B (2013) Bioavailability of elements in soil. In: Essentials of medical geology: Revised Edition. Springer, pp 351–373
ATSDR A for TS and DR (2019) Toxicological profile for lead (draft for public comment). Atlanta, GA: U.S.
Basack SB, Oneto ML, Fuchs JS, Wood EJ, Kesten EM (1998) Esterases of Corbicula fluminea as biomarkers of exposure to organophosphorus pesticides. Bull Environ Contam Toxicol 61:569–576. https://doi.org/10.1007/s001289900799
Booth LH, O’Halloran K (2001) A comparison of biomarker responses in the earthworm Aporrectodea caliginosa to the organophosphorus insecticides diazinon and chlorpyrifos. Environ Toxicol Chem 20:2494–2502
Cacciatore LC, Verrengia Guerrero N, Cochón AC (2013) Cholinesterase and carboxylesterase inhibition in Planorbarius corneus exposed to binary mixtures of azinphos-methyl and chlorpyrifos. Aquat Toxicol 128–129:124–134. https://doi.org/10.1016/j.aquatox.2012.12.005
Cáceres Wenzel MI, Gigena J, Fuchs JS et al (2016) Goethite nanoparticles in Eisenia andrei: uptake, subcellular effects and their influence on the accumulation of Cd and Pb. Química Viva:29–44 (in Spanish)
Caselli F, Gastaldi L, Gambi N, Fabbri E (2006) In vitro characterization of cholinesterases in the earthworm Eisenia andrei. Comp Biochem Physiol - C Toxicol Pharmacol 143:416–421. https://doi.org/10.1016/j.cbpc.2006.04.003
Chen C, Wang Y, Zhao X, Wang Q, Qian Y (2014) Comparative and combined acute toxicity of butachlor, imidacloprid and chlorpyrifos on earthworm, Eisenia fetida. Chemosphere 100:111–115. https://doi.org/10.1016/j.chemosphere.2013.12.023
Chernyshova IV, Ponnurangam S, Somasundaran P (2011) Effect of nanosize on catalytic properties of ferric (hydr)oxides in water: mechanistic insights. J Catal 282:25–34. https://doi.org/10.1016/j.jcat.2011.05.021
Collange B, Wheelock CE, Rault M, Mazzia C, Capowiez Y, Sanchez-Hernandez JC (2010) Inhibition, recovery and oxime-induced reactivation of muscle esterases following chlorpyrifos exposure in the earthworm Lumbricus terrestris. Environ Pollut 158:2266–2272. https://doi.org/10.1016/j.envpol.2010.02.009
Cross KM, Lu Y, Zheng T et al (2010) Water decontamination using iron and iron oxide nanoparticles - nanotechnology applications for clean water [book]. In: Savage N, Diallo M, Duncan J, Street ASE (eds) Nanotechnology applications for clean water, New York
Dallinger R (1993) Strategies of metal detoxification in terrestrial invertebrates. Ecotoxicol Met Invertebr:245–289
Dowling AP (2004) Development of nanotechnologies. Nano Today 7:30–35. https://doi.org/10.1016/S1369-7021(04)00628-5
DTU Environment (2018) The nanodatabase. http://nanodb.dk/en/.
Ellman GL, Courtney KD, Andres V, Featherstone 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
Fang Q, Shi Q, Guo Y, Hua J, Wang X, Zhou B (2016) Enhanced bioconcentration of Bisphenol A in the presence of nano-TiO2 can lead to adverse reproductive outcomes in zebrafish. Environ Sci Technol 50:1005–1013. https://doi.org/10.1021/acs.est.5b05024
Fischer E, Horvith I (1977) In vivo cumulation and discharge of azine, thiazine and xanthene dyes and their effects on the chloragogen cells of Lumbricidae (Oligochaeta). Acta Biol Hung 28:33–47
García-Gómez C, Babín M, García S, Almendros P, Pérez RA, Fernández MD (2019) Joint effects of zinc oxide nanoparticles and chlorpyrifos on the reproduction and cellular stress responses of the earthworm Eisenia andrei. Sci Total Environ 688:199–207. https://doi.org/10.1016/j.scitotenv.2019.06.083
Gong P, Perkins EJ (2016) Earthworm toxicogenomics: a renewed genome-wide quest for novel biomarkers and mechanistic insights. Appl Soil Ecol 104:12–24. https://doi.org/10.1016/j.apsoil.2015.11.005
Hjorth R, Coutris C, Nguyen NHA et al (2017) Ecotoxicity testing and environmental risk assessment of iron nanomaterials for sub-surface remediation – recommendations from the FP7 project NanoRem. Chemosphere. https://doi.org/10.1016/j.chemosphere.2017.05.060
Homa J, Rorat A, Kruk J, Cocquerelle C, Plytycz B, Vandenbulcke F (2015) Dermal exposure of Eisenia andrei earthworms: effects of heavy metals on metallothionein and phytochelatin synthase gene expressions in coelomocytes. Environ Toxicol Chem 34:1397–1404. https://doi.org/10.1002/etc.2944
Hackenberger DK, Stjepanović N, Lončarić Ž, Hackenberger BK (2019) Effects of single and combined exposure to nano and bulk zinc-oxide and propiconazole on Enchytraeus albidus. Chemosphere 224:572–579. https://doi.org/10.1016/j.chemosphere.2019.02.189
Jänsch S, Frampton GK, Römbke J, van den Brink P, Scott-Fordsmand JJ (2006) Effects of pesticides on soil invertebrates in model ecosystem and field studies: a review and comparison with laboratory. Environ Toxicol Chem 25:2490–2501
Kaegi R, Sinnet B, Zuleeg S et al (2010) Release of silver nanoparticles from outdoor facades. Environ Pollut. https://doi.org/10.1016/j.envpol.2010.06.009
Karaca A, Kizilkaya R, Turgay OC, Cetin SC (2010) Effects of earthworms on the availability and removal of heavy metals in soil. In: Soil heavy metals. pp 369–388
Kristoff G, Guerrero NV, de D’Angelo AMP, Cochón AC (2006) Inhibition of cholinesterase activity by azinphos-methyl in two freshwater invertebrates: Biomphalaria glabrata and Lumbriculus variegatus. Toxicology 222:185–194. https://doi.org/10.1016/j.tox.2006.02.018
Lowe CN, Butt KR (2007) Earthworm culture, maintenance and species selection in chronic ecotoxicological studies: a critical review. Eur J Soil Biol 43. https://doi.org/10.1016/j.ejsobi.2007.08.028
Lowry OH, Rosebrough NJ, Lewis Farr A, Randall RJ (1951) Protein measurement with the fenol phenol reagent. Readings 193:265–275
Ma C, Liu H, Chen G, et al (2017) Effects of titanium oxide nanoparticles on tetracycline accumulation and toxicity in: Oryza sativa (L.)
Missaoui WN, Arnold RD, Cummings BS (2018) Toxicological status of nanoparticles: what we know and what we don’t know. Chem Biol Interact November 1:1–12. https://doi.org/10.1016/j.cbi.2018.07.015
Morgan JE, Norey CG, Morgan AJ, Kay J (1989) A comparison of the cadmium-binding proteins isolated from the posterior alimentary canal of the earthworms Dendrodrilus rubidus and Lumbriculus rubellus. Comp Biochem Physiol Part C, Comp 92:15–21. https://doi.org/10.1016/0742-8413(89)90195-3
Nanorem (2017) NanoRem pilot site—Spolchemie II, Czech Republic: remediation of BTEX compounds using nano-goethite. NanoRem Bull 8:8–13
OECD (1984) “OECD 207 -earthworm, acute toxicity tests.” OECD Guidel Test Chem 207:9
Oneto ML, Basack SB, Casabé NB et al (2005) Biological responses in the freshwater bivalve Corbicula fluminea and the earthworm Eisenia fetida exposed to fenitrothion. Fresenius Environ Bull 14:716–720
Pachapur VL, Dalila Larios A, Cledón M, Brar SK, Verma M, Surampalli RY (2016) Behavior and characterization of titanium dioxide and silver nanoparticles in soils. Sci Total Environ 563–564:933–943. https://doi.org/10.1016/j.scitotenv.2015.11.090
Parveen S, Misra R, Sahoo SK (2012) Nanoparticles: a boon to drug delivery, therapeutics, diagnostics and imaging. Nanomedicine Nanotechnology, Biol Med 8:147–166. https://doi.org/10.1016/j.nano.2011.05.016
Roberts TL (2014) Cadmium and phosphorous fertilizers: the issues and the science. Procedia Eng 83:52–59. https://doi.org/10.1016/j.proeng.2014.09.012
Sanchez-Hernandez JC, Wheelock CE (2009) Tissue distribution, isozyme abundance and sensitivity to chlorpyrifos-oxon of carboxylesterases in the earthworm Lumbricus terrestris. Environ Pollut 157:264–272. https://doi.org/10.1016/j.envpol.2008.06.041
Sanvicens N, Marco MP (2008) Multifunctional nanoparticles - properties and prospects for their use in human medicine. Trends Biotechnol 26:425–433. https://doi.org/10.1016/j.tibtech.2008.04.005
Stepić S, Hackenberger BK, Velki M, Lončarić Ž, Hackenberger DK (2013) Effects of individual and binary-combined commercial insecticides endosulfan, temephos, malathion and pirimiphos-methyl on biomarker responses in earthworm Eisenia andrei. Environ Toxicol Pharmacol 36:715–723. https://doi.org/10.1016/J.ETAP.2013.06.011
van Gestel CAM, Dirven-van Breemen EM, Baerselman R (1993) Accumulation and elimination of cadmium, chromium and zinc and effects on growth and reproduction in Eisenia andrei (Oligochaeta, Annelida). Sci Total Environ 134:585–597. https://doi.org/10.1016/S0048-9697(05)80061-0
Velki M, Hackenberger BK (2013a) Inhibition and recovery of molecular biomarkers of earthworm Eisenia andrei after exposure to organophosphate dimethoate. Soil Biol Biochem 57:100–108. https://doi.org/10.1016/j.soilbio.2012.09.018
Velki M, Hackenberger BK (2013b) Different sensitivities of biomarker responses in two epigeic earthworm species after exposure to pyrethroid and organophosphate insecticides. Arch Environ Contam Toxicol 65:498–509. https://doi.org/10.1007/s00244-013-9930-4
Vijver MG, Vink JPM, Miermans CJH, Van Gestel CAM (2003) Oral sealing using glue: a new method to distinguish between intestinal and dermal uptake of metals in earthworms. Soil Biol Biochem 35:125–132. https://doi.org/10.1016/S0038-0717(02)00245-6
Wang Y, Chen C, Qian Y, Zhao X, Wang Q, Kong X (2015) Toxicity of mixtures of λ -cyhalothrin , imidacloprid and cadmium on the earthworm Eisenia fetida by combination index ( CI ) -isobologram method. Ecotoxicol Environ Saf 111:242–247. https://doi.org/10.1016/j.ecoenv.2014.10.015
Wheelock CE, Shan G, Ottea J (2005) Overview of carboxylesterases and their role in the metabolism of insecticides. J Pestic Sci 30:75–83. https://doi.org/10.1584/jpestics.30.75
Wheelock CE, Phillips BM, Anderson BS, Miller JL, Miller MJ, Hammock BD (2008) Applications of carboxylesterase activity in environmental monitoring and toxicity identification evaluations (TIEs). Rev Environ Contam Toxicol 195:117–178. https://doi.org/10.1007/978-0-387-77030-7_5
Wu X, Cobbina SJ, Mao G, Xu H, Zhang Z, Yang L (2016) A review of toxicity and mechanisms of individual and mixtures of heavy metals in the environment. Environ Sci Pollut Res 23:8244–8259. https://doi.org/10.1007/s11356-016-6333-x
Wu Y, Pang H, Liu Y, Wang X, Yu S, Fu D, Chen J, Wang X (2019) Environmental remediation of heavy metal ions by novel-nanomaterials: a review. Environ Pollut 246:608–620. https://doi.org/10.1016/j.envpol.2018.12.076
Acknowledgments
The experiments using the filter paper test are part of the PhD thesis of MICW.
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This work was financially supported by grants from the University of Buenos Aires (grants 20020130100454BA, 20020170100106BA).
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The experiments on artificial soil were performed by JSF, MICW, and FNB; MICW, JSF, and ACC wrote the manuscript.
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Cáceres-Wenzel, M.I., Fuchs, J.S., Bernassani, F.N. et al. Combined effects of goethite nanoparticles with metallic contaminants and an organophosphorus pesticide on Eisenia andrei. Environ Sci Pollut Res 27, 20066–20075 (2020). https://doi.org/10.1007/s11356-020-08547-0
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DOI: https://doi.org/10.1007/s11356-020-08547-0