Abstract
Co-exposure soil studies of pollutants are necessary for an appropriate ecological risk assessment. Here, we examined the effects of two-component mixtures of metal oxide nanoparticles (ZnO NPs or goethite NPs) with the insecticide chlorpyrifos (CPF) under laboratory conditions in short-term artificial soil assays using Eisenia andrei earthworms. We characterized NPs and their mixtures by scanning electron microscopy, atomic force microscopy, dynamic light scattering and zeta potential, and evaluated effects on metal accumulation, oxidative stress enzymes, and neurotoxicity related biomarkers in single and combined toxicity assays. Exposure to ZnO NPs increased Zn levels compared to control in single and combined exposure (ZnO NPs + CPF) at 72 h and 7 days, respectively. In contrast, there was no indication of Fe increase in organisms exposed to goethite NPs. One of the most notable effects on oxidative stress biomarkers was produced by single exposure to goethite NPs, showing that the worms were more sensitive to goethite NPs than to ZnO NPs. Acetylcholinesterase and carboxylesterase activities indicated that ZnO NPs alone were not neurotoxic to earthworms, but similar degrees of inhibition were observed after single CPF and ZnO NPs + CPF exposure. Differences between single and combined exposure were found for catalase and superoxide dismutase (goethite NPs) and for glutathione S-transferase (ZnO NPs) activities, mostly at 72 h. These findings suggest a necessity to evaluate mixtures of NPs with co-existing contaminants in soil, and that the nature of metal oxide NPs and exposure time are relevant factors to be considered when assessing combined toxicity, as it may have an impact on ecotoxicological risk assessment.
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Data Availability
The authors declare that the data supporting the findings of this study are available from the corresponding author upon reasonable request.
Abbreviations
- AChE:
-
Acetylcholinesterase
- BSA:
-
Bovine serum albumin
- CES:
-
Carboxylesterase
- CAT:
-
Catalase
- CDNB:
-
Chlorodinitrobenzene
- CPF:
-
Chlorpyrifos
- DTNB:
-
5,5′ Dithiobis-2 nitrobenzoic acid
- GST:
-
Glutathione-S-transferase
- MO-NPs:
-
Metal oxide nanoparticles
- NBT:
-
Nitro blue tetrazolium
- NPs:
-
Nanoparticles
- OP:
-
Organophosphate
- ROS:
-
Reactive oxygen species
- SOD:
-
Superoxide dismutase
References
Baragaño D, Alonso J, Gallego JR et al (2020) Zero valent iron and goethite nanoparticles as new promising remediation techniques for As-polluted soils. Chemosphere 238. https://doi.org/10.1016/j.chemosphere.2019.124624
Beig B, Niazi MBK, Jahan Z et al (2023) Development and testing of zinc sulfate and zinc oxide nanoparticle-coated urea fertilizer to improve N and Zn use efficiency. Front Plant Sci 13:1–16. https://doi.org/10.3389/fpls.2022.1058219
Bernard F, Brulle F, Dumez S et al (2015) Antioxidant responses of Annelids, Brassicaceae and Fabaceae to pollutants: A review. Ecotoxicol Environ Saf 114:273–303. https://doi.org/10.1016/j.ecoenv.2014.04.024
Brunetti G, Donner E, Laera G et al (2015) Fate of zinc and silver engineered nanoparticles in sewerage networks. Water Res 77:72–84. https://doi.org/10.1016/j.watres.2015.03.003
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). http://www.redalyc.org/articulo.oa?id=86347590005
Cáceres-Wenzel MI, Fuchs JS, Bernassani FN, Cochón AC (2020) Combined effects of goethite nanoparticles with metallic contaminants and an organophosphorus pesticide on Eisenia andrei. Environ Sci Pollut Res 27:20066–20075. https://doi.org/10.1007/s11356-020-08547-0
Carrasco V, Amarelle V, Lagos-Moraga S et al (2021) Production of cadmium sulfide quantum dots by the lithobiontic Antarctic strain Pedobacter sp. UYP1 and their application as photosensitizer in solar cells. Microb Cell Fact 20:1–10. https://doi.org/10.1186/s12934-021-01531-4
Causin HF, Bordón DAE, Burrieza H (2020) Salinity tolerance mechanisms during germination and early seedling growth in Chenopodium quinoa Wild. genotypes with different sensitivity to saline stress. Environ Exp Bot 172:103995. https://doi.org/10.1016/j.envexpbot.2020.103995
Dayem AA, Hossain MK, Bin LS et al (2017) The Role of Reactive Oxygen Species (ROS) in the Biological Activities of Metallic Nanoparticles. Int J Mol Sci 18:1–21. https://doi.org/10.3390/ijms18010120
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
García-Gómez C, Babín M, García S et al (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
García-Gómez C, García-Gutiérrez S, Obrador A, Fernández MD (2020) Study of Zn availability, uptake, and effects on earthworms of zinc oxide nanoparticle versus bulk applied to two agricultural soils: Acidic and calcareous. Chemosphere 239:124814. https://doi.org/10.1016/j.chemosphere.2019.124814
García-Gómez C, Pérez RA, Albero B et al (2023) Interaction of ZnO Nanoparticles with Metribuzin in a Soil–Plant System: Ecotoxicological Effects and Changes in the Distribution Pattern of Zn and Metribuzin. Agronomy 13. https://doi.org/10.3390/agronomy13082004
Giannopolitis C, Ries SK (1977) Superoxide Dismutases. Plant Physiol 59:315–318. https://doi.org/10.1016/S0079-6603(08)60843-0
Habig WH, Jakoby WB (1981) [51] Assays for differentiation of glutathione S-transferases. In: Methods in Enzymology. Academic Press, pp 398–405
Hou J, Zhang F, Wang P et al (2018) Enhanced anaerobic biological treatment of chlorpyrifos in farmland drainage with zero valent iron. Chem Eng J 336:352–360. https://doi.org/10.1016/j.cej.2017.12.032
Hu CW, Li M, Cui YB et al (2010) Toxicological effects of TiO2 and ZnO nanoparticles in soil on earthworm Eisenia fetida. Soil Biol Biochem 42:586–591. https://doi.org/10.1016/j.soilbio.2009.12.007
ISO (2012) ISO 11268-1:2012. Soil quality. Effects of pollutants on earthworms - Part 1: Determination of acute toxicity to Eisenia fetida/Eisenia andrei. ISO (International Organization for Standardization), Geneva
Jansen KL, Cole TB, Park SS et al (2009) Paraoxonase 1 (PON1) modulates the toxicity of mixed organophosphorus compounds. Toxicol Appl Pharmacol 236:142–153. https://doi.org/10.1016/j.taap.2009.02.001
Kabir E, Kumar V, Kim KH et al (2018) Environmental impacts of nanomaterials. J Environ Manag 225:261–271. https://doi.org/10.1016/j.jenvman.2018.07.087
Khan I, Saeed K, Khan I (2017) Nanoparticles: Properties, applications and toxicities. Arab J Chem. https://doi.org/10.1016/j.arabjc.2017.05.011
Klaine SJ, Alvarez PJJ, Batley GE et al (2008) Nanomaterials in the environment: Behavior, fate, bioavailability, and effects. Environ Toxicol Chem 27:1825–1851. https://doi.org/10.1897/08-090.1
Kritchenkov AS, Egorov AR, Volkova OV et al (2021) Novel biopolymer-based nanocomposite food coatings that exhibit active and smart properties due to a single type of nanoparticles. Food Chem 343. https://doi.org/10.1016/j.foodchem.2020.128676
Lahive E, Matzke M, Svendsen C et al (2023) Soil properties influence the toxicity and availability of Zn from ZnO nanoparticles to earthworms. Environ Pollut 319:0–9. https://doi.org/10.1016/j.envpol.2022.120907
Li M, Xu G, Yang X et al (2020) Metal oxide nanoparticles facilitate the accumulation of bifenthrin in earthworms by causing damage to body cavity. Environ Pollut 263:114629. https://doi.org/10.1016/j.envpol.2020.114629
Ling X, Yan Z, Liu Y, Lu G (2021) Transport of nanoparticles in porous media and its effects on the co-existing pollutants. Environ Pollut 283:117098. https://doi.org/10.1016/j.envpol.2021.117098
Lončarić, Hackenberger DK, Jug I, Hackenberger BK (2020) Is nano ZnO/chlorpyrifos mixture more harmful to earthworms than bulk ZnO? A multigeneration approach. Chemosphere 247. https://doi.org/10.1016/j.chemosphere.2020.125885
Lowry OH, Rosebrough NJ, Lewis Farr A, Randall RJ (1951) Protein measurement with the fenol phenol reagent. Readings 193:265–275
Lu PJ, Fu WE, Huang SC et al (2018) Methodology for sample preparation and size measurement of commercial ZnO nanoparticles. J Food Drug Anal 26:628–636. https://doi.org/10.1016/j.jfda.2017.07.004
Ma H, Williams PL, Diamond SA (2013) Ecotoxicity of manufactured ZnO nanoparticles - A review. Environ Pollut 172:76–85. https://doi.org/10.1016/j.envpol.2012.08.011
Martínez G, Merinero M, Pérez-Aranda M et al (2021) Environmental impact of nanoparticles’ application as an emerging technology: A review. Materials (basel) 14:1–26. https://doi.org/10.3390/ma14071710
Mohd Yusof H, Abdul Rahman NA, Mohamad R et al (2022) Optimization of biosynthesis zinc oxide nanoparticles: Desirability-function based response surface methodology, physicochemical characteristics, and its antioxidant properties. OpenNano 8. https://doi.org/10.1016/j.onano.2022.100106
Mu L, Sprando RL (2010) Application of nanotechnology in cosmetics. Pharm Res 27:1746–1749. https://doi.org/10.1007/s11095-010-0139-1
Naasz S, Altenburger R, Kühnel D (2018) Environmental mixtures of nanomaterials and chemicals: the Trojan-horse phenomenon and its relevance for ecotoxicity. Sci Total Environ 635:1170–1181. https://doi.org/10.1016/j.scitotenv.2018.04.180
Nowack B, Bucheli TD (2007) Occurrence, behavior and effects of nanoparticles in the environment. Environ Pollut 150:5–22. https://doi.org/10.1016/j.envpol.2007.06.006
OECD (1984) Test No. 207: earthworm, acute toxicity tests, OECD guidelines for the testing of chemicals, section 2. OECD Publishing, Paris. https://doi.org/10.1787/9789264070042-en
Peijnenburg W, Praetorius A, Scott-Fordsmand J, Cornelis G (2016) Fate assessment of engineered nanoparticles in solids dominated media – Current insights and the way forward. Environ Pollut 218:1365–1369. https://doi.org/10.1016/j.envpol.2015.11.043
Rajput VD, Minkina T, Sushkova S et al (2018) Effect of nanoparticles on crops and soil microbial communities. J Soils Sediments 18:2179–2187. https://doi.org/10.1007/s11368-017-1793-2
Rizwan M, Ali S, Qayyum MF et al (2017) Effect of metal and metal oxide nanoparticles on growth and physiology of globally important food crops: A critical review. J Hazard Mater 322:2–16. https://doi.org/10.1016/J.JHAZMAT.2016.05.061
Saint-Denis M, Labrot F, Narbonne JF, Ribera D (1998) Glutathione, glutathione-related enzymes, and catalase activities in the earthworm Eisenia fetida andrei. Arch Environ Contam Toxicol 35:602–614
Sanchez-Hernandez JC (2006) Earthworm biomarkers in ecological risk assessment. Rev Environ Contam Toxicol 188:85–126. https://doi.org/10.1007/978-0-387-32964-2_3
Sanchez-Hernandez JC, Mazzia C, Capowiez Y, Rault M (2009) Carboxylesterase activity in earthworm gut contents: Potential (eco)toxicological implications. Comp Biochem Physiol - C Toxicol Pharmacol 150:503–511. https://doi.org/10.1016/j.cbpc.2009.07.009
Sanchez-Hernandez JC, Notario del Pino J, Domínguez J (2015) Earthworm-induced carboxylesterase activity in soil: Assessing the potential for detoxification and monitoring organophosphorus pesticides. Ecotoxicol Environ Saf 122:303–312. https://doi.org/10.1016/j.ecoenv.2015.08.012
Šebesta M, Kolenčík M, Ratna Sunil B et al (2021) Field application of ZnO and TiO2 nanoparticles on agricultural plants. Agronomy 11:1–13. https://doi.org/10.3390/agronomy11112281
Stephensen E, Sturve J, Förlin L (2002) Effects of redox cycling compounds and activity of glutathione-related enzymes in rainbow trout liver. Comp Biochem Physiol Part C 4:435–442. https://doi.org/10.1186/1476-5926-4-4
Świątek ZM, van Gestel CAM, Bednarska AJ (2017) Toxicokinetics of zinc-oxide nanoparticles and zinc ions in the earthworm Eisenia andrei. Ecotoxicol Environ Saf 143:151–158
Thompson CM, Richardson RJ (2004) 3 Anticholinesterase. In: Marrs TC, Ballantyne B (eds) Pesticide Toxicology and International Regulation. John Wiley & Sons Ltd, England, pp 89–127
Torabi Farsani A, Arabi M, Shadkhast M (2021) Ecotoxicity of chlorpyrifos on earthworm Eisenia fetida (Savigny, 1826): Modifications in oxidative biomarkers. Comp Biochem Physiol Part - C Toxicol Pharmacol 249:109145. https://doi.org/10.1016/j.cbpc.2021.109145
Trigueiro NSS de, Gonçalves BB, Dias FC et al (2021) Co-exposure of iron oxide nanoparticles and glyphosate-based herbicide induces DNA damage and mutagenic effects in the guppy (Poecilia reticulata). Environ Toxicol Pharmacol 81. https://doi.org/10.1016/j.etap.2020.103521
Haq A ul, Saeed M, Usman M et al (2020) Sorption of chlorpyrifos onto zinc oxide nanoparticles impregnated Pea peels (Pisum sativum L): equilibrium, kinetic and thermodynamic studies. Environ Technol Innov 17. https://doi.org/10.1016/j.eti.2019.100516
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
Verma Y, Singh SK, Jatav HS et al (2022) Interaction of zinc oxide nanoparticles with soil: Insights into the chemical and biological properties. Environ Geochem Health 44:221–234. https://doi.org/10.1007/s10653-021-00929-8
Vidal A, Blouin M, Lubbers I et al (2023) The role of earthworms in agronomy: consensus, novel insights and remaining challenges. In: Sparks DL (ed) Advances in Agronomy, 1st edn. Academic Press, pp 1–78
Waychunas GA, Kim CS, Banfield JF (2005) Nanoparticulate iron oxide minerals in soils and sediments: Unique properties and contaminant scavenging mechanisms. J Nanoparticle Res 7:409–433. https://doi.org/10.1007/s11051-005-6931-x
Wu H, Yin JJ, Wamer WG et al (2014) Reactive oxygen species-related activities of nano-iron metal and nano-iron oxides. J Food Drug Anal 22:86–94. https://doi.org/10.1016/j.jfda.2014.01.007
Wu X, Wang W, Zhu L (2018) Enhanced organic contaminants accumulation in crops: Mechanisms, interactions with engineered nanomaterials in soil. Environ Pollut 240:51–59. https://doi.org/10.1016/j.envpol.2018.04.072
Xu CY, Deng KY, Li JY, Xu RK (2015) Impact of environmental conditions on aggregation kinetics of hematite and goethite nanoparticles. J Nanoparticle Res 17:1–13
Zhang F, He M, Zhang C et al (2021) Combined toxic effects of dioxin-like PCB77 with Fe-based nanoparticles in earthworm Eisenia fetida. Sci Total Environ 766:144347. https://doi.org/10.1016/j.scitotenv.2020.144347
Acknowledgements
We want to thank Dr. Fabio Causin for the technical support provided during SOD activity measurements, Dr. Santiago Herrera for the technical support provided during AFM analysis and Dr. Paola Ondarza for constructive criticism of the manuscript.
Funding
This work was supported by research grants from Secretaría Nacional de Ciencia y Técnica -Universidad de Buenos Aires (UBACyT) N° 20020170100106BA and N° 20020170100743BA, Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) PICT 2010–00544 and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) PIP 2021–2023 N° 11220200100133CO.
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Marcela I. Cáceres-Wenzel: Methodology, Investigation, Formal analysis, Writing- Original draft preparation, Writing- Reviewing & Editing; Florencia N. Bernassani: Investigation, Formal analysis, Writing- Original draft preparation, Julio S. Fuchs: Methodology, Conceptualization, Supervision; Eduardo Cortón: Supervision, Resources, Funding acquisition; Adriana C. Cochón: Conceptualization, Resources, Writing- Reviewing & Editing, Funding acquisition.
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Cáceres-Wenzel, M.I., Bernassani, F.N., Fuchs, J.S. et al. Mixture toxicity study of two metal oxide nanoparticles and chlorpyrifos on Eisenia andrei earthworms. Environ Sci Pollut Res (2024). https://doi.org/10.1007/s11356-024-33604-3
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DOI: https://doi.org/10.1007/s11356-024-33604-3