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Microplastic fibers influence Ag toxicity and bioaccumulation in Eisenia andrei but not in Enchytraeus crypticus

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Abstract

Microplastic fibers (MF) are released from synthetic textiles during washing and end up in the wastewater. Similarly, silver nanoparticles (AgNP), incorporated in textiles as antimicrobial agents, are released in washing machines, also reaching the wastewater treatment plants. Therefore, both MF and AgNP co-exist in the environment and enter the soil compartment mainly via the application of biosolids. Yet, the combined effect of MF and AgNP has not been studied. Here, we assessed the effects of polyester MF on the toxicity of AgNP and AgNO3 to the earthworm Eisenia andrei and the enchytraeid Enchytraeus crypticus. The organisms were exposed to a range of concentration of AgNP (32, 100, 320, 1000, 3200 mg Ag/kg) and AgNO3 (12.8, 32, 80, 200, 500 mg Ag/kg) in LUFA 2.2 soil in the absence or presence of MF (0.01% DW). Reproduction tests were conducted and the toxicity outcomes compared between soils with and without MF. The exposure to MF caused a decrease in the number of juveniles and changed the biochemical composition of earthworms. Moreover, the presence of MF increased the toxicity of AgNP to earthworm reproduction (EC50 = 165 mg Ag/kg) when compared to AgNP exposure alone (EC50 = 450 mg Ag/kg), but did not alter the toxicity of AgNO3 (EC50 = 40 mg Ag/kg). For enchytraeids, no significant difference in Ag toxicity could be detected when MF was added to the soil for both AgNP and AgNO3. Overall, Ag bioaccumulation was not affected by MF, except for a decrease in earthworm body concentration at the highest Ag soil concentration (3200 mg Ag/kg). Our results suggest that the presence of MF in the soil compartment may be a cause of concern, and that the joint exposure to Ag may be deleterious depending on the Ag form, organism, and endpoint. The present work provides the first evidence that a realistic MF concentration in soil lowers AgNP concentration necessary to provoke reproductive impairment in earthworms. The influence of MF on the risk assessment of AgNP should be considered.

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All data generated or analysed during this study are included in this published article (and its supplementary information files)

References

  • Aja M, Jaya M, Vijayakumaran NK, Hubert JI (2014) FT-IR spectroscopy as a sentinel technology in earthworm toxicology. Spectrochim Acta A Mol Biomol Spectrosc 120:534–541

    Article  CAS  Google Scholar 

  • Andre J, King RA, Stürzenbaum SR, Kille P, Hodson ME, Morgan AJ (2010) Molecular genetic differentiation in earthworms inhabiting a heterogeneous Pb-polluted landscape. Environ Pollut 158:883–890

    Article  CAS  Google Scholar 

  • Browne MA, Crump P, Niven SJ, Teuten E, Tonkin A, Galloway T, Thompson R (2011) Accumulation of microplastic on shorelines worldwide: sources and sinks. Environ Sci Technol 45:9175–9179

    Article  CAS  Google Scholar 

  • Coleman DC, Wall DH (2015) Soil fauna: occurrence, biodiversity, and roles in ecosystem function. In: Paul EA (Ed.) Soil Microbiology, Ecology and Biochemistry. Academic Press, San Diego, p 111–150

    Chapter  Google Scholar 

  • Cornelis G, Kirby JK, Beak D, Chittleborough D, McLaughlin MJ (2010) A method for determination of retention of silver and cerium oxide manufactured nanoparticles in soils. Environ Chem 7:298–308

    Article  CAS  Google Scholar 

  • de Souza Machado AA, Lau CW, Till J, Kloas W, Lehmann A, Becker R, Rillig MC (2018) Impacts of microplastics on the soil biophysical environment. Environ Sci Technol 52:9656–9665

    Article  CAS  Google Scholar 

  • Dholakiya B (2012) Unsaturated polyester resin for specialty applications. In: Saleh HEM (Ed.) Polyester. IntechOpen, London, p 167–202

    Google Scholar 

  • Diez-Ortiz M, Lahive E, George S, Ter Schure A, van Gestel CAM, Jurkschat K, Svendsen C, Spurgeon DJ (2015) Short-term soil bioassays may not reveal the full toxicity potential for nanomaterials; bioavailability and toxicity of silver ions (AgNO3) and silver nanoparticles to earthworm Eisenia fetida in long-term aged soils. Environ Pollut 203:191–198

    Article  CAS  Google Scholar 

  • Durán N, Marcato PD, De Souza GIH, Alves OL, Esposito E (2007) Antibacterial effect of silver nanoparticles produced by fungal process on textile fabrics and their effluent treatment. J Biomed Nanotechnol 3:203–208

    Article  CAS  Google Scholar 

  • Fuller S, Gautam A (2016) A procedure for measuring microplastics using pressurized fluid extraction. Environ Sci Technol 50:5774–5780

    Article  CAS  Google Scholar 

  • Gaylor MO, Harvey E, Hale RC (2013) Polybrominated diphenyl ether (PBDE) accumulation by earthworms (Eisenia fetida) exposed to biosolids-, polyurethane foam microparticle-, and penta-BDE-amended soils. Environ Sci Technol 47:13831–13839

    Article  CAS  Google Scholar 

  • Geyer R, Jambeck JR, Law KL (2017) Production, use, and fate of all plastics ever made. Sci Adv 3:e1700782

    Article  CAS  Google Scholar 

  • Gies EA, LeNoble JL, Noël M, Etemadifar A, Bishay F, Hall ER, Ross PS (2018) Retention of microplastics in a major secondary wastewater treatment plant in Vancouver, Canada. Mar Pollut Bull 133:553–561

    Article  CAS  Google Scholar 

  • Hayashi Y, Heckmann LH, Simonsen V, Scott-Fordsmand JJ (2013) Time-course profiling of molecular stress responses to silver nanoparticles in the earthworm Eisenia fetida. Ecotoxicol Environ Saf 98:219–226

    Article  CAS  Google Scholar 

  • Hernandez E, Nowack B, Mitrano DM (2017) Polyester textiles as a source of microplastics from households: a mechanistic study to understand microfiber release during washing. Environ Sci Technol 51:7036–7046

    Article  CAS  Google Scholar 

  • Hodson ME, Duffus-Hodson CA, Clark A, Prendergast-Miller MT, Thorpe KL (2017) Plastic bag derived-microplastics as a vector for metal exposure in terrestrial invertebrates. Environ Sci Technol 51:4714–4721

    Article  CAS  Google Scholar 

  • Horton AA, Svendsen C, Williams RJ, Spurgeon DJ, Lahive E (2017a) Large microplastic particles in sediments of tributaries of the River Thames, UK – Abundance, sources and methods for effective quantification. Mar Pollut Bull 114:218–226

    Article  CAS  Google Scholar 

  • Horton AA, Walton A, Spurgeon DJ, Lahive E, Svendsen C (2017b) Microplastics in freshwater and terrestrial environments: evaluating the current understanding to identify the knowledge gaps and future research priorities. Sci Total Environ 586:127–141

    Article  CAS  Google Scholar 

  • Huerta Lwanga E, Gertsen H, Gooren H, Peters P, Salánki T, van der Ploeg M, Besseling E, Koelmans AA, Geissen V (2016) Microplastics in the terrestrial ecosystem: implications for Lumbricus terrestris (Oligochaeta, Lumbricidae). Environ Sci Technol 50:2685–2691

    Article  CAS  Google Scholar 

  • Jiang X, Chang Y, Zhang T, Qiao Y, Klobučar G, Li M (2020) Toxicological effects of polystyrene microplastics on earthworm (Eisenia fetida). Environ Pollut 259:113896

    Article  CAS  Google Scholar 

  • Kalčíková G, Skalar T, Marolt G, Kokalj AJ (2020) An environmental concentration of aged microplastics with adsorbed silver significantly affects aquatic organisms. Water Res 175:115644

    Article  CAS  Google Scholar 

  • Khan FR, Syberg K, Shashoua Y, Bury NR (2015) Influence of polyethylene microplastic beads on the uptake and localization of silver in zebrafish (Danio rerio). Environ Pollut 206:73–79

    Article  CAS  Google Scholar 

  • 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 225:113174

    Article  CAS  Google Scholar 

  • Levard C, Hotze EM, Lowry GV, Brown Jr GE (2012) Environmental transformations of silver nanoparticles: impact on stability and toxicity. Environ Sci Technol 46:6900–6914

    Article  CAS  Google Scholar 

  • Li P, Zou X, Wang X, Su M, Chen C, Sun X, Zhang H (2020) A preliminary study of the interactions between microplastics and citrate-coated silver nanoparticles in aquatic environments. J Hazard Mater 385:121601

    Article  CAS  Google Scholar 

  • Mitrano DM, Rimmele E, Wichser A, Erni R, Height M, Nowack B (2014) Presence of nanoparticles in wash water from conventional silver and nano-silver textiles. ACS Nano 8:7208–7219

    Article  CAS  Google Scholar 

  • Monikh FA, Vijver MG, Guo Z, Zhang P, Darbha GK, Peijnenburg WJGM (2020) Metal sorption onto nanoscale plastic debris and trojan horse effects in Daphnia magna: Role of dissolved organic matter. Water Res 186:116410

    Article  CAS  Google Scholar 

  • Muthukaruppan G (2015) Heavy metal induced biomolecule and genotoxic changes in earthworm Eisenia fetida. Invertebr Surviv J 12:237–245

    Google Scholar 

  • Ng EL, Lwanga EH, Eldridge SM, Johnston P, Hu HW, Geissen V, Chen D (2018) An overview of microplastic and nanoplastic pollution in agroecosystems. Sci Total Environ 627:1377–1388

    Article  CAS  Google Scholar 

  • Nizzetto L, Futter M, Langaas S (2016) Are agricultural soils dumps for microplastics of urban origin? Environ Sci Technol 50:10777–10779

    Article  CAS  Google Scholar 

  • OECD (2004a) Test No. 222: Earthworm Reproduction Test (Eisenia fetida/Eisenia andrei). In OECD Guidelines for the Testing of Chemicals. Organisation for Economic Co-operation and Development, Paris, 2004

  • OECD (2004b) Test No. 220: Enchytraeid Reproduction Test. In OECD Guidelines for the Testing of Chemicals. Organisation for Economic Co-operation and Development, Paris, 2004

  • Patricia CS, Nerea GV, Erik U, Elena SM, Eider B, Manu S (2017) Responses to silver nanoparticles and silver nitrate in a battery of biomarkers measured in coelomocytes and in target tissues of Eisenia fetida earthworms. Ecotoxicol Environ Saf 141:57–63

    Article  CAS  Google Scholar 

  • Pirc U, Vidmar M, Mozer A, Kržan A (2016) Emissions of microplastic fibers from microfiber fleece during domestic washing. Environ Sci Pollut Res 23:22206–22211

    Article  CAS  Google Scholar 

  • Prendergast-Miller MT, Katsiamides A, Abbass M, Sturzenbaum SR, Thorpe KL, Hodson ME (2019) Polyester-derived microfibre impacts on the soil-dwelling earthworm Lumbricus terrestris. Environ Pollut 251:453–459

    Article  CAS  Google Scholar 

  • Ribeiro F, O’Brien JW, Galloway T, Thomas KV (2019) Accumulation and fate of nano- and micro-plastics and associated contaminants in organisms. Trends Analyt Chem 111:139–147

    Article  CAS  Google Scholar 

  • Rodríguez-Seijo A, Lourenço J, Rocha-Santos TAP, da Costa J, Duarte AC, Vala H, Pereira R (2017) Histopathological and molecular effects of microplastics in Eisenia andrei Bouché. Environ Pollut 220:495–503

    Article  CAS  Google Scholar 

  • Rosu D, Cascaval CN, Rosu L (2008) Synthesis and characterization of some composites with bioactive properties on the basis of vinyl ester resins. e-Polymers 8:1–10

    Article  Google Scholar 

  • Scheurer M, Bigalke M (2018) Microplastics in Swiss floodplain soils. Environ Sci Technol 52:3591–3598

    Article  CAS  Google Scholar 

  • Schlich K, Klawonn T, Terytze K, Hund‐Rinke K (2013) Effects of silver nanoparticles and silver nitrate in the earthworm reproduction test. Environ Toxicol Chem 32:181–188

    Article  CAS  Google Scholar 

  • Selonen S, Dolar A, Kokalj AJ, Skalar T, Dolcet LP, Hurley R, van Gestel CAM (2020) Exploring the impacts of plastics in soil – The effects of polyester textile fibers on soil invertebrates. Sci Total Environ 700:134451

    Article  CAS  Google Scholar 

  • Shoults-Wilson WA, Reinsch BC, Tsyusko OV, Bertsch PM, Lowry GV, Unrine JM (2011a) Role of particle size and soil type in toxicity of silver nanoparticles to earthworms. Soil Sci Soc Am J 75:365–377

    Article  CAS  Google Scholar 

  • Shoults-Wilson WA, Reinsch BC, Tsyusko OV, Bertsch PM, Lowry GV, Unrine JM (2011b) Effect of silver nanoparticle surface coating on bioaccumulation and reproductive toxicity in earthworms (Eisenia fetida). Nanotoxicology 5:432–444

    Article  CAS  Google Scholar 

  • Sillanpää M, Sainio P (2017) Release of polyester and cotton fibers from textiles in machine washings. Environ Sci Pollut Res 24:19313–19321

    Article  CAS  Google Scholar 

  • Santorufo L, van Gestel CAM, Maisto G (2012) Ecotoxicological assessment of metal-polluted urban soils using bioassays with three soil invertebrates. Chemosphere 88:418–425

    Article  CAS  Google Scholar 

  • Topuz E, van Gestel CAM (2017) The effect of soil properties on the toxicity and bioaccumulation of Ag nanoparticles and Ag ions in Enchytraeus crypticus. Ecotoxicol Environ Saf 144:330–337

    Article  CAS  Google Scholar 

  • Tosza E, Dumnicka E, Niklińska M, Rożen A (2010) Enchytraeid and earthworm communities along a pollution gradient near Olkusz (southern Poland). Eur J Soil Biol 46:218–224

    Article  CAS  Google Scholar 

  • Tourinho PS, van Gestel CAM, Morgan AJ, Kille P, Svendsen C, Jurkschat K, Mosselmans JFW, Soares AMVM, Loureiro S (2016) Toxicokinetics of Ag in the terrestrial isopod Porcellionides pruinosus exposed to Ag NPs and AgNO3 via soil and food. Ecotoxicology 25:267–278

    Article  CAS  Google Scholar 

  • Tourinho PS, Kočí V, Loureiro S, van Gestel CAM (2019) Partitioning of chemical contaminants to microplastics: Sorption mechanisms, environmental distribution and effects on toxicity and bioaccumulation. Environ Pollut 252:1246–1256

    Article  CAS  Google Scholar 

  • Tsyusko OV, Hardas SS, Shoults-Wilson WA, Starnes CP, Joice G, Butterfield DA, Unrine JM (2012) Short-term molecular-level effects of silver nanoparticle exposure on the earthworm, Eisenia fetida. Environ Pollut 171:249–255

    Article  CAS  Google Scholar 

  • USEPA (2009) Targeted national sewage sludge survey statistical analysis report. Appendix 1. United States Environmental Protection Agency Office of Water. EPA-822-R-08-018, Washington.

    Google Scholar 

  • Van der Ploeg MJC, Handy RD, Waalewijn‐Kool PL, van den Berg JHJ, Herrera Rivera ZE, Bovenschen J, Molleman B, Baveco JM, Tromp P, Peters RJB (2014) Effects of silver nanoparticles (NM‐300K) on Lumbricus rubellus earthworms and particle characterization in relevant test matrices including soil. Environ Toxicol Chem 33:743–752

    Article  CAS  Google Scholar 

  • Van Vliet PCJ, Didden WAM, Van der Zee SEATM, Peijnenburg WJGM (2006) Accumulation of heavy metals by enchytraeids and earthworms in a floodplain. Eur J Soil Biol 42:S117–S126

    CAS  Google Scholar 

  • Wang H-T, Ding J, Xiong C, Zhu D, Li G, Jia X-Y, Zhu Y-G, Xue X-M (2019a) Exposure to microplastics lowers arsenic accumulation and alters gut bacterial communities of earthworm Metaphire californica. Environ Pollut 251:110–116

    Article  CAS  Google Scholar 

  • Wang J, Coffin S, Sun C, Schlenk D, Gan J (2019b) Negligible effects of microplastics on animal fitness and HOC bioaccumulation in earthworm Eisenia fetida in soil. Environ Pollut 249:776–784

    Article  CAS  Google Scholar 

  • Whiteley CM, Dalla Valle M, Jones KC, Sweetman AJ (2013) Challenges in assessing release, exposure and fate of silver nanoparticles within the UK environment. Environ Sci Process Impacts 15:2050–2058

    Article  CAS  Google Scholar 

  • Wigger H, Hackmann S, Zimmermann T, Köser J, Thöming J, von Gleich A (2015) Influences of use activities and waste management on environmental releases of engineered nanomaterials. Sci Total Environ 535:160–171

    Article  CAS  Google Scholar 

  • Zhang GS, Zhang FX, Li XT (2019) Effects of polyester microfibers on soil physical properties: Perception from a field and a pot experiment. Sci Total Environ 670:1–7

    Article  CAS  Google Scholar 

  • Zhou Y, Liu X, Wang J (2020) Ecotoxicological effects of microplastics and cadmium on the earthworm Eisenia foetida. J Hazard Mater 392:122273

    Article  CAS  Google Scholar 

  • Zohdi V, Whelan DR, Wood BR, Pearson JT, Bambery KR, Black MJ (2015) Importance of tissue preparation methods in FTIR micro-spectroscopical analysis of biological tissues: ‘Traps for new users’. PLoS ONE 10:e0116491

    Article  CAS  Google Scholar 

  • Zubris KAV, Richards BK (2005) Synthetic fibers as an indicator of land application of sludge. Environ Pollut 138:201–211

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the European Structural and Investment Funds, OP RDE-funded project ‘CHEMFELLS4UCTP’ (No. CZ.02.2.69/0.0/0.0/17_050/0008485) and the Ministry of Education, Youth and Sports of the Czech Republic and the European Union (European Structural and Investment Funds - Operational Programme Research, Development and Education) in the frames of the project “Modular platform for autonomous chassis of specialized electric vehicles for freight and equipment transportation”, Reg. No. CZ.02.1.01/0.0/0.0/16_025/0007293. Thanks are due to FCT/MCTES for the financial support to CESAM (UIDP/50017/2020+UIDB/50017/2020), through national funds.

Author contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by P. S. T., V. S. S. L. P. T., A. D., R. V., J. C., and A. M. The first draft of the manuscript was written by P. S. T. and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Funding

This work was supported by the European Structural and Investment Funds, OP RDE-funded project ‘CHEMFELLS4UCTP’ (No. CZ.02.2.69/0.0/0.0/17_050/0008485) and the Ministry of Education, Youth and Sports of the Czech Republic and the European Union (European Structural and Investment Funds - Operational Programme Research, Development and Education) in the frames of the project “Modular platform for autonomous chassis of specialized electric vehicles for freight and equipment transportation”, Reg. No. CZ.02.1.01/0.0/0.0/16_025/0007293.

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Authors and Affiliations

  1. Department of Environmental Chemistry, Faculty of Environmental Technology, University of Chemistry and Technology Prague, Prague, Czech Republic

    Paula S. Tourinho & Vladimír Kočí

  2. CESAM & Department of Biology, University of Aveiro, Aveiro, Portugal

    Susana Loureiro

  3. Department of Biotechnology, Faculty of Food and Biochemical Technology, University of Chemistry and Technology Prague, Prague, Czech Republic

    V. S. S. L. Prasad Talluri

  4. Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia

    Andraž Dolar

  5. Department of Ecological Science, Faculty of Science, Vrije Universiteit, Amsterdam, The Netherlands

    Rudo Verweij & Cornelis A. M. van Gestel

  6. Faculty of Textile Engineering, Technical University of Liberec, Liberec, Czech Republic

    Jiří Chvojka

  7. Department of Metals and Corrosion Engineering, Faculty of Chemical Technology, University of Chemistry and Technology Prague, Prague, Czech Republic

    Alena Michalcová

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  1. Paula S. Tourinho
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Tourinho, P.S., Loureiro, S., Talluri, V.S.S.L.P. et al. Microplastic fibers influence Ag toxicity and bioaccumulation in Eisenia andrei but not in Enchytraeus crypticus. Ecotoxicology 30, 1216–1226 (2021). https://doi.org/10.1007/s10646-021-02424-3

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