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Effect of microplastics on the activity of carboxylesterase and phosphatase enzymes in Scinax squalirostris tadpoles

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Abstract

Microplastics (MPs) are critical emerging pollutants around the world. There is a growing interest in the effects of MP ingestion, non-digestion, and toxicity on aquatic organisms. Amphibian tadpoles are the vertebrate group that has received the least attention regarding this issue. The aim of the present study was to determine the ingestion of polyethylene MPs by Scinax squalirostris tadpoles by atomic force microscopy (AFM) and to evaluate the activities of carboxylesterase (CbE, using 4-naphthyl butyrate-NB-, and 1-naphthyl acetate –NA- as substrates) and alkaline phosphatase (ALP) under MP exposure. Enzyme activities were analyzed spectrophotometrically at 2 and 10 days of exposure. Tadpoles were exposed to two different treatments during 10 days: a negative control (CO, dechlorinated water) and MP (60 mg L−1). AFM images of the digestive contents of tadpoles revealed the presence of MPs. After 10 days of MP exposure, CbE (NB) activity was significantly higher and CbE (NA) activity was significantly lower in MP treatments than in controls. ALP activity decreased in MP treatments after 2 and 10 days of exposure. The detection of MP particles in the intestinal contents and the effects on metabolic enzymes in a common frog species evidenced the potential health risk of MP to aquatic vertebrates. Thus, the differential response in enzymes and substrates demonstrate the need for considering the complex effects of contaminants and nutrients on ecosystems for ecotoxicological risk characterization.

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The datasets generated and analyzed during the study are available from the corresponding author on reasonable request.

References

  • Alabi, O. A., Ologbonjaye, K. I., & Awosolu, O. (2019). Public and environmental health effects of plastic wastes disposal: A review. Journal of Toxicology and Risk Assessment, 5, 021. https://doi.org/10.23937/2572-4061.1510021

  • Allasia, M., Passeggi, M. C. G., Gugliotta, L. M., & Minari, R. J. (2019). Water hybrid acrylic/protein nano composite with enhanced hydrophobicity by incorporating a water repelling protein. Industrial and Engineering Chemistry Research, 58, 21070–21079. https://doi.org/10.1021/acs.iecr.9b02518

    Article  CAS  Google Scholar 

  • American Society of Ichthyologists & Herpetologists. (2004). Guidelines for use of live amphibians and reptiles in field and laboratory research. Herpetological Animal Care and Use Committee of the American Society of Ichthyologists and Herpetologists (2nd ed.). Washington D.C.

  • Anbumani, S., & Kakkar, P. (2018). Ecotoxicological effects of microplastics on biota: a review. Environmental Science and Pollution Research, 25(15), 14373–14396. https://doi.org/10.1007/s11356018-1999-x

  • Araújo, A. P., Gomes, A. R., & Malafaia, G. (2020). Hepatotoxicity of pristine polyethylene microplastics in neotropical Physalaemuscuvieri tadpoles (Fitzinger, 1826). Journal of Hazardous Materials, 386, 121992. https://doi.org/10.1016/j.jhazmat.2019.121992

    Article  CAS  Google Scholar 

  • Attademo, A. M., Peltzer, P. M., Lajmanovich, R. C., Cabagna-Zenklusen, M. C., Junges, C. M., & Basso, A. (2014). Biological endpoints, enzyme activities, and blood cell parameters in two anuran tadpole species in rice agroecosystems of mid-eastern Argentina. Environmetal Monitoring and Assessment, 186(1), 635–649.

    Article  CAS  Google Scholar 

  • Attademo, A. M., Lajmanovich, R. C., Peltzer, P. M., Cuzziol Boccioni, A. P., Martinuzzi, C., Simonielo, F., & Repetti, M. R. (2021). Effects of the emulsifiable herbicide Dicamba on amphibian tadpoles: An underestimated toxicity risk?. Environmental Science and Pollution Research, 28, 31962–31974. https://doi.org/10.1007/s11356-021-13000-x

  • Attademo, A. M., Sanchez-Hernandez, J. C., Lajmanovich R. C., Peltzer, P. M., & Junges, C. (2017). Effect of diet on carboxylesterase activity of tadpoles (Rhinella arenarum) exposed to chlorpyrifos. Ecotoxicology and Environmental Safety, 135, 10–16.

  • Blaustein, A. R., Han, B. A., Relyea, R. A., Johnson, P. T., Buck, J. C., Gervasi, S. S., & Kats, L. B. (2011). The complexity of amphibian population declines: Understanding the role of cofactors in driving amphibian losses. Annals of the New York Academy of Sciences, 1223(1), 108–119.

    Article  Google Scholar 

  • Blettler, M. C., Ulla, M. A., Rabuffetti, A. P., & Garello, N. (2017). Plastic pollution in freshwater ecosystems: Macro-meso- and microplastic debris in floodplain lake. Environmental Monitoring and Assessment, 189–581. https://doi.org/10.1007/s10661-017-6305-8

  • Bunyan, P. J., & Jennings, D. M. (1968). Organophosphorus poisoning; some properties of avian esterase. Journal of Agricultural and Food Chemistry, 16, 326–331.

    Article  CAS  Google Scholar 

  • Davies, B. R., Biggs, J., Williams, P. J., Lee, J. T., & Thompson, S. (2007). A comparison of the catchment sizes of rivers, streams, ponds, ditches and lakes: Implications for protecting aquatic biodiversity in an agricultural landscape. In Pond conservation in Europe (pp 7–17), Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9088-1_2

  • Eaton, P., & West, P. (2010). Atomic force microscopy. Oxford University Press, Oxford

  • Erkes-Medrano, D., Thompson, R. C., & Aldridge, D. C. (2015). Microplastics in freshwater systems: A review of the emerging threats, identification of knowledge gaps and prioritization of research needs. Water Research, 75, 63–82. https://doi.org/10.1016/j.watres.2015.02.012

    Article  CAS  Google Scholar 

  • Gomori, G. (1953). Human esterases. Journal of Laboratory and Clinical Medicine, 42, 445–453.

    CAS  Google Scholar 

  • Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16(3), 183–190.

    Google Scholar 

  • Hajighasemi, M., Nocek, B. P., Tchigvintsev, A., Brown, G., Flick, R., Xu, X., & Yakunin, A. F. (2016). Biochemical and structural insights into enzymatic depolymerization of polylactic acid and other polyesters by microbial carboxylesterases. Biomacromolecules, 17(6), 2027–2039.

    Article  CAS  Google Scholar 

  • Han, Y., Chen, J., Li, Z., Chen, H., & Qiu, H. (2020). Recent progress and prospects of alkaline phosphatase biosensor based on fluorescence strategy. Biosensors and Bioelectronics, 148, 111811.

    Article  CAS  Google Scholar 

  • Hirt, N., & Body-Malapel, M. (2020). Immunotoxicity and intestinal effects of nano-and microplastics: A review of the literature. Particle and Fiber Toxicology, 17(1), 1–22. https://doi.org/10.1186/s12989-020-00387-7

    Article  Google Scholar 

  • Horcas, I., Fernández, R., Gomez-Rodriguez, J. M., Colchero, J. W. S. X., Gómez-Herrero, J. W. S., & Baro, A. M. (2007). WSXM: A software for scanning probe microscopy and a tool for nanotechnology. Review of Scientific Instruments, 78(1), 013705.

    Article  CAS  Google Scholar 

  • Hu, L., Su, L., Xue, Y., Mu, J., Zhu, J., Xu, J., & Shi, H., (2016). Uptake, accumulation and elimination of polystyrene microspheres in tadpoles of Xenopus tropicalis. Chemosphere, 164, 611–617. https://doi.org/10.1016/j.chemosphere.2016.09.002

  • Hu, S., Niu, Z., Chen, Y., Li, Y., & Zhang, H. (2017). Global wetlands: Potential distribution, wetland loss, and status. Science of the Total Environment, 586, 319–327. https://doi.org/10.1016/j.scitotenv.2017.02.001

    Article  CAS  Google Scholar 

  • Kawai, F., Kawabata, T., & Oda, M. (2019). Current knowledge on enzymatic PET degradation and its possible application to waste stream management and other fields. Applied Microbiology and Biotechnology, 103(11), 4253–4268. https://doi.org/10.1007/s00253-019-09717-y

    Article  CAS  Google Scholar 

  • Kilkenny, C., Browne, W. J., Cuthill, I. C., Emerson, M., & Altman, D. G. (2010). Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. PLoS Biology, 8, e1000412.

    Article  Google Scholar 

  • Laizure, S. C., Herring, V., Hu, Z. B. S., Witbrodt, K., & Parker, R. B. (2013). The role of human carboxylesterases in drug metabolism: Have we overlooked their importance? Pharmacotherapy, 33(2), 210–222. https://doi.org/10.1002/phar.1194

    Article  CAS  Google Scholar 

  • Lajmanovich, R. C., Attademo, A. M., Lener, G., Cuzziol Boccioni, A. P., Peltzer, P. M., Martinuzzi, C.S., & Repetti, M. R. (2022). Glyphosate and glufosinate ammonium, herbicides commonly used on genetically modified crops, and their interaction with microplastics: Ecotoxicity in anuran tadpoles. Science of the Total Environment, 804, 150177. https://doi.org/10.1016/j.scitotenv.2021.150177

  • Lambert, S., & Wagner, M. (2016). Characterisation of nanoplastics during the degradation of polystyrene. Chemosphere, 145, 265–268. https://doi.org/10.1016/j.chemosphere.2015.11.078

    Article  CAS  Google Scholar 

  • Lechner, A., Keckeis, H., Lumesberger-Loisl, F., Zens, B., Krusch, R., Tritthart, M., Glas, M., & Schludermann, E. (2014). The Danube so colourful: A potpourri of plastic litter outnumbers fish larvae in Europe’s second largest river. Environmental Pollution, 188, 177–181. https://doi.org/10.1016/j.envpol.2014.02.006

    Article  CAS  Google Scholar 

  • Lenfant, N., Hotelier, T., Velluet, E., Bourne, Y., Marchot, P., & Chatonnet, A. (2013). ESTHER, the database of the α/β-hydrolase fold superfamily of proteins: Tools to explore diversity of functions. Nucleic Acids Research, 41, 423–429.

    Article  Google Scholar 

  • Lian, J., Nelson, R., & Lehner, R. (2018). Carboxylesterases in lipid metabolism: From mouse to human. Protein & Cell, 9(2), 178–195.

    Article  CAS  Google Scholar 

  • Liu, Z., Yu, P., Cai, M., Wu, D., Zhang, M., Chen, M., & Zhao, Y. (2019). Effects of microplastics on the innate immunity and intestinal microflora of juvenile Eriocheir sinensis. Science of the Total Environment, 685, 836–846. https://doi.org/10.1016/j.scitotenv.2019.06.265

    Article  CAS  Google Scholar 

  • Ma, J., Niu, X., Zhang, D., Lu, L., Ye, X., Deng, W., & Lin, Z. (2020). High levels of microplastic pollution in aquaculture water of fish ponds in the Pearl River Estuary of Guangzhou, China. Science of the Total Environment, 744, 140679.

  • Mazorra, M. T., Rubiom, J. A., & Blasco, J. (2002). Acid and alkaline phosphatase activities in the clam Scrobicularia plana: Kinetic characteristics and effects of heavy metals. Comparative Biochemistry and Physiology B: Biochemistry and Molecular Biology, 131(2), 241–249.

    Article  CAS  Google Scholar 

  • Nos, D., Navarro, J., Sánchez-Hernández, J. C., & Solé, M. (2020). Tetrabromobisphenol A inhibits carboxylesterase activity of marine organisms from different trophic levels. Chemosphere, 238, 124592. https://doi.org/10.1016/j.chemosphere.2019.124592

    Article  CAS  Google Scholar 

  • Oehlmann, J., Schulte-Oehlmann, U., Kloas, W., Jagnytsch, O., Lutz, I., Kusk, K. O., & Tyler, C. R. (2009). A critical analysis of the biological impacts of plasticizers on wildlife. Philosophical Transactions of the Royal Society B: Biological, 364(1526), 2047–2062. https://doi.org/10.1098/rstb.2008.0242

    Article  CAS  Google Scholar 

  • Oliveira, M., Gravato, C., & Guilhermino, L. (2012). Acute toxic effects of pyrene on Pomatoschistus microps (Teleostei, Gobiidae): Mortality, biomarkers and swimming performance. Ecological Indicators, 19, 206–214. https://doi.org/10.1016/j.ecolind.2011.08.006

    Article  CAS  Google Scholar 

  • Ozaki, H., Sugihara, K., Watanabe, Y., Moriguchi, K., Uramaru, N., Sone, T., & Kitamura, S. (2017). Comparative study of hydrolytic metabolism of dimethyl phthalate, dibutyl phthalate and di (2-ethylhexyl) phthalate by microsomes of various rat tissues. Food and Chemistry Toxicology, 100, 217–224. https://doi.org/10.1016/j.fct.2016.12.019

    Article  CAS  Google Scholar 

  • Pazos, R., Bauer, D. E., & Gómez, N. (2018). Microplastics integrating the coastal planktonic community in the inner zone of the Río de la Plata estuary (South America). Environmental Pollution, 243, 134–142. https://doi.org/10.1016/j.envpol.2018.08.064

    Article  CAS  Google Scholar 

  • PlasticsEurope. (2020). Plastics-The Facts 2020. An analysis of European plastics production, demand, and waste data. Available: https://plasticseurope.org/knowledge-hub/plastics-the-facts-2020/

  • Revel, M., Châtel, A., Perrein-Ettajani, H., Bruneau, M., Akcha, F., Sussarellu, R., & Mouneyrac, C. (2020). Realistic environmental exposure to microplastics does not induce biological effects in the Pacific oyster Crassostrea gigas. Marine Pollution Bulletin, 150, 110627.

    Article  CAS  Google Scholar 

  • Ríos, M. F., Hernández-Moresino, R. D., & Galván, D. E. (2020). Assessing urban microplastic pollution in a benthic habitat of Patagonia Argentina. Marine Pollution Bulletin, 159, 111491.

    Article  Google Scholar 

  • Rochman, C. M., Hoh, E., Kurobe, T., & Teh, S. J. (2013). Ingested plastic transfers hazardous chemicals to fish and induces hepatic stress. Science Reports, 3, 3263. https://doi.org/10.1038/srep03263

    Article  Google Scholar 

  • Sanchez-Hernandez, J. C., del Pino, J. N., & Domínguez, J. (2015). Earthworm-induced carboxylesterase activity in soil: Assessing the potential for detoxification and monitoring organophosphorus pesticides. Ecotoxicology and Environmental Safety, 122, 303–312. https://doi.org/10.1016/j.ecoenv.2015.08.012

    Article  CAS  Google Scholar 

  • Sanchez-Hernandez, J. C., Ríos, J. M., & Attademo, A. M. (2018). Response of digestive enzymes and esterases of ecotoxicological concern in earthworms exposed to chlorpyrifos-treated soils Ecotoxicology, 27(1–2). https://doi.org/10.1007/s10646-018-1914-8

  • Schmieg, H., Huppertsberg, S., Knepper, T. P., Krais, S., Reitter, K., Rezbach, F., & Triebskorn, R. (2020a) Polystyrene microplastics do not affect juvenile brown trout (Salmo trutta af. fario) or modulate effects of the pesticide methiocarb. Environmental Sciences Europe, 32(1), 1–15. https://doi.org/10.1186/s12302-020-00327-4

  • Schmieg, H., Burmester, J. K., Krais, S., Ruhl, A. S., Tisler, S., Zwiener, C., & Triebskorn, R. (2020b). Interacting effects of polystyrene microplastics and the antidepressant amitriptyline on early life stages of brown trout (Salmo trutta af. fario). Water, 12(9), 2361. https://doi.org/10.3390/w12092361

  • Sharifinia, M., Bahmanbeigloo, Z. A., Keshavarzifard, M., Khanjani, M. H., & Lyons, B. P. (2020). Microplastic pollution as a grand challenge in marine research: A closer look at their adverse impacts on the immune and reproductive systems. Ecotoxicology and Environmental Safety, 204, 111109. https://doi.org/10.1016/j.ecoenv.2020.111109

    Article  CAS  Google Scholar 

  • Trestrail, C., Nugegoda, D., & Shimeta, J. (2020). Invertebrate responses to microplastic ingestion: Reviewing the role of the antioxidant system. Science of the Total Environment, 734, 138559. https://doi.org/10.1016/j.scitotenv.2020.138559

    Article  CAS  Google Scholar 

  • Tussellino, M., Ronca, R., Formiggini, F., De Marco, N., Fusco, S., Netti, P. A., & Carotenuto, R. (2015). Polystyrene nanoparticles affect Xenopus laevis development. Journal of Nanopart Research, 17(2), 70. https://doi.org/10.1007/s11051-015-2876-x

    Article  CAS  Google Scholar 

  • Vaira, M., Akmentins, M., Attademo, M., Baldo, D., Barrasso, D., Barrionuevo, S., Céspedez, J., et al. (2012). Categorization of the conservation status of the amphibians of the Argentine Republic. Cuaderno De Herpetologia, 26, 131–159. (in Spanish).

    Google Scholar 

  • Von Moos, N., Burkhardt-Holm, P., & Kohler, A. (2012). Uptake and effects of microplastics on cells and tissue of the blue mussel Mytilus edulis L. after an experimental exposure. Environmental Science and Technology, l46(20), 11327–11335. https://doi.org/10.1021/es302332w

  • Wang, Y., Song R., Li, Y., & Shen, J. (2003) Understanding tapping-mode atomic force microscopy data on the surface of soft block copolymers. Surface Science, 530, 136–148. https://doi.org/10.1016/S0039-6028(03)00388-1

  • Watts, A. J., Urbina, M. A., Corr, S., Lewis, C., & Galloway, T. S. (2015). Ingestion of plastic microfibers by the crab Carcinus maenas and its effect on food consumption and energy balance. Environmental Science and Technology, 49(24), 14597–14604. https://doi.org/10.1021/acs.est.5b04026

    Article  CAS  Google Scholar 

  • Wen, B., Jin, S. R., Chen, Z. Z., Gao, J. Z., Liu, Y. N., Liu, J. H., & Feng, X. S. (2018). Single and combined effects of microplastics and cadmium on the cadmium accumulation, antioxidant defense and innate immunity of the discus fish (Symphysodona equifasciatus). Environmental Pollution, 243, 462–471. https://doi.org/10.1016/j.envpol.2018.09.029

    Article  CAS  Google Scholar 

  • Zhang, W., Ma, X., Zhang, Z., Wang, Y., Wang, J., Wang, J., & Ma, D. (2015). Persistent organic pollutants carried on plastic resin pellets from two beaches in China. Marine Pollution Bulletin, 99(1–2), 28–34. https://doi.org/10.1016/j.marpolbul.2015.08.002

    Article  CAS  Google Scholar 

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Acknowledgements

We thank the Laboratorio de Física de Superficies e Interfaces (LASUI, IFIS-Litoral, CONICET-UNL) for lending us the SPM equipment and P. Felaj for technical support in AFM experiments.

Funding

This study was supported in part by National Agency for Promotion of Science and Technology (PICT 2018 Nº 3293) and Course of Action for Research and Science Promotion (CAI + D-UNL, PICT Nº 50620190100036LI).

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Andres M. Attademo: conception, design, execution (measurement), interpretation, and writing. Rafael C. Lajmanovich: conception, design, execution (sampling), and interpretation. Paola Peltzer: design and interpretation. Ana Paula Cuzziol Boccioni: execution (sampling) and interpretation. Fernanda Simonielo: execution (measurement) and interpretation. Vanina G. Franco: execution (measurement) and interpretation. Mario C.G. Passeggi: interpretation.

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Correspondence to Andrés M. Attademo.

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The animals used in this research have been treated according to the criteria of the ASIH (2004) and with approval by the Animal Ethics Committee of the Facultad de Bioquímica y Ciencias Biológicas (FBCB), Universidad Nacional del Litoral (UNL), Santa Fe, Argentina. http://www.fbcb.unl.edu.ar/pages/investigacion/comite-deetica.php.

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Attademo, A.M., Cuzziol Boccioni, A.P., Peltzer, P.M. et al. Effect of microplastics on the activity of carboxylesterase and phosphatase enzymes in Scinax squalirostris tadpoles. Environ Monit Assess 194, 718 (2022). https://doi.org/10.1007/s10661-022-10322-2

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