Abstract
Urban waste is a complex mixture of different substances, including microplastics and pharmaceuticals and personal care products. Microplastics have a high affinity for hydrophobic substances. One of these substances is triclosan, a bactericide used in a variety of hygiene products. Therefore, microplastics (MPs) may serve as a vector between triclosan and aquatic organisms. The current study sought to evaluate the effects of the interaction between microplastics and triclosan based on a mechanistic approach in which the oyster Crassostrea brasiliana was used as a model. The organisms were exposed to three conditions: the control, microplastic (MP), and microplastic contaminated with triclosan (MPT). The organisms were exposed for 3 or 7 days. After the exposure time, hemolymph was sampled for performing the neutral red retention time assay and, subsequently, the gills, digestive glands, and adductor muscles were dissected for measuring biomarkers responses (EROD, DBF, GST, GPx, GSH, lipid peroxidation, DNA strand breaks, and AChE). Our results demonstrate combined effects of MPs associated with triclosan on oyster physiology and biochemistry, as well as on lysosomal membrane stability. These results contribute to understanding the effects of contaminants of emerging concern and microplastics on aquatic organisms.
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Abessa DMS, Rachid BRF, Moser GAO, Oliveira AJFC (2012) Environmental effects of sewage oceanic disposal by submarine outfall: a review. O Mundo da Saúde 36(4):643–661
Andrews JD (1979) Pelecypoda: Ostreidae. In: Giese AC, Pierse JS (eds) Reproduction of marine invertebrates. Academic Press, New York, pp 293–341
Avio CG, Gorbi S, Milan M, Benedetti M et al (2015) Pollutants bioavailability and toxicological risk from microplastics to marine mussels. Environ Pollut 198:211–222. https://doi.org/10.1016/j.envpol.2014.12.021
Barceló D, Petrovic M (2007) Pharmaceuticals and personal care products (PPCPs) in the environment. Anal Bioanal Chem 387(4):1141–1142. https://doi.org/10.1007/s00216-006-1012-2
Bejgarn S, MacLeod M, Bogdal C, Breitholtz M (2015) Toxicity of leachate from weathering plastics: An exploratory screening study with Nitokra spinipes. Chemosphere 132:114-119. https://doi.org/10.1016/j.chemosphere.2015.03.010
Bila DM, Dezotti M (2003) Fármacos no meio ambiente. Quím Nova 26(4):523–530
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(1–2):248–254
Brandts I, Teles M, Gonçalves AP et al (2018) Effects of nanoplastics on Mytilus galloprovincialis after individual and combined exposure with carbamazepine. Sci Tot Environ 643:775–784. https://doi.org/10.1016/j.scitotenv.2018.06.257
Browne MA, Dissanayake A, Galloway TS et al (2008) Ingested microscopic plastic translocates to the circulatory system of the mussel, Mytilus edulis (L.). Environ Sci Technol 42(13):5026–5031. https://doi.org/10.1021/es800249a
Browne MA, Niven SJ, Galloway TS, Rowland SJ, Thompson RC (2013) Microplastic moves pollutants and additives to worms, reducing functions linked to health and biodiversity. Curr Biol 23(23):2388–2392. https://doi.org/10.1016/j.cub.2013.10.012
Carr SA, Liu J, Tesoro AG (2016) Transport and fate of microplastic particles in wastewater treatment plants. Water Res 91:174–182. https://doi.org/10.1016/j.watres.2016.01.002
Castro FJ, dos Santos DRA, Buongermino CRP et al (2014) Ecotoxicological assessment of four pharmaceuticals compounds through acute toxicity tests. O Mundo da Saúde 38(1):51–55
Catharino MGM, Vasconcellos MBA, Kirschbaum AA et al (2015) Passive biomonitoring study and effect biomarker in oysters Crassostrea brasiliana (Lamark, 1819: Mollusca, Bivalvia) in Santos and Cananéia Estuaries in São Paulo State, Brazil. J Radioanal Nucl Chem 303(3):2297–2302. https://doi.org/10.1007/s10967-014-3720-y
Christo SW, Ivachuk CS, Veronese F (2015) Descrição alimentar e estágio de maturação de Crassostrea brasiliana comercializadas no mercado municipal de Paranaguá, Paraná, Brasil. Braz J Aquat Sci Technol. https://doi.org/10.14210/bjast.v19n2.5794.
Cole M, Lindeque P, Fileman E et al (2013) Microplastic ingestion by zooplankton. Environ Sci Technol 47:6646–6655. https://doi.org/10.1021/es400663f
Cole M, Coppock R, Lindeque PK, Altin D, Reed S, Pond DW, Sorensen L, Galloway TS, Booth AM (2019) Effects of nylon microplastic on feeding, lipid accumulation, and moulting in a Coldwater Copepod. Environ Sci Technol 312:7075–7082. https://doi.org/10.1021/acs.est.9b01853
Cortez FS, Pereira CDS, Santos AR et al (2012) Biological effects of environmentally relevant concentrations of the pharmaceutical Triclosan in the marine mussel Perna perna (Linnaeus, 1758). Environ Poll 168:145–150. https://doi.org/10.1016/j.envpol.2012.04.024
Deblonde T, Cossu-Leguille C, Hartemann P (2011) Emerging pollutants in wastewater: a review of the literature. Int J Hyg Environ Health 214(6):442–448. https://doi.org/10.1016/j.ijheh.2011.08.002
dos Reis IM, Mattos JJ, Garcez RC et al (2015) Histological responses and localization of the cytochrome P450 (CYP2AU1) in Crassostrea brasiliana exposed to phenanthrene. Aquat Toxicol 169:79–89. https://doi.org/10.1016/j.aquatox.2015.10.011
Ellman GL, Courtney KD, Andres-Jr V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):88–95
Espinosa C, Beltrán JMG, Esteban MA, Cuesta A (2018) In vitro effects of virgin microplastics on fish head-kidney leucocyte activities. Environ Pollut 235:30–38. https://doi.org/10.1016/j.envpol.2017.12.054
Farrell P, Nelson K (2013) Trophic level transfer of microplastic: Mytilus edulis (L.) to Carcinus maenas (L.). Environ Pollut 177:1–3. https://doi.org/10.1016/j.envpol.2013.01.046
Fisner M, Taniguchi S, Majer AP et al (2013) Concentration and composition of polycyclic aromatic hydrocarbons (PAHs) in plastic pellets: implications for small-scale diagnostic and environmental monitoring. Mar Pollut Bull 76:349–354. https://doi.org/10.1016/j.marpolbul.2013.09.045
Foley CJ, Feiner ZS, Malinich TD, Höök TO (2018) A meta-analysis of the effects of exposure to microplastics on fish and aquatic invertebrates. Sci Tot Environ 631:550–559. https://doi.org/10.1016/j.scitotenv.2018.03.046
Freitas R, Coppola F, Costa S et al (2019) Does salinity modulates the response of Mytilus galloprovincialis exposed to triclosan and diclofenac? Environ Pollut 251:756–765. https://doi.org/10.1016/j.envpol.2019.04.115
Gagné F, Blaise C (1993) Hepatic metallothionein level and mixed function oxidase activity in fingerling rainbow trout (Oncorhynchus mykiss) after acute exposure to pulp and paper mill effluents. Water Res 27(11):1669–1682
Gagné F, André C, Cejka P et al (2007) Toxicological effects of primary-treated urban wastewaters, before and after ozone treatment, on freshwater mussels (Elliptio complanata). Comp Biochem Phys Part C 145:542–552
GESAMP (2016) Sources, fate and effects of microplastics in the marine environment: part two of a global assessment. In:Kershaw PJ, Rochman CM (eds) IMO/FAO/UNESCO IOC/UNIDO/WMO/IAEA/UN/UNEP/UNDP joint group of experts on the scientific aspects of marine environmental protection. Reports and studies series. GESAMP No. 93, International Maritime Organization, London, p 220
Gomes CHAM, Silva FC, Lopes GR, Melo CMR (2014) The reproductive cycle of the oyster Crassostrea gasar. Braz J Biol 74(4):967–976. https://doi.org/10.1590/1519-6984.04912
Heath RJ, White SW, Rock CO (2001) Lipid biosynthesis as a target for antibacterial agents. Prog Lipid Res 40(6):467–497. https://doi.org/10.1016/S0163-7827(01)00012-1
Keen JH, Habig WH, Jakoby WB (1976) Mechanism for the several activities of the glutathione S-transferases. J Biol Chem 251(20):6183–6188
Kim JW, Ishibashi H, Yamauchi R et al (2009) Acute toxicity of pharmaceutical and personal care products on freshwater crustacean (Thamnocephalus platyurus) and fish (Oryzias latipes). J Toxicol Sci 34(2):227–232. https://doi.org/10.2131/jts.34.227
La Farre M, Pérez S, Kantiani L, Barceló D (2008) Fate and toxicity of emerging pollutants, their metabolites and transformation products in the aquatic environment. Trends Anal Chem 27(11):991–1007. https://doi.org/10.1016/j.trac.2008.09.010
Li J, Zhang K, Zhang H (2018) Adsorption of antibiotics on microplastics. Environ Pollut 237:460–467. https://doi.org/10.1016/j.envpol.2018.02.050
Liu C, Chang VW, Gin KY (2013) Environmental toxicity of PFCs: an enhanced integrated biomarker assessment and structure–activity analysis. Environ Toxicol Chem 32(10):2226–2233. https://doi.org/10.1002/etc.2306
Lowe DM, Moore MN, Evans BM (1992) Contaminant impact on interactions of molecular probes with lysosomes in living hepatocytes from dab Limanda limanda. Mar Ecol Prog Ser 91:135–140
Lowe DM, Fossato VU, Depledge MH (1995) Contaminant-induced lysossomal membrane damage in blood cells of mussels Mytilus galloprovincialis from the Venice Lagoon: an in vitro study. Mar Ecol Prog Ser 129:189–196
Lüchmann KH, Mattos JJ, Siebert MN et al (2011) Biochemical biomarkers and hydrocarbons concentrations in the mangrove oyster Crassostrea brasiliana following exposure to diesel fuel water-accommodated fraction. Aquat Toxicol 105(3):652–660. https://doi.org/10.1016/j.aquatox.2011.09.003
Lüchmann KH, Mattos JJ, Siebert MN et al (2012) Suppressive subtractive hybridization libraries prepared from the digestive gland of the oyster Crassostrea brasiliana exposed to a diesel fuel water-accommodated fraction. Environ Toxicol Chem 31(6):1249–1253. https://doi.org/10.1002/etc.1837
Lüchmann KH, Dafre AL, Trevisan R et al (2014) A light in the darkness: new biotransformation genes, antioxidant parameters and tissue-specific responses in oysters exposed to phenanthrene. Aquat Toxicol 152:324–334. https://doi.org/10.1016/j.aquatox.2014.04.021
Lüchmann KH, Clark MS, Bainy AC et al (2015) Key metabolic pathways involved in xenobiotic biotransformation and stress responses revealed by transcriptomics of the mangrove oyster Crassostrea brasiliana. Aquat Toxicol 166:10–20. https://doi.org/10.1016/j.aquatox.2015.06.012
Machado IC, Maio FDD, Kira CS, Carvalho MDFH (2002) Estudo da ocorrência dos metais pesados Pb, Cd, Hg, Cu, e Zn na ostra de mangue Crassostrea brasiliana do estuário de Cananéia-SP, Brasil. Rev Inst Adolfo Lutz 61(1):13–18
Maranho LA, Pereira CDS, Choueri RB, Cesar A, Gusso-Choueri PK, Torres RJ, Abessa DMS, Morais RD, Mozeto AA, DelValls TA, Martín-Díaz ML (2012) The application of biochemical responses to assess environmental quality of tropical estuaries: field surveys. J Environ Monit 14:2608–2615. https://doi.org/10.1039/C2EM30465A
Maranho LA, Baena-Nogueras RM, Lara-Martín PA (2014) Bioavailability, oxidative stress, neurotoxicity and genotoxicity of pharmaceuticals bound to marine sediments. The use of the polychaete Hediste diversicolor as bioindicator species. Environ Res 134:353–365. https://doi.org/10.1016/j.envres.2014.08.014
Maranho LA, Garrido-Pérez MC, DelValls TA, Martín-Díaz ML (2015) Suitability of standardized acute toxicity tests for marine sediment assessment: pharmaceutical contamination. Water Air Soil Pollut 226(3):65. https://doi.org/10.1007/s11270-014-2273-6
Maranho LA, Fontes MK, Kamimura ASS et al (2017) Exposure to crack cocaine causes adverse effects on marine mussels Perna perna. Mar Poll Bull 123(1–2):410–414. https://doi.org/10.1016/j.marpolbul.2017.08.043
Martínez-Gómez C, Bignell J, Lowe D (2015) Lysosomal membrane stability in mussels. In: ICES techniques in marine environmental sciences, no. 56
Murphy F, Ewins C, Carbonnier F, Quinn B (2016) Wastewater treatment works (WwTW) as a source of microplastics in the aquatic environment. Environ Sci Technol 50(11):5800–5808. https://doi.org/10.1021/acs.est.5b05416
Newton APN, Cadena SMS, Rocha MEM, Carnieri EGS, De Oliveira MBM (2005) Effect of triclosan (TRN) on energy-linked functions of rat liver mitochondria. Toxicol Lett 160(1):49–59. https://doi.org/10.1016/j.toxlet.2005.06.004
Nobre CR, Santana MFM, Maluf A, Cortez FS, Cesar A, Pereira CDS, Turra A (2015) Assessment of microplastic toxicity to embryonic development of the sea urchin Lytechinus variegatus (Echinodermata: Echinoidea). Mar Pollut Bull 92(1):99–104. https://doi.org/10.1016/j.marpolbul.2014.12.050
Ogata Y, Takada H, Mizukawa K et al (2009) International pellet watch: global monitoring of persistent organic pollutants (POPs) in coastal waters. 1. Initial phase data on PCBs, DDTs, and HCHs. Mar Pollut Bull 58:1437–1446. https://doi.org/10.1016/j.marpolbul.2009.06.014
Olive PL (1988) DNA precipitation assay: a rapid and simple method for detecting DNA damage in mammalian cells. Environ Mol Mutagen 11(4):487–495
Oliveira M, Ribeiro A, Hylland K, Guilhermino L (2013) Single and combined effects of microplastics and pyrene on juveniles (0 + group) of the common goby Pomatoschistus microps (Teleostei, Gobiidae). Ecol Indic 34:641–647. https://doi.org/10.1016/j.ecolind.2013.06.019
Pereira CDS, Abessa DMS, Choueri RB, Almagro-Pastor V, Cesar A, Maranho LA, Martín-Díaz ML, Torres RJ, Gusso-Choueri PK, Almeida JE, Cortez FS, Mozeto AA, Silbiger HLN, Sousa ECPM, Del Valls TA, Bainy ACD (2014) Ecological relevance of Sentinels’ biomarker responses: a multi-level approach. Mar Environ Res 96:118–126. https://doi.org/10.1016/j.marenvres.2013.11.002
Pereira CDS, Maranho LA, Cortez FS et al (2016) Occurrence of pharmaceuticals and cocaine in a Brazilian coastal zone. Sci Total Environ 548:148–154. https://doi.org/10.1016/j.scitotenv.2016.01.051
Pinsino A, Bergami E, Della Torre C et al (2017) Amino-modified polystyrene nanoparticles affect signalling pathways of the sea urchin (Paracentrotus lividus) embryos. Nanotoxicology 11(2):201–209. https://doi.org/10.1080/17435390.2017.1279360
Pittura L, Avio CG, Giuliani ME et al (2018) Microplastics as vehicles of environmental PAHs to marine organisms: combined chemical and physical hazards to the Mediterranean mussels, Mytilus galloprovincialis. Front Mar Sci 5:103. https://doi.org/10.3389/fmars.2018.00103
Prata JC, Lavorante BR, Maria da Conceição BSM, Guilhermino L (2018) Influence of microplastics on the toxicity of the pharmaceuticals procainamide and doxycycline on the marine microalgae Tetraselmis chuii. Aquat Toxicol 197:143–152. https://doi.org/10.1016/j.aquatox.2018.02.015
Pusceddu FH (2016) Avaliação do risco ambiental de sedimentos contaminados com triclosan, ibuprofeno e 17α-etinilestradiol empregando invertebrados marinhos bentônicos. Doctoral thesis, São Paulo University
Pusceddu FH, Choueri RB, Pereira CDS et al (2018) Environmental risk assessment of triclosan and ibuprofen in marine sediments using individual and sub-individual endpoints. Environ Pollut 232:274–283. https://doi.org/10.1016/j.envpol.2017.09.046
Reis Filho RW, Luvizotto-Santos R, Vieira EM (2007) Poluentes emergentes como desreguladores endócrinos. J Braz Soc Ecotoxicol 2:283–288
Santana MFM, Moreira FT, Turra A (2017) Trophic transference of microplastics under a low exposure scenario: insights on the likelihood of particle cascading along marine food-webs. Mar Pollut Bull 121(1–2):154–159. https://doi.org/10.1016/j.marpolbul.2017.05.061
Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205
Siebert MN, Mattos JJ, Piazza CE et al (2017) Characterization of ethoxyresorufin O-deethylase activity (EROD) in oyster Crassostrea brasiliana. Comp Biochem Phys Part B Biochem Mol Biol 203:115–121. https://doi.org/10.1016/j.cbpb.2016.10.002
Sies H, Koch OR, Martino E, Boveris A (1979) Increased biliary glutathione disulfide release in chronically ethanol-treated rats. FEBS Lett 103(2):287–290
UNEP (2015) Plastic in Cosmetics, are we polluting the environment through our personal care? Leslie HA. United Nations Environment Programme
Villalaín J, Mateo CR, Aranda FJ, Shapiro S, Micol V (2001) Membranotropic effects of the antibacterial agent triclosan. Arch Biochem Biophys 390(1):128–136. https://doi.org/10.1006/abbi.2001.2356
Von Moos N, Burkhardt-Holm P, Köhler A (2012) Uptake and effects of microplastics on cells and tissue of the blue mussel Mytilus edulis L. after an experimental exposure. Environ Sci Technol 46(20):11327–11335. https://doi.org/10.1021/es302332w
Wang J, Tan Z, Peng J, Qiu Q, Li M (2016) The behaviors of microplastics in the marine environment. Mar Environ Res 113:7–17. https://doi.org/10.1016/j.marenvres.2015.10.014
Wills ED (1987) Evaluation of lipid peroxidation in lipids and biological membranes. In: Snell K, Mullock B (eds) Biochemical toxicology: a practical approach. IRL Press, Washington, pp 127–150
Wu C, Zhang K, Huang X, Liu J (2016) Sorption of pharmaceuticals and personal care products to polyethylene debris. Environ Sci Pollut Res 23(9):8819–8826. https://doi.org/10.1007/s1135
Zarfl C, Matthies M (2010) Are marine plastic particles transport vectors for organic pollutants to the Arctic? Mar Pollut Bull 60(10):1810–1814. https://doi.org/10.1016/j.marpolbul.2010.05.026
Acknowledgements
C. R. Nobre thanks the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for the financial support for this research (FAPESP Grant #2017/12193-9). L. A. Maranho thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the financial support for research (Grant #150934/2017-3). P. K. Gusso–Choueri thanks the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for the financial support (FAPESP Grant #2017/04970-5). D. M. S. Abessa, R. B. Choueri, and C. D. S. Pereira thank CNPq for productivity fellowships.
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Nobre, C.R., Moreno, B.B., Alves, A.V. et al. Effects of Microplastics Associated with Triclosan on the Oyster Crassostrea brasiliana: An Integrated Biomarker Approach. Arch Environ Contam Toxicol 79, 101–110 (2020). https://doi.org/10.1007/s00244-020-00729-8
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DOI: https://doi.org/10.1007/s00244-020-00729-8