Abstract
The aim of this study is to evaluate the exposure effects to copper-doped zinc oxide nanoparticles (Cu–ZnO NPs) on bivalves through physiological and biochemical multi-markers. To achieve this objective, the selected biological material is the bioindicator mussel Mytilus galloprovincialis used as a sentinel species of marine pollution. The filtration and respiration capacity of the mussel was significantly decreased (p < 0.05) following exposure to Cu–ZnO NPs, reaching a minimum in mussels exposed to 100 µg/L. Superoxide dismutase (SOD), catalase (CAT) activities, and malondialdehyde (MDA) levels were increased, and the highest values were recorded after exposure to 100 µg/L of Cu–ZnO NPs. In addition, acetylcholinesterase (AChE) activity was reduced to a minimum following exposure to 100 µg/L of Cu–ZnO NPs. The estimation of the toxicity of Cu–ZnO NPs through physiological parameters showed that the impact depends on the considered chemical compound and its concentration. In addition, results highlight the sensitivity threshold of the antioxidant defense system in mussels and confirm the capacity of these contaminants to generate reactive oxygen species and even disrupt the nervous system. Overall, using an integrative approach combining the physiological and biochemical responses represents a good way to understand the relational profile between contaminants and marine organisms that could be part of biomonitoring programs of coastal ecosystems.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data that support the findings of this study are available on request from the corresponding author (rakia.ayariepkliti@instm.rnrt.tn), upon request.
References
Aebi, H. (1974). Catalase. In H. U. Bergmeyer (Ed.), Methods of enzymatic analysis (pp. 671–684). Academic Press.
Akrami, H., Mirjalili, B. F., Khoobi, M., Nadri, H., Moradi, A., Sakhteman, A., Emami, S., Foroumadi, A., & Shafiee, A. (2014). Indolinone-based acetylcholinesterase inhibitors: Synthesis, biological activity and molecular modeling. European Journal of Medicinal Chemistry, 84, 375–381. https://doi.org/10.1016/j.ejmech.2014.01.017
Anbuselvan, N., & Sridharan, M. (2018). Heavy metal assessment in surface sediments off Coromandel Coast of India: Implication on marine pollution. Marine Pollution Bulletin, 131, 712–726. https://doi.org/10.1016/j.marpolbul.2018.04.074
Andral, B., Galgani, F., Tomasino, C., Bouchoucha, M., Blottiere, C., Scarpato, A., Benedicto, J., Deudero, S., Calvo, M., & Cento, A. (2011). Chemical contamination baseline in the Western basin of the Mediterranean Sea based on transplanted mussels. Archives of Environmental Contamination and Toxicology, 61, 261–271. https://doi.org/10.1007/s00244-010-9599-x
Apeti, D. A., Lauenstein, G. G., Christensen, J. D., Kimbrough, K., Johnson, W. E., Kennedy, M., & Grant, K. G. (2010). A historical assessment of coastal contamination in Birch Harbor, Maine based on the analysis of mussels collected in the 1940s and the Mussel Watch Program. Marine Pollution Bulletin, 60(5), 732–742. https://doi.org/10.1016/j.marpolbul.2009.11.021
Azizi, G., Akodad, M., Baghour, M., Layachi, M., & Moumen, A. (2018). The use of Mytilus spp. mussels as bioindicators of heavy metal pollution in the coastal environment. A review. Journal of Materials and Environmental Sciences, 9, 1170–1181. https://doi.org/10.26872/jmes.2018.9.4.129
Baker, T. J., Tyler, C. R., & Galloway, T. S. (2014). Impacts of metal and metal oxide nanoparticles on marine organisms. Environmental Pollution, 186, 257–271. https://doi.org/10.1016/j.envpol.2013.11.014
Barboza, L. G. A., Vieira, L. R., Branco, V., Carvalho, C., & Guilhermino, L. (2018). Microplastics increase mercury bioconcentration in gills and bioaccumulation in the liver, and cause oxidative stress and damage in Dicentrarchus labrax juveniles. Scientific Reports, 8, 1–9. https://doi.org/10.1038/s41598-018-34125-z
Basti, L., Nagai, S., Watanabe, S., Oda, T., & Tanaka, Y. (2016). Neuroenzymatic activity and physiological energetics in Manila clam, Ruditapes philippinarum, during short-term sublethal exposure to harmful alga, Heterocapsa circularisquama. Aquatic Toxicology, 176, 76–87. https://doi.org/10.1016/j.aquatox.2016.04.011
Bonsignore, M., Manta, D. S., Sharif, E.A.A.-T., D’Agostino, F., Traina, A., Quinci, E. M., Giaramita, L., Monastero, C., Benothman, M., & Sprovieri, M. (2018). Marine pollution in the Libyan coastal area: Environmental and risk assessment. Marine Pollution Bulletin, 128, 340–352. https://doi.org/10.1016/j.marpolbul.2018.01.043
Booij, K., Zegers, B. N., & Boon, J. P. (2002). Levels of some polybrominated diphenyl ether (PBDE) flame retardants along the Dutch coast as derived from their accumulation in SPMDs and blue mussels (Mytilus edulis). Chemosphere, 46, 683–688. https://doi.org/10.1016/s0045-6535(01)00232-6
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254. https://doi.org/10.1006/abio.1976.9999
Buege, J. A., & Aust, S. D. (1978). Microsomal lipid peroxidation. Methods in Enzymology, 52, 302–310. https://doi.org/10.1016/S0076-6879(78)52032-6
Canesi, L., Fabbri, R., Gallo, G., Vallotto, D., Marcomini, A., & Pojana, G. (2010). Biomarkers in Mytilus galloprovincialis exposed to suspensions of selected nanoparticles (Nano carbon black, C60 fullerene, Nano-TiO2, Nano-SiO2). Aquatic Toxicology, 100, 168–177. https://doi.org/10.1016/j.aquatox.2010.04.009
Cesar-Ribeiro, C., Rosa, H. C., Rocha, D. O., Dos Reis, C. G. B., Prado, T. S., Muniz, D. H. C., Carrasco, R., Silva, F. M., Martinelli-Filho, J. E., & Palanch-Hans, M. F. (2017). Light-stick: A problem of marine pollution in Brazil. Marine Pollution Bulletin, 117, 118–123. https://doi.org/10.1016/j.marpolbul.2017.01.055
Cid, A., Picado, A., Correia, J. B., Chaves, R., Silva, H., Caldeira, J., Matos, A. P. A., & Diniz, M. S. (2015). Oxidative stress and histological changes following exposure to diamond nanoparticles in the freshwater Asian clam Corbicula fluminea (Müller, 1774). Journal of Hazardous Materials, 284, 27–34. https://doi.org/10.1016/j.jhazmat.2014.10.055
Coughlan, J. (1969). The estimation of filtering rate from the clearance of suspensions. Marine Biology, 2, 356–358. https://doi.org/10.1007/BF00355716
Da Costa, E. M. (1778). Historia naturalis testaceorum Britanniæ, or, the British conchology; containing the descriptions and other particulars of natural history of the shells of Great Britain and Ireland: illustrated with figures.
Dhull, V., Gahlaut, A., Dilbaghi, N., & Hooda, V. (2013). Acetylcholinesterase biosensors for electrochemical detection of organophosphorus compounds: a review. Biochemistry Research International. https://doi.org/10.1155/2013/731501
Ellman, G., Diane Courtney, K., Andres, V., & Featherstone, R. M. (1961). New and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology, 7, 88–95. https://doi.org/10.1016/0006-2952(61)90145-9
Faraday, M. (1857). On the relations of gold and other metals to light. Proceedings of the Royal Society of London. https://doi.org/10.1098/rspl.1856.0094
Gerhardt, L. C., Jell, G. M. R., & Boccaccini, A. R. (2007). Titanium dioxide (TiO2) nanoparticles filled poly (D, L lactid acid) (PDLLA) matrix composites for bone tissue engineering. Journal of Materials Science: Materials in Medicine, 18, 1287–1298. https://doi.org/10.1007/s10856-006-0062-5
Gioda, C. R., Loro, V. L., Pretto, A., Salbego, J., Dressler, V., & Flores, E. M. (2013). Sublethal zinc and copper exposure affect acetylcholinesterase activity and accumulation in different tissues of Leporinus obtusidens. Bulletin of Environmental Contamination and Toxicology, 90, 12–16. https://doi.org/10.1007/s00128-012-0896-0
Gomes, T., Chora, S., Pereira, C. G., Cardoso, C., & Bebianno, M. J. (2014). Proteomic response of mussels Mytilus galloprovincialis exposed to CuO NPs and Cu2+: An exploratory biomarker discovery. Aquatic Toxicology, 155, 327–336. https://doi.org/10.1016/j.aquatox.2014.07.015
Gomes, T., Pereira, C. G., Cardoso, C., Pinheiro, J. P., Cancio, I., & Bebianno, M. J. (2012). Accumulation and toxicity of copper oxide nanoparticles in the digestive gland of Mytilus galloprovincialis. Aquatic Toxicology, 118, 72–79. https://doi.org/10.1016/j.aquatox.2012.03.017
Gornati, R., Longo, A., Rossi, F., Maisano, M., Sabatino, G., Mauceri, A., Bernardini, G., & Fasulo, S. (2016). Effects of titanium dioxide nanoparticle exposure in Mytilus galloprovincialis gills and digestive gland. Nanotoxicology, 10, 807–817. https://doi.org/10.3109/17435390.2015.1132348
Gottschalk, F., Sonderer, T., Scholz, R. W., & Nowack, B. (2009). Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, fullerenes) for different regions. Environmental Science & Technology, 43, 9216–9222. https://doi.org/10.1021/es9015553
He, S. B., Wu, G. W., Deng, H. H., Liu, A. L., Lin, X. H., Xia, X. H., & Chen, W. (2014). Choline and acetylcholine detection based on peroxidase-like activity and protein antifouling property of platinum nanoparticles in bovine serum albumin scaffold. Biosensors and Bioelectronics, 62, 331–336. https://doi.org/10.1016/j.bios.2014.07.005
Holas, O., Musilek, K., Pohanka, M., & Kuca, K. (2012). The progress in the cholinesterase quantification methods. Expert Opinion on Drug Discovery, 7, 1207–1223. https://doi.org/10.1517/17460441.2012.729037
Huang, X., Liu, Z., Xie, Z., Dupont, S., Huang, W., Wu, F., Kong, H., Liu, L., Sui, Y., & Lin, D. (2018). Oxidative stress induced by titanium dioxide nanoparticles increases under seawater acidification in the thick shell mussel Mytilus coruscus. Marine Environmental Research, 137, 49–59. https://doi.org/10.1016/j.marenvres.2018.02.029
Islam, M. S., & Tanaka, M. (2004). Impacts of pollution on coastal and marine ecosystems including coastal and marine fisheries and approach for management: A review and synthesis. Marine Pollution Bulletin, 48, 624–649. https://doi.org/10.1016/j.marpolbul.2003.12.004
Khan, I., Saeed, K., & Khan, I. (2019). Nanoparticles: Properties, applications and toxicities. Arabian Journal of Chemistry, 12(7), 908–931. https://doi.org/10.1016/j.arabjc.2017.05.011
Leite, C., Coppola, F., Monteiro, R., Russo, T., Polese, G., Lourenço, M. A., Silva, M. R., Ferreira, P., Soares, A. M., & Freitas, R. (2020). Biochemical and histopathological impacts of rutile and anatase (TiO2 forms) in Mytilus galloprovincialis. Science of the Total Environment, 719, 134886. https://doi.org/10.1016/j.scitotenv.2019.134886
Luo, Z., Wang, Z., Li, Q., Pan, Q., Yan, C., & Liu, F. (2011). Spatial distribution, electron microscopy analysis of titanium and its correlation to heavy metals: Occurrence and sources of titanium nanomaterials in surface sediments from Xiamen Bay, China. Journal of Environmental Monitoring, 13, 1046–1052. https://doi.org/10.1039/C0EM00199F
Manduzio, H., Monsinjon, T., Rocher, B., Leboulenger, F., & Galap, C. (2003). Characterization of an inducible isoform of the Cu/Zn superoxide dismutase in the blue mussel Mytilus edulis. Aquatic Toxicology, 64, 73–83. https://doi.org/10.1016/S0166-445X(03)00026-2
Marklund, S., & Marklund, G. (1974). Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. European Journal of Biochemistry, 47, 469. https://doi.org/10.1111/j.1432-1033.1974.tb03714.x
Marquardt, C., Fritsch-Decker, S., Al-Rawi, M., Diabaté, S., & Weiss, C. (2017). Autophagy induced by silica nanoparticles protects RAW264. 7 macrophages from cell death. Toxicology, 379, 40–47. https://doi.org/10.1016/j.tox.2017.01.019
Pacheco, A., Martins, A., & Guilhermino, L. (2018). Toxicological interactions induced by chronic exposure to gold nanoparticles and microplastics mixtures in Daphnia magna. Science of the Total Environment, 628, 474–483. https://doi.org/10.1016/j.scitotenv.2018.02.081
Palmberg, C., Dernis, H., & Miguet, C. (2009). "Nanotechnology: an overview based on indicators and statistics", OECD Science, Technology and Industry Working Papers, 2009/07, OECD Publishing. https://doi.org/10.1787/223147043844
Pan, J. F., Buffet, P. E., Poirier, L., Amiard-Triquet, C., Gilliland, D., Joubert, Y., Pilet, P., Guibbolini, M., de Faverney, C. R., Roméo, M., Valsami-Jones, E., & Mouneyrac, C. (2012). Size dependent bioaccumulation and ecotoxicity of gold nanoparticles in an endobenthic invertebrate: The Tellinid clam Scrobicularia plana. Environmental Pollution, 168, 37–43. https://doi.org/10.1016/j.envpol.2012.03.051
Renault, S., Baudrimont, M., Mesmer-Dudons, N., Gonzalez, P. M., Mornet, S., & Brisson, A. (2008). Impacts of gold nanoparticle exposure on two freshwater species: A phytoplanktonic alga (Scenedesmus subspicatus) and a benthic bivalve (Corbicula fluminea). Gold Bulletin, 41, 116–126. https://doi.org/10.1007/BF03216589
Roma, J., Matos, A. R., Vinagre, C., & Duarte, B. (2020). Engineered metal nanoparticles in the marine environment: A review of the effects on marine fauna. Marine Environmental Research, 161, 105110. https://doi.org/10.1016/j.marenvres.2020.105110
Saidani, W., Sellami, B., Khazri, A., Mezni, A., Dellali, M., Joubert, O., Sheehan, D., & Beyrem, H. (2019). Metal accumulation, biochemical and behavioral responses on the Mediterranean clams Ruditapes decussatus exposed to two photocatalyst nanocomposites (TiO2 NPs and AuTiO2NPs). Aquatic Toxicology, 208, 71–79. https://doi.org/10.1016/j.aquatox.2019.01.003
Schallreuter, K. U., Gibbons, N. C., Elwary, S. M., Parkin, S. M., & Wood, J. M. (2007). Calcium-activated butyrylcholinesterase in human skin protects acetylcholinesterase against suicide inhibition by neurotoxic organophosphates. Biochemical and Biophysical Research Communications, 355, 1069–1074.
Sellami, B., Mezni, A., Khazri, A., Bouzidi, I., Saidani, W., Sheehan, D., & Beyrem, H. (2017). Toxicity assessment of ZnO-decorated Au nanoparticles in the Mediterranean clam Ruditapes decussatus. Aquatic Toxicology, 188, 10–19. https://doi.org/10.1016/j.aquatox.2017.04.005
Stara, A., Pagano, M., Capillo, G., Fabrello, J., Sandova, M., Albano, M., et al. (2020). Acute effects of neonicotinoid insecticides on Mytilus galloprovincialis: A case study with the active compound thiacloprid and the commercial formulation calypso 480 SC. Ecotoxicology and Environmental Safety, 203, 110980. https://doi.org/10.1016/j.ecoenv.2020.110980
Sun, P., Li, K., Yi, S., Li, H., & Chen, X. (2022). Effects of silver nanoparticles on denitrification and associated N2O release in estuarine and marine sediments. Journal of Ocean University of China, 21(1), 131–140. https://doi.org/10.1007/s11802-021-4888-3
Takano, H., Zou, Y., Hasegawa, H., Akazawa, H., Nagai, T., & Komuro, I. (2003). Oxidative stress-induced signal transduction pathways in cardiac myocytes: Involvement of ROS in heart diseases. Antioxidants and Redox Signaling, 5, 789–794. https://doi.org/10.1089/152308603770380098
Thunberg, C. P. (1793). Tekning och Beskrifning på en stor Ostronsort ifrån Japan. Kongliga Vetenskaps Academiens Nya Handlingar, 14(4–6), 140–142.
Tomaszewski, J. E., McLeod, P. B., & Luthy, R. G. (2008). Measuring and modeling reduction of DDT availability to the water column and mussels following activated carbon amendment of contaminated sediment. Water Research, 42, 4348–4356. https://doi.org/10.1016/j.watres.2008.07.016
Trevisan, R., Delapedra, G., Mello, D. F., Arl, M., Schmidt, É. C., Meder, F., Monopoli, M., Cargnin-Ferreira, E., Bouzon, Z. L., & Fisher, A. S. (2014). Gills are an initial target of zinc oxide nanoparticles in oysters Crassostrea gigas, leading to mitochondrial disruption and oxidative stress. Aquatic Toxicology, 153, 27–38. https://doi.org/10.1016/j.aquatox.2014.03.018
Urban-Malinga, B., Wodzinowski, T., Witalis, B., Zalewski, M., Radtke, K., & Grygiel, W. (2018). Marine litter on the seafloor of the southern Baltic. Marine Pollution Bulletin, 127, 612–617. https://doi.org/10.1016/j.marpolbul.2017.12.052
Wegner, A., Besseling, E., Foekema, E. M., Kamermans, P., & Koelmans, A. A. (2012). Effects of nanopolystyrene on the feeding behavior of the blue mussel (Mytilus edulis L.). Environmental Toxicology and Chemistry, 31(11), 2490–2497. https://doi.org/10.1002/etc.1984
Xia, B., Zhu, L., Han, Q., Sun, X., Chen, B., & Qu, K. (2017). Effects of TiO2 nanoparticles at predicted environmental relevant concentration on the marine scallop Chlamys farreri: An integrated biomarker approach. Environmental Toxicology and Pharmacology, 50, 128–135. https://doi.org/10.1016/j.etap.2017.01.016
Yip, Y. J., Lee, S. S. C., Neo, M. L., Teo, S. L. M., & Valiyaveettil, S. (2022). A comparative investigation of toxicity of three polymer nanoparticles on acorn barnacle (Amphibalanus amphitrite). Science of the Total Environment, 806, 150965. https://doi.org/10.1016/j.scitotenv.2021.150965
Acknowledgements
This study was partly supported by Faculty of Sciences of Bizerte, University of Carthage, Tunisian International Center for Environmental Technologies and the National Institute of Marine Sciences and Technologies. The authors are grateful to all teams for their assistance and help.
Author information
Authors and Affiliations
Contributions
I.B. conducts the laboratory work and wrote the main manuscript R.A-K helps in interpreting results and reviewing the manuscript B.H. and B.S. laboratory work and editing K.M. supervisor
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Communicated by Maria Virginia Alves Martins
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Bouzidi, I., Ayari-Kliti, R., Beyrem, H. et al. The response of the Mediterranean mussel Mytilus galloprovincialis (Lamarck, 1819) exposed to copper-doped zinc nanoparticles. J. Sediment. Environ. 9, 135–143 (2024). https://doi.org/10.1007/s43217-023-00161-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s43217-023-00161-7