Genotoxic Testing of Titanium Dioxide Nanoparticles in Far Eastern Mussels, Mytilus Trossulus

Document Type: Original Research Paper

Authors

1 V.I. Il’icev Pacific Oceanological Institute, Far Eastern Branch, Russian Academy of Sciences, Vladivostok 690041, Russia

2 A.V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok 690041, Russia

Abstract

Manufactured nanoparticles (NP) have caused extreme concern about their ecotoxicological effects on the marine systems. In this study, we investigated the biological effects (oxidative stress and genotoxic response) of TiO2-NP at predicted environmental relevant concentrations (0.2 mg/l and 1 mg/l) on marine mussel Mytilus trossulus a dominant member of the far eastern coastal community. The results of the experiment revealed that TiO2-NP when suspended in seawater, formed agglomerates ranging from 400 nm to several μm in diameter. However, TiO2-NP caused obviously oxidative damage on the mussel as evidenced by the significant elevated levels of malondialdehyde (MDA) in the gill and digestive gland. The genotoxic potential of TiO2-NP was assessed by comet assay, which detect primary DNA damage. The gill and digestive gland cells showed significantly enhanced DNA damage for both concentrations of TiO2-NP compared to the control group. These results propose that the TiO2-NP are entering the marine coastal waters can cause genotoxic effect on mollusks and comet assay can be successfully applied as an effective tool for risk assessment of NP on the marine invertebrates. The findings of this study demonstrate that the aggregation of TiO2-NP does not reduced of NP ecotoxicity, but only changes the biological responses.

Keywords


Abdel-Latifa H.M.R., Dawoodb M.A.O., Menanteau-Ledoubled S. and El-Matboulid M. (2020) Environmental transformation of n-TiO2 in the aquatic systems and their ecotoxicity in bivalve mollusks: A systematic review. Ecotoxicol. Environ. Saf. 200: 110776.
Azizi G., Akodad M., Baghour M., Layachi M. and Moumen A. (2018). The use of Mytilus spp. mussels as bioindicators of heavy metal pollution in the coastal environment. J. Mater. Environ. Sci. 9 (4): Page 1170-1181.
Baker T.J., Tyler C.R. and Galloway T.S. (2014). Impacts of metal and metal oxide nanoparticles on marine organisms. Environ. Pollut. 186: 257-271.
Barmo C., Ciacci C., Canonico B., Fabbri R., Cortese K., Balbi T., Marcomini A., Pojana G., Gallo G. and Canesi L. (2013). In vivo effects of n-TiO2 on digestive gland and immune function of the marine bivalve Mytilus galloprovincialis. Aquat. Toxicol. 132-133: 9-18.
Buege, J.A. and Aust, S.D. (1978). Microsomal lipid peroxidation. Methods Enzymol . 52: 302–310.
Canesi L., Fabbri R., Gallo G., Vallotto D., Marcomini A. and Pojana G. (2010). Biomarkers in Mytilus galloprovincialis exposed to suspensions of selected nanoparticles (Nano carbon black, C60 fullerene, Nano-TiO2, Nano-SiO2). Aquat. Toxicol. 100: 168-177.
Canesi L., Ciacci C., Fabbri R., Marcomini A., Pojana G. and Gallo G. (2012). Bivalve mollusks as a unique target group for nanotoxity. Mar. Environ. Res. 76: 16 -21.
Chen Z., Wang Y., Ba T., Li Y., Pu J., Chen T., Song Y., Gu Y., Qian Q., Yang J. and Jia G. (2014). Genotoxic evaluation of titanium dioxide nanoparticles in vivo and in vitro. Toxicol. Lett. 226: 314-319.
Chelomin V.P., Slobodskova V.V. Zakhartsev M. and Kukla S. (2017). Genotoxic Potential of Copper Oxide Nanoparticles in the Bivalve Mollusk Mytilus trossulus. J. Ocean Univ. China. 16: 339-345.
Collins A.R., Ma A.G. and Duthie S.J. (1995). The kinetics of repair of oxidative DNA damage (strand breaks and oxidised pyrimidines) in human cells. Mutat. Res. 336: 69-77.
D'Agata A., Fasulo S., Dallas L.J., Fisher A.S., Maisano M., Readman J.W. and Jha A.N. (2014). Enhanced toxicity of 'bulk' titanium dioxide compared to 'fresh' and 'aged' nano-TiO2 in marine mussels (Mytilus galloprovincialis). Nanotoxicology. 8: 549-558.
Della Torre C., Balbi T., Grassi G., Frenzilli G., Bernardeschi M., Smerilli A., Guidi P., Canesi L., Nigro M., Monaci F., Scarcelli V., Rocco L., Focardi S., Monopoli M. and Corsi I. (2015). Titanium dioxide nanoparticles modulate the toxicological response to cadmium in the gills of Mytilus galloprovincialis. J. Hazard. Mater. 297: 92-100.
Doyle J.J., Ward J.E. and Mason R. (2015). An examination of the ingestion, bioaccumulation, and depuration of titanium dioxide nanoparticles by the blue mussel (Mytilus edulis) and the eastern oyster (Crassostrea virginica). Mar. Environ. Res. 110: 45-52.
Doyle J.J., Ward J.E. and Mason R. (2016). Exposure of bivalve shellfish to titania nanoparticles under an environmental-spill scenario: Encounter, ingestion and egestion. Journal of the Marine Biological Association of the United Kingdom. 96: 137-149.
Farkas J., Bergum S., Nilsen E.W., Olsen A.J., Salaberria I., Ciesielski T.M., Bączek T., Konieczna L., Salvenmoser W. and Jenssen B.M. (2015). The impact of TiO2 nanoparticles on uptake and toxicity of benzo(a)pyrene in the blue mussel (Mytilus edulis). Sci. Total. Environ. 511: 469-476.
Farrokhpay S. Morris G. E., Fornasiero D. and Self P. (2010). Stabilisation of titania pigment particles with anionic polymeric dispersants. Powder Technology. 202: 143-150.
Pollution, 7(1): 129-140, Winter 2021
139
Galloway T., Lewis C., Dolciotti I., Johnston B.D., Moger J. and Regoli F. (2010). Sublethal toxicity of nanotitanium dioxide and carbon nanotubes in a sediment dwelling marine polychaete. Environ. Pollut. 158: 1748-1755.
Gambardella C., Aluigi M.G., Ferrando S., Gallus L., Ramoino P., Gatti A.M., Rottigni M. and Falugi C. (2013). Developmental abnormalities and changes in cholinesterase activity in sea urchin embryos and larvae from sperm exposed to engineered nanoparticles. Aquat. Toxicol. 130-131: 77-85.
Girardello F., Custódio Leite C., Vianna Villela I., da Silva Machado M., Luiz Mendes Juchem A., Roesch-Ely M., Neves Fernandes A., Salvador M. and Antonio Pêgas Henriques J. (2016). Titanium dioxide nanoparticles induce genotoxicity but not mutagenicity in golden mussel Limnoperna fortunei. Aquat. Toxicol. 170: 223-228.
Gomes T., Araújo O., Pereira R., Almeida A.C., Cravo A. and Bebianno M.J. (2013). Genotoxicity of copper oxide and silver nanoparticles in the mussel Mytilus galloprovincialis. Mar. Environ. Res. 84: 51-59.
Gornati R., Longo A., Rossi F., Maisano M., Sabatino G., Mauceri A., Bernardini G. and Fasulo S. (2016). Effects of titanium dioxide nanoparticle exposure in Mytilus galloprovincialis gills and digestive gland. Nanotoxicology. 10: 807-817.
Han B., Pei Z., Shi L., Wang Q., Li Ch., Zhang B., Su X., Zhang N., Zhou L., Zhao B., Niu Yu. and Zhang R. (2020) TiO2 Nanoparticles Caused DNA Damage in Lung and Extra-Pulmonary Organs. Int J Nanomedicine. 15:6279-6294.
Haynes V.N., Ward J.E., Russell B.J. and Agrios A.G. (2017). Photocatalytic effects of titanium dioxide nanoparticles on aquatic organisms—Current knowledge and suggestions for future research. Aquat. toxicol. 185: 138-148.
Hou J., Wang L., Wang Ch., Liu H., Li Sh. and Wang X. (2019) Toxicity and mechanisms of action of titanium dioxide nanoparticles in living organisms. J. Environ. Sci. 75: 40-53.
Huang X., Liu Z., Xie Z., Dupont S., Huang W., Wu F., Kong H., Liu L., Sui Y., Lin D., Lu W., Hu M. and Wang Y. (2018). Oxidative stress induced by titanium dioxide nanoparticles increases under seawater acidification in the thick shell mussel Mytilus coruscus. Mar. Environ. Res. 137: 49-59.
Jugan M.L., Barillet S., Simon-Deckers A., Herlin-Boime N., Sauvaigo S., Douki T. and Carriere M. (2012) Titanium dioxide nanoparticles exhibit genotoxicity and impair DNA repair activity in A549 cells. Nanotoxicol. 6: 501 – 513.
Li N., Ma L., Wang J., Zheng L., Liu J., Duan Y., Liu H., Zhao X., Wang S., Wang H., Hong F. and Xie Y. (2010). Interaction Between Nano-Anatase TiO(2) and Liver DNA from Mice In Vivo. Nanoscale Res. Lett. 5: 108-115.
Marisa I., Matozzo V., Martucci A., Franceschinis E., Brianese N. and Marin M.G. (2018). Bioaccumulation and effects of titanium dioxide nanoparticles and bulk in the clam Ruditapes philippinarum. Mar Environ Res. 136: 179-189.
Matranga V, Corsi I. (2012). Toxic effects of engineered nanoparticles in the marine environment: model organisms and molecular approaches. Mar Environ Res. 76: 32-40.
Mitchelmore C.L. and Chipman J.K. (1998). Detection of DNA strand breaks in brown trout (Salmo trutta) hepatocytes and blood cells using the single cell gel electrophoresis (comet) assay. Aquat. Toxicol. 41: 161-182.
Miller R.J., Bennett S., Keller A.A., Pease S. and Lenihan H.S. (2012). TiO2 nanoparticles are phototoxic to marine phytoplankton. PLoS One. 7: e30321..
Mueller N. and Nowack B. (2008). Exposure Modeling of Engineered Nanoparticles in the Environment. Environ. Sci. Technol. 42: 4447–4453.
Owen R. and Depledge M. (2005). Nanotechnology and the environment: risks and rewards. Mar. Pollut. Bull. 50: 609-612.
Patel S., Patel P. and Bakshi S.R. (2017). Titanium dioxide nanoparticles: an in vitro study of DNA binding, chromosome aberration assay, and comet assay. Cytotechnology. 69: 245-263.
Reeves J.F., Davies S.J., Dodd N.J. and Jha A.N. (2008). Hydroxyl radicals (*OH) are associated with titanium dioxide (TiO(2)) nanoparticle-induced cytotoxicity and oxidative DNA damage in fish cells. Mutat. Res. 640: 113-122.
Rocco L., Santonastaso M., Nigro M., Mottola F., Costagliola D., Bernardeschi M., Guidi P., Lucchesi P., Scarcelli V., Corsi I., Stingo V. and Frenzilli G. (2015). Genomic and chromosomal damage in the marine mussel Mytilus galloprovincialis: Effects of the combined exposure to titanium dioxide nanoparticles and cadmium chloride. Mar. Environ. Res. 111: 144-148.
Roma J., Matos A., Vinagre C. and Duarte B. (2020) Engineered metal nanoparticles in the
Kukla, S., et al.
Pollution is licensed under a "Creative Commons Attribution 4.0 International (CC-BY 4.0)"
140
marine environment: A review of the effects on marine fauna. Mar. Environ. Res. 161: 105-110.
Mottola F., Iovine C., Santonastaso M., Romeo M-L., Pacifico S., Cobellis L. and Rocco L. (2019) NPs-TiO2 and Lincomycin Coexposure InducesDNA Damage in Cultured Human Amniotic Cells. Nanomaterials. 9(11): 1511.
Saidania W., Sellamib B., Khazria A., Meznic A., Dellalia M., Joubertd O., Sheehane D. and Beyrema H. (2019). Metal accumulation, biochemical and behavioral responses on the Mediterranean clams Ruditapes decussatus exposed to two photocatalyst nanocomposites (TiO2 NPs and AuTiO2NPs). Aquat. Toxicol. 208: 71–79.
Shukla R.K., Sharma V., Pandey A.K., Singh S., Sultana S. and Dhawan A. (2011). ROS-mediated genotoxicity induced by titanium dioxide nanoparticles in human epidermal cells. Toxicol. in Vitro. 2: 231-241.
Skocaj M., Filipic M., Petkovic J. and Novak S. (2011) Titanium dioxide in our everyday life; is it safe? Radiol. Oncol. 45: 227-247.
Slobodskova, V. V., Solodova, E. E., Slinko, E. N. and Chelomin,V. P. (2010). Evaluation of thegenotoxicity of cadmium in gill cells of the clam Corbicula japonica using the comet assay. Russ. J. Mar. Biol. 36: 311-315.
Slobodskova, V. V., Zhuravel, E. V., Kukla, S. P. and Chelomin, V. P. (2019). Evaluation of DNA Damage in the Marine Mussel Crenomytilus grayanus as a Genotoxic Biomarker of Pollution. J. Ocean Univ. China 18, 159–164.
Sureda A., Capó X., Busquets-Cortés C. and Tejada S. (2018). Acute exposure to sunscreen containing titanium induces an adaptive response and oxidative stress in Mytillus galloprovincialis. Ecotoxicol. Environ. Saf. 149: 58-63.
Tedesco S., Doyle H., Blasco J., Redmond G. and Sheehan D. (2010). Oxidative stress and toxicity of gold nanoparticles in Mytilus edulis. Aquat. Toxicol. 100: 178-186.
Tiede K., Hassellöv M., Breitbarth E., Chaudhry Q. and Boxall A.B. (2009). Considerations for environmental fate and ecotoxicity testing to support environmental risk assessments for engineered nanoparticles. J. Chromatogr. A. 1216: 503-509.
Vevers W.F. and Jha A.N. (2008). Genotoxic and cytotoxic potential of titanium dioxide (TiO2) nanoparticles on fish cells in vitro. Ecotoxicology. 17: 410-420.
Vignardi C.P., Hasue F.M., Sartório P.V., Cardoso C.M., Machado A.S., Passos M.J., Santos T.C., Nucci J.M., Hewer T.L., Watanabe I.S., Gomes V. and Phan N.V. (2015). Genotoxicity, potential cytotoxicity and cell uptake of titanium dioxide nanoparticles in the marine fish Trachinotus carolinus (Linnaeus, 1766). Aquat. Toxicol. 158: 218-229.
Wang Z., Xia B., Chen B., Sun X., Zhu L., Zhao J., Du P. and Xing B. (2017). Trophic transfer of TiO2 nanoparticles from marine microalga (Nitzschia closterium) to scallop (Chlamys farreri) and related toxicity. Environ. Sci.: Nano. 4: 415-424.
Wanga T., Huanga X., Jianga X., Hua M., Huang W. and Wanga Y. (2019). Differential in vivo hemocyte responses to nano titanium dioxide in mussels: Effects of particle size. Aquat. Toxicol. 212: 28–36.
Ward J.E. and Kach D.J. (2009). Marine aggregates facilitate ingestion of nanoparticles by suspension-feeding bivalves. Mar. Environ. Res. 68: 137-142.
Westerhoff P., Song G., Hristovski K. and Kiser M.A. (2011). Occurrence and removal of titanium at full scale wastewater treatment plants: implications for TiO2 nanomaterials. J. Environ. Monit. 13: 1195-1203.
Xia B., Zhu L., Han Q., Sun X., Chen B. and Qu K. (2017). Effects of TiO2 nanoparticles at predicted environmental relevant concentration on the marine scallop Chlamys farreri: An integrated biomarker approach. Environ. Toxicol. Pharmacol. 50: 128-135.
Zhu X., Zhou J. and Cai Z. (2011). The toxicity and oxidative stress of TiO2 nanoparticles in marine abalone (Haliotis diversicolor supertexta). Mar. Pollut. Bull. 63: 334-338.