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Unravelling the suitability of Branchinecta gaini as a potential biomonitor of contaminants of emerging concern in the Antarctic Peninsula region

Published online by Cambridge University Press:  07 June 2022

Marcelo González-Aravena Open the ORCID record for Marcelo González-Aravena [Opens in a new window] ,
Graciela Iturra ,
Alejandro Font ,
César A. Cárdenas ,
Rodolfo Rondon ,
Elisa Bergami Open the ORCID record for Elisa Bergami [Opens in a new window]  and
Ilaria Corsi
Marcelo González-Aravena*
Affiliation:
Departamento Científico, Instituto Antártico Chileno, Punta Arenas, Chile
Graciela Iturra
Affiliation:
Departamento Científico, Instituto Antártico Chileno, Punta Arenas, Chile
Alejandro Font
Affiliation:
Departamento Científico, Instituto Antártico Chileno, Punta Arenas, Chile
César A. Cárdenas
Affiliation:
Departamento Científico, Instituto Antártico Chileno, Punta Arenas, Chile Millennium Institute Biodiversity of Antarctic and Subantarctic Ecosystems (BASE), Santiago, Chile
Rodolfo Rondon
Affiliation:
Departamento Científico, Instituto Antártico Chileno, Punta Arenas, Chile
Elisa Bergami
Affiliation:
Department of Life Sciences, University of Modena and Reggio Emilia, Via Campi 213/D, 41125 Modena, Italy Department of Physical, Earth and Environmental Sciences, University of Siena, Via Mattioli 4, 53100 Siena, Italy
Ilaria Corsi
Affiliation:
Department of Physical, Earth and Environmental Sciences, University of Siena, Via Mattioli 4, 53100 Siena, Italy
*
mgonzalez@inach.cl
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Abstract

The occurrence and impact of contaminants of emerging concerns (CECs) have been investigated in Antarctica much less than in other parts of the world. Although legacy anthropogenic pollutants can reach Antarctica via long-range transport, CECs mainly originate from local sources. Here, we investigated the ability of a freshwater crustacean, the Antarctic fairy shrimp Branchinecta gaini, to cope with nanoscale titanium dioxide (n-TiO2), a widely used pigment in consumer products (e.g. paintings), including those for personal care (e.g. sunscreens). An in vivo acute short-term exposure study (9 h, n-TiO2 concentration range 50–200 μg ml-1) was performed and the expression levels of several genes involved in stress response were evaluated. No effect on the expression of heat-shock protein chaperone genes was found, with the exception of Hsp70a, which was significantly upregulated at 200 μg ml-1 n-TiO2. Similarly, cytochrome P450 was upregulated at 100 and 200 μg ml-1 n-TiO2, while the expression levels of cathepsin L and of antioxidant genes such as superoxide dismutase and glutathione peroxidase were significantly reduced with increasing concentrations of n-TiO2. This study shows for the first time the responsiveness and sensitivity of an Antarctic freshwater crustacean to n-TiO2 exposure and supports its suitability as a biomonitor of CECs in Antarctica.

Keywords

biomonitoringecotoxicitygene expressiontitanium dioxide nanoparticles
Type
Biological Sciences
Information
Antarctic Science , Volume 34 , Issue 4 , August 2022 , pp. 281 - 288
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of Antarctic Science Ltd

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References

Al-Kattan, A., Wichser, A., Vonbank, R., Brunner, S., Ulrich, A., Zuin, S. & Nowack, B. 2013. Release of TiO2 from paints containing pigment-TiO2 or nano-TiO2 by weathering. Environmental. Science: Processes & Impacts, 15, 2186–2193.Google ScholarPubMed
Ates, M., Daniels, J., Arslan, Z. & Farah, I. 2013. Effects of aqueous suspensions of titanium dioxide nanoparticles on Artemia salina: assessment of nanoparticle aggregation, accumulation and toxicity. Environmental Monitoring Assessment, 185, 3339–3348.CrossRefGoogle ScholarPubMed
Aueviriyavit, S., Phummiratch, D., Kulthong, K. & Maniratanachote, R. 2012. Titanium dioxide nanoparticles-mediated in vitro cytotoxicity does not induce Hsp70 and Grp78 expression in human bronchial epithelial A549 cells. Biological Trace Element Research, 149, 123–132.CrossRefGoogle Scholar
Baker, T.J., Tyler, C.R. & Galloway, T.S. 2014. Impacts of metal and metal oxide nanoparticles on marine organisms. Environmental Pollution (Barking, Essex: 1987), 186, 257–271.CrossRefGoogle ScholarPubMed
Baldwin, W.S., Marko, P.B. & Nelson, D.R. 2009. The cytochrome P450 (CYP) gene superfamily in Daphnia pulex. BMC Genomics, 10, 169.CrossRefGoogle ScholarPubMed
Bergami, E., Manno, C., Cappello, S., Vannuccini, M.L. & Corsi, I. 2020. Nanoplastics affect moulting and faecal pellet sinking in Antarctic krill (Euphausia superba) juveniles. Environment International, 143, 105999.CrossRefGoogle ScholarPubMed
Bergami, E., Bocci, E., Vannuccini, M.L., Monopoli, M., Salvati, A., Dawson, K.A. & Corsi, I. 2016. Nano-sized polystyrene affects feeding, behavior and physiology of brine shrimp Artemia franciscana larvae. Ecotoxicology and Environmental Safety, 123, 18–25.CrossRefGoogle ScholarPubMed
Bergami, E., Pugnalini, S., Vannuccini, M., Manfra, L., Faleri, C., Savorelli, F., et al. 2017. Long-term toxicity of surface-charged polystyrene nanoplastics to marine planktonic species Dunaliella tertiolecta and Artemia franciscana. Aquatic Toxicology, 189, 159–169.CrossRefGoogle ScholarPubMed
Blasco, J. & Corsi, I. eds. 2019. Ecotoxicology of nanoparticles in aquatic systems, 1st ed. Boca Raton, FL, USA: CRC Press, 290 pp.CrossRefGoogle Scholar
Brunelli, A., Pojana, G., Callegaro, S. & Marcomini, A. 2013. Agglomeration and sedimentation of titanium dioxide nanoparticles (n-TiO2) in synthetic and real waters. Journal of Nanoparticle Research, 15, 1684.CrossRefGoogle Scholar
Butler, A.M., Aiton, A.L. & Warner, A.H. 2001. Characterization of a novel heterodimeric cathepsin L-like protease and cDNA encoding the catalytic subunit of the protease in embryos of Artemia franciscana. Biochemistry and Cell Biology = Biochimie et Biologie Cellulaire, 79, 43–56.CrossRefGoogle ScholarPubMed
Chu, B., Yao, F., Cheng, C., Wu, Y., Mei, Y., Li, X., et al. 2014. The potential role of As-sumo-1 in the embryonic diapause process and early embryo development of Artemia sinica. PLoS ONE, 9, e85343.CrossRefGoogle ScholarPubMed
Clemente, Z., Castro, V.L., Jonsson, C.M. & Fraceto, L.F. 2014. Minimal levels of ultraviolet light enhance the toxicity of TiO2 nanoparticles to two representative organisms of aquatic systems. Journal of Nanoparticle Research, 16, 2559.CrossRefGoogle Scholar
Corsi, I., Bergami, E. & Grassi, G. 2020. Behavior and bio-interactions of anthropogenic particles in marine environment for a more realistic ecological risk assessment. Frontiers in Environmental Science, 8, 60.CrossRefGoogle Scholar
Domínguez-Morueco, N., Moreno-Merino, L., Molins-Delgado, D., Díaz-Cruz, M.S., Aznar-Alemany, Ò., Eljarrat, E., et al. 2021. Anthropogenic contaminants in freshwater from the northern Antarctic Peninsula region. Ambio, 50, 544–559.CrossRefGoogle ScholarPubMed
Dulio, V., van Bavel, B., Brorström-Lundén, E., Harmsen, J., Hollender, J., Schlabach, M., et al. 2018. Emerging pollutants in the EU: 10 years of NORMAN in support of environmental policies and regulations. Environmental Sciences Europe, 30, 5.CrossRefGoogle ScholarPubMed
Emnet, P., Gaw, S., Northcott, G., Storey, B. & Graham, L. 2015. Personal care products and steroid hormones in the Antarctic coastal environment associated with two Antarctic research stations, McMurdo Station and Scott Base. Environmental Research, 136, 331–342.CrossRefGoogle ScholarPubMed
Gbotsyo, Y.A., Rowarth, N.M., Weir, L.K. & MacRae, T.H. 2020. Short-term cold stress and heat shock proteins in the crustacean Artemia franciscana. Cell Stress and Chaperones, 25, 1083–1097.CrossRefGoogle ScholarPubMed
Gondikas, A.P., von der Kammer, F., Reed, R.B., Wagner, S., Ranville, J.F. & Hofmann, T. 2014. Release of TiO2 nanoparticles from sunscreens into surface waters: a one-year survey at the Old Danube Recreational Lake. Environmental Science & Technology, 48, 5415–5422.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Grotti, M., Soggia, F., Lagomarsino, C., Riva, S.D., Goessler, W. & Francesconi, K.A. 2008. Natural variability and distribution of trace elements in marine organisms from Antarctic coastal environments. Antarctic Science, 20, 39–52.CrossRefGoogle Scholar
Hawes, T.C. 2008. Feeding behaviour in the Antarctic fairy shrimp, Branchinecta gaini. Polar Biology, 31, 1287–1289.CrossRefGoogle Scholar
James, M.O. & Boyle, S.M. 1998. Cytochromes P450 in Crustacea. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology, 121, 157–172.Google ScholarPubMed
Kim, H., Kim, J.S. & Lee, Y.M. 2017. Changes in activity and transcription of antioxidant enzymes and heat shock protein 90 in the water flea, Daphnia magna - exposed to mercury. Toxicology Environmental Health Science. 9, 300–308.CrossRefGoogle Scholar
Kim, K.T., Klaine, S.J., Cho, J., Kim, S.-H. & Kim, S.D. 2010. Oxidative stress responses of Daphnia magna exposed to TiO2 nanoparticles according to size fraction. Science of the Total Environment, 408, 2268–2272.CrossRefGoogle Scholar
Klaine, S., Alvarez, P., Batley, G., Fernandez, T., Handy, R., Lyon, D., et al. 2008. Nanomaterials in the environment: behavior, fate, bioavailability, and effects. Environmental Toxicology and Chemistry, 27, 1825–1851.CrossRefGoogle ScholarPubMed
Kögel, T., Bjorøy, Ø., Toto, B., Bienfait, A.M. & Sanden, M. 2020. Micro- and nanoplastic toxicity on aquatic life: determining factors. Science of the Total Environment, 709, 136050.CrossRefGoogle ScholarPubMed
Krasnobaev, A., Ten Dam, G., Boerrigter-Eenling, R., Peng, F., Van Leeuwen, S.P.J., Morley, S.A., et al. 2020. Legacy and emerging persistent organic pollutants in Antarctic benthic invertebrates near Rothera Point, western Antarctic Peninsula. Environmental Science & Technology, 54, 2763–2771.CrossRefGoogle ScholarPubMed
Labille, J., Slomberg, D., Catalano, R., Robert, S., Apers-Tremelo, M.-L., Boudenne, J.-L., et al. 2020. Assessing UV filter inputs into beach waters during recreational activity: a field study of three French Mediterranean beaches from consumer survey to water analysis. Science of the Total Environment, 706, 136010,CrossRefGoogle ScholarPubMed
Le Boulay, C., Sellos, D. & Van Wormhoudt, A. 1998. Cathepsin L gene organization in crustaceans. Gene, 218, 77–84.CrossRefGoogle ScholarPubMed
Libralato, G., Prato, E., Migliore, L., Cicero, A.M. & Manfra, L. 2016. A review of toxicity testing protocols and endpoints with Artemia spp. Ecological Indicators, 69, 35–49.CrossRefGoogle Scholar
Livak, K. & Schmittgen, T. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) method. Methods, 25, 402–408.CrossRefGoogle Scholar
Menze, M.A., Fortner, G., Nag, S. & Hand, S.C. 2010. Mechanisms of apoptosis in Crustacea: what conditions induce versus suppress cell death? Apoptosis, 15, 293–312.CrossRefGoogle ScholarPubMed
Morley, S.A., Abele, D., Barnes, D.K.A., Cárdenas, C.A., Cotté, C., Gutt, J., et al. 2020. Global drivers on Southern Ocean ecosystems: changing physical environments and anthropogenic pressures in an Earth system. Frontiers in Marine Science, 7, 1097.CrossRefGoogle Scholar
Nedbalová, L., Nývlt, D., Lirio, J.M., Kavan, J. & Elster, J. 2017. Current distribution of Branchinecta gaini on James Ross Island and Vega Island. Antarctic Science, 29, 341–342.CrossRefGoogle Scholar
OECD (2004), Test No. 202: Daphnia sp. Acute Immobilisation Test, OECD Guidelines for the Testing of Chemicals, Section 2. Paris, France: OECD Publishing. Available at https://doi.org/10.1787/9789264069947-enGoogle Scholar
Okuda-Shimazaki, J., Takaku, S., Kanehira, K., Sonezaki, S. & Taniguchi, A. 2010. Effects of titanium dioxide nanoparticle aggregate size on gene expression. International Journal of Molecular Sciences, 11, 2383–2392.CrossRefGoogle ScholarPubMed
Peck, L. 2004. Physiological flexibility: the key to success and survival for Antarctic fairy shrimps in highly fluctuating extreme environments. Freshwater Biology, 49, 1195–1205.CrossRefGoogle Scholar
Pfaffl, M.W., Tichopad, A., Prgomet, C. & Neuvians, T.P. 2004. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper - Excel-based tool using pair-wise correlations. Biotechnology Letters, 26, 509–515.CrossRefGoogle ScholarPubMed
Pociecha, A. & Dumont, H. 2008. Life cycle of Boeckella poppei Mrazek and Branchinecta gaini Daday (King George Island, South Shetlands). Polar Biology, 31, 245–248.CrossRefGoogle Scholar
Qiao, Y., Wang, J., Mao, Y., Liu, M., Song, X., Su, Y., et al. 2017. Identification and molecular characterization of cathepsin L gene and its expression analysis during early ontogenetic development of kuruma shrimp Marsupenaeus japonicus. Acta Oceanologica Sinica, 36, 52–60.CrossRefGoogle Scholar
Rewitz, K.F., Styrishave, B., Løbner-Olsen, A. & Andersen, O. 2006. Marine invertebrate cytochrome P450: emerging insights from vertebrate and insects analogies. Comparative Biochemistry and Physiology. Toxicology & Pharmacology: CBP, 143, 363–381.CrossRefGoogle ScholarPubMed
Robichaud, C.O., Uyar, A.E., Darby, M.R., Zucker, L.G. & Wiesner, M.R. 2009. Estimates of upper bounds and trends in nano-TiO2 production as a basis for exposure assessment. Environmental Science & Technology, 43, 4227–4233.CrossRefGoogle ScholarPubMed
Sauvé, S. & Desrosiers, M. 2014. A review of what is an emerging contaminant. Chemistry Central Journal, 8, 15.CrossRefGoogle ScholarPubMed
Scenihr. 2007. Opinion on the scientific aspects of the existing and proposed definitions relating to products of nanoscience and nanotechnologies. Brussels, Belgium: European Commission, 22 pp.Google Scholar
Shah, S.N.A., Shah, Z., Hussain, M. & Khan, M. 2017. Hazardous effects of titanium dioxide nanoparticles in ecosystem. Bioinorganic Chemistry and Applications, 2017, 4101735.CrossRefGoogle ScholarPubMed
Shankar, K. & Mehendale, H.M. 2014. Cytochrome P450. In Encyclopedia of toxicology. Cambridge, MA, USA: Academic Press, 1125–1127.CrossRefGoogle Scholar
Siegert, M., Atkinson, A., Banwell, A., Brandon, M., Convey, P., Davies, B., et al. 2019. The Antarctic Peninsula under a 1.5°c global warming scenario. Frontiers in Environmental Science, 7, 102.CrossRefGoogle Scholar
Slijkerman, D.M.E. & Keur, M. 2018. Sunscreen ecoproducts: product claims, potential effects and environmental risks of applied UV filters. Wageningen, The Netherlands: Wageningen Marine Research, 75 pp.CrossRefGoogle Scholar
Stone, V., Nowack, B., Baun, A., van den Brink, N., von der Kammer, F., Dusinska, M., et al. 2010. Nanomaterials for environmental studies: classification, reference material issues, and strategies for physico-chemical characterisation. Science of the Total Environment, 408, 1745–1754.CrossRefGoogle ScholarPubMed
Thiagarajan, V., Seenivasan, R., Jenkins, D., Chandrasekaran, N. & Mukherjee, A. 2020. Combined effects of nano-TiO2 and hexavalent chromium towards marine crustacean Artemia salina. Aquatic Toxicology, 225, 105541.CrossRefGoogle ScholarPubMed
Tovar-Sánchez, A., Sánchez-Quiles, D., Basterretxea, G., Benedé, J.L., Chisvert, A., Salvador, A., et al. 2013. Sunscreen products as emerging pollutants to coastal waters. PLoS ONE, 8, e65451.CrossRefGoogle ScholarPubMed
Varó, I., Perini, A., Torreblanca, A., Garcia, Y., Bergami, E., Vannuccini, M.L. & Corsi, I. 2019. Time-dependent effects of polystyrene nanoparticles in brine shrimp Artemia franciscana at physiological, biochemical and molecular levels. Science of the Total Environment, 675, 570–580.CrossRefGoogle ScholarPubMed
Yang, G., Wang, J., Luo, T. & Zhang, X. 2019. White spot syndrome virus infection activates caspase 1-mediated cell death in crustacean. Virology, 528, 37–47.CrossRefGoogle ScholarPubMed
Zhang, W., Liu, Z., Tang, S., Li, D., Jiang, Q. & Zhang, T. 2020. Transcriptional response provides insights into the effect of chronic polystyrene nanoplastic exposure on Daphnia pulex. Chemosphere, 238, 124563.CrossRefGoogle ScholarPubMed
Ziental, D., Czarczynska-Goslinska, B., Mlynarczyk, D.T., Glowacka-Sobotta, A., Stanisz, B., Goslinski, T. & Sobotta, L. 2020. Titanium dioxide nanoparticles: prospects and applications in medicine. Nanomaterials, 10, 387.CrossRefGoogle ScholarPubMed
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