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Toxicity assessment of gold ions and gold nanoparticles to golden perch larvae (Macquaria ambigua)

Part of: Frank Reith memorial issue

Published online by Cambridge University Press:  08 February 2021

Jeremiah Shuster Open the ORCID record for Jeremiah Shuster [Opens in a new window] ,
Maria A.D. Rea ,
Bhanu Nidumolu  and
Anupama Kumar
Jeremiah Shuster*
Affiliation:
The University of Adelaide, School of Biological Sciences, North Terrace, Adelaide, South Australia5005, Australia Commonwealth Scientific and Industry Research Organization: Land and Water, Environmental Protection and Technologies Team, Waite Road PMB2, Urrbrae, South Australia5064, Australia
Maria A.D. Rea
Affiliation:
Commonwealth Scientific and Industry Research Organization: Land and Water, Environmental Protection and Technologies Team, Waite Road PMB2, Urrbrae, South Australia5064, Australia Flinders University, College of Science and Engineering, Sturt Road, Bedford Park, South Australia5042, Australia
Bhanu Nidumolu
Affiliation:
Commonwealth Scientific and Industry Research Organization: Land and Water, Environmental Protection and Technologies Team, Waite Road PMB2, Urrbrae, South Australia5064, Australia
Anupama Kumar
Affiliation:
Commonwealth Scientific and Industry Research Organization: Land and Water, Environmental Protection and Technologies Team, Waite Road PMB2, Urrbrae, South Australia5064, Australia
*
*Author for correspondence: Jeremiah Shuster, Email: [email protected]
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Abstract

Golden perch (Macquaria ambigua) is a freshwater game-fish native to central and southeast Australia. Larvae of this fish species were used in two different types of experiments to evaluate the effects of short-term exposures (up to 6 days) to aqueous gold, 5 nm gold nanoparticles (AuNPs), or 50 nm AuNPs. Relative to the control, increased gold concentrations corresponded with yolk-sac edema (swelling). Larvae exposed to 50 μM of 5 nm AuNPs had yolk-sacs that were ~1.5 times larger resulting in the appearance of bent notochords. After two days of exposure, 100% mortality was observed. Total mortalities were <25% in the other larvae–gold systems, suggesting that these larvae can quickly adapt to the presence of gold. In terms of an oxidative stress response, the larvae from all systems did not express high enzymatic activity. The state of the gold determined how much could be taken up (or immobilised) by a larva. Aqueous gold and 5 nm AuNPs easily pass through cells; therefore, larvae exposed to these forms of gold contained the highest concentrations. Scanning electron microscopy confirmed that cells comprising the epithelium and fins contained AuNPs. Aqueous gold was reduced to nanometre-scale particles within cells. Comparatively, 5 nm AuNPs appeared to be aggregated within cells forming clusters hundreds of nanometres in size. On the contrary, 50 nm AuNPs were not observed within cells but were detected within larvae by (single particle) inductively coupled plasma mass spectroscopy, suggesting that these AuNPs were probably taken up through the mouth or gills. The results of the present study demonstrate that exposure to AuNPs had adverse effects on developing golden perch larvae. Additionally, these effects were dependent on the size of the AuNPs.

Keywords

golden perchoxidative stressgold nanoparticlesgoldbiomineralisation
Type
Article – Frank Reith memorial issue
Information
Mineralogical Magazine , Volume 85 , Issue 1 , February 2021 , pp. 94 - 104
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of The Mineralogical Society of Great Britain and Ireland

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Footnotes

This paper is part of a thematic set in memory of Frank Reith

Guest Associate Editor: Janice Kenney

References

Aebi, H. (1984) Catalase. Methods in Enzymology, 105, 121–126.CrossRefGoogle ScholarPubMed
Alkilany, A.M. and Murphy, C.J. (2010) Toxicity and cellular uptake of gold nanoparticles: What we have learned so far? Journal of Nanoparticle Research, 12, 2313–2333.CrossRefGoogle ScholarPubMed
Basu, S. and Pal, T. (2007) Glutathione-induced aggregation of gold nanoparticles: electromagnetic interactions in a closely packed assembly. Journal of Nanoscience and Nanotechnology, 7, 1904–1910.CrossRefGoogle Scholar
Bhagyaraj, S. M. and Oluwafemi, O.S. (2018) Nanotechnology: The science of the invisible. Pp. 1–18 in: Micro and Nano Technologies – Synthesis of Inorganic Nanomaterials (Bhaygaraj, S.M., Oluwatobi, S.O., Kalarikkal, N. and Thomas, S., editors). Woodhead Publishing, Cambridge, UK.Google Scholar
Bohu, T., Anand, R., Noble, R., Lintern, M., Kaksonen, A.H., Mei, Y., Cheng, K.Y., Deng, X., Veder, J., Bunce, M., Power, M. and Verral, M. (2019) Evidence for fungi and gold redox interaction under Earth surface conditions. Nature Communications, 10, 2290.CrossRefGoogle ScholarPubMed
Bradford, M.M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.CrossRefGoogle Scholar
Brust, M., Walker, M., Bethell, D., Schiffrin, D.J. and Whyman, R.J. (1994) Synthesis of thio derivatised gold nanoparticles in a two-phase liquid/liquid system. Journal of the Chemical Society, Chemical Communications, 7, 801–802.CrossRefGoogle Scholar
Carragher, J.F. and Rees, C.M. (1994) Primary and secondary stress responses in golden perch, Macquariaambigua. Comparative Biochemistry and Physiology, 107A, 49–56.CrossRefGoogle Scholar
Chao, S.J., Huang, C.P., Chen, P.C. and Huang, C. (2017) Teratogenic responses of zebrafish embryos to decabromodiphenyl ether (BDE-209) in the presence of nano-SiO2 particles. Chemosphere, 178, 449–457.CrossRefGoogle ScholarPubMed
Choi, J.S., Kim, R.O., Yoon, S. and Kim, W.K. (2016) Developmental toxicity of zinc oxide nanoparticles to zebrafish (Danio rerio): A transcriptomic analysis. PLoS ONE, 11, e0160763, https://doi.org/10.1371/journal.pone.0160763CrossRefGoogle ScholarPubMed
Chen, Y.S., Hung, Y.C., Lian, I. and Huang, G.S. (2009) Assessment of the in-vitro toxicity of gold nanoparticles. Nanoscale Research Letters, 4, 858–864.CrossRefGoogle Scholar
Chen, X., Li, Q.W. and Wang, X.M. (2014) Gold nanostructures for bioimaging, drug delivery and therapeutics. Pp. 163–176 in: Precious Metals for Biomedical Applications (Baltzer, N. and Copponnex, T., editors). Woodhead Publishing, Cambridge, UK.CrossRefGoogle Scholar
Chen, Z., Wang, Z., Chen, J., Wang, S. and Huang, X. (2012) Sensitive and selective detection of glutathione based on resonance light scattering using sensitive gold nanoparticles as colorimetric probes, Analyst, 137, 3132–3137.CrossRefGoogle ScholarPubMed
Daruich De Souza, C., Nogueira, B.R., Elisa, M. and Rostelato, C.M. (2019) Review of the methodologies used in the synthesis gold nanoparticles by chemical reduction. Journal of Alloys and Compounds, 798, 714–740.CrossRefGoogle Scholar
Drotar, A., Phelps, P. and Fall, R. (1985) Evidence for glutathione peroxidase activities in cultured plant cells. Plant Science, 42, 35–40.CrossRefGoogle Scholar
Dykman, L.A. and Khlebtsov, N.G. (2011) Gold nanoparticles in biology and medicine: Recent advances and prospects. Acta Naturae, 3, 34–55.CrossRefGoogle ScholarPubMed
Feichtmeier, N.S., Walther, P. and Leopold, K. (2015) Uptake, effect, and regeneration of barley plant exposed to gold nanoparticles. Environmental Science and Pollution Research, 22, 8549–8558.CrossRefGoogle Scholar
Ferry, J.L., Craig, P., Hexel, C., Sisco, P., Frey, R., Pennington, P.L., Fulton, M.H., Scott, I.G., Decho, A.W., Kashiwada, S., Murphy, C.J. and Shaw, T.J. (2009) Transfer of gold nanoparticles from the water column to the estuarine food web. Nature Nanotechnology, 4, 441–444.CrossRefGoogle ScholarPubMed
Frens, G. (1973) Controlled nucleation for the regulation of the particle size in monodispersed gold suspensions. Nature Physical Science, 241, 20–22.CrossRefGoogle Scholar
Hanlie, H., Liyun, T., Qiujuan, B. and Yong, Z. (2006) Interface characteristics between colloidal gold and kaolinite surface by XPS. Journal of Wuhan University of Technology – Material Science Edition, 21, 90–93.CrossRefGoogle Scholar
Harris, J.H. and Rowland, S.J, (1996) Family Percichthyidae: Australian freshwater cods and basses. Pp. 150–163 in: Freshwater Fishes of South-Eastern Australia. (McDowall, R.M., editor). Reed, Chatswood, NSW, Australia.Google Scholar
Holmström, K.M. and Finkel, T. (2014) Cellular mechanisms and physiological consequences of redox-dependent signalling. Nature Reviews Molecular Cell Biology, 15, 411–421.CrossRefGoogle ScholarPubMed
Jiang, Y., Huo, S., Mizuhara, T., Das, R., Lee, Y., Hou, S, Moyano, D.F., Duncan, B.D., Liang, X. and Rotello, V.M. (2015) The interplay of size and surface functionality on the cellular uptake of sub-10 nm gold nanoparticles. ACS Nano, 9, 9986–9993.CrossRefGoogle ScholarPubMed
Ju-Nam, Y. and Lead, J.R. (2008) Manufactured nanoparticles: An overview of their chemistry, interactions and potential environmental implications. Science of the Total Environment, 400, 396–414.CrossRefGoogle ScholarPubMed
Khaksar, M., Jolley, D.F., Sekine, R., Vasilev, K., Johannessen, B., Donner, E. and Lombi, E. (2015) In situ chemical transformation of silver nanoparticles along the water-sediment continuum. Environmental Science & Technology, 49, 318–325.CrossRefGoogle ScholarPubMed
Kim, T., Lee, C., Joo, S. and Lee, K. (2008) Kinetics of gold nanoparticle aggregation: Experiments and modelling. Journal of Colloidal and Interface Science, 318, 238–243.CrossRefGoogle Scholar
Liu, M., Li, Q., Liang, L., Li, J., Wang, K., Li, J., Lv, M., Chen, N., Song, H., Lee, J., Shi, J., Wang, L., Lal, R. and Fan, C. (2017) Real-time visualization of clustering and intracellular transport of gold nanoparticles by correlative imaging. Nature Communications, 8, 15646.CrossRefGoogle ScholarPubMed
Lombi, E., Donner, E., Taheri, S., Tavakkoli, E., Jamting, A.K., McClure, S., Naidu, R., Miller, B.W., Scheckel, K.G. and Vasilev, K. (2013) Tranformation of silver/silver chloride nanoparticles during anaerobic treatment of wastewater and post-processing of sewage sludge. Environmental Pollution, 176, 193–197.CrossRefGoogle Scholar
Lu, S.C. (2009) Regulation of glutathione synthesis. Molecular Aspects of Medicine, 30, 42–59.CrossRefGoogle ScholarPubMed
Mallen-Cooper, M., Stuart, I.G., Hides-Pearson, F. and Harris, J.H. (1995) Migration in the Murray River and Assessment of the Torrumbarry Fishway. Final Report for Natural Resources Management Strategy Project N002. NSW Fisheries and CRC for Freshwater Ecology, Cronulla, NSW, Australia.Google Scholar
Masouleh, F.F., Amiri, B.M., Mirvaghefi, A., Ghafoori, H. and Madsen, S.S. (2017) Silver nanoparticles cause osmoregulatory impairment and oxidative stress in Caspian kutum (Rutiluskutum, Kamensky 1901). Environmental Monitoring and Assessment, 189, 1–12.CrossRefGoogle Scholar
Ortego, L., Cardoso, F., Martins, S., Fillat, M.F., Laguna, A., Meireles, M., Villacampa, M.D. and Concepción Gimeno, M. (2014) Strong inhibition of thioredoxin reductase by highly cytotoxic gold(I) complexes. DNA binding study. Journal of Inorganic Biochemistry, 130, 32–37.CrossRefGoogle Scholar
Perala, S.R.K. and Kumar, S. (2013) On the mechanism of metal nanoparticle synthesis in the Brust-Schiffrin method. Langmuir, 29, 9863–9873.CrossRefGoogle ScholarPubMed
Rea, M.A., Shuster, J., Kumar, A., Reith, F. and Stephan, C. (2020) extraction of gold nanoparticles from fish larvae and soils. PerkinElmer Application Notes, 1–5.Google Scholar
Reeves, S.J., Plimer, I.R. and Foster, D. (1999) Exploitation of gold in historic sewage sludge stockpile, Werribee, Australia: Resource evaluation, chemical extraction and subsequent utilization of sludge. Journal of Geochemical Exploration, 65, 141–153.CrossRefGoogle Scholar
Reith, F., Brugger, J., Zammit, C., Nies, D.H. and Southam, G. (2013) Geobiological cycling of gold: From fundamental process understanding to exploration solutions. Minerals, 3, 367–394.CrossRefGoogle Scholar
Reynolds, L.F. (1983) Migration patterns of five fish species in the Murray-Darling river system. Australian Journal of Marine and Freshwater Research, 34, 857–871.CrossRefGoogle Scholar
Sant, K.E. and Timme-laragy, A.R. (2018) Zebrafish as a model for toxicological perturbation of yolk and nutrition in the early embryo. Current Environmental Health Reports, 5, 125–133.CrossRefGoogle ScholarPubMed
Schieber, M. and Chandel, N.S. (2014) ROS function in redox signalling and oxidative stress. Current Biology, 10, R453–R462.CrossRefGoogle Scholar
Shuster, J. and Reith, F. (2018) Reflecting on gold geomicrobiology research: Thoughts and considerations for future endeavours. Minerals, 8, 1–12.CrossRefGoogle Scholar
Shuster, J., Reith, F., Cornelis, G., Parsons, J.E., Parsons, J.M. and Southam, G. (2017) Secondary gold structures: Relics of past biogeochemical transformations and implications for colloidal gold dispersion in subtropical environments. Chemical Geology, 450, 154–164.CrossRefGoogle Scholar
Shuster, J., Southam, G. and Reith, F. (2019) Applications of scanning electron microscopy in geomicrobiology. Pp. 148–165 in: Analytical Geomicrobiology: A Handbook of Instrumental Techniques (Kenney, J.P.L., Veeramani, H. and Alessi, D., editors). Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Smith, I.K., Vierheller, T.L. and Thorne, C.A. (1988) Assay of glutathione reductase in crude tissue homogenates using 5,5’dithiobis(2-nitrobenzoic acid). Analytical Biochemistry, 175, 408–413.CrossRefGoogle Scholar
Townsend, D.M., Tew, K.D. and Tapiero, H. (2003) The importance of glutathione in human disease. Biomedicine and Pharmacotherapy, 57, 145–155.CrossRefGoogle ScholarPubMed
Turkevich, J., Stevenson, P.C. and Hillier, J. (1951) A study of the nucleation and growth processes in the synthesis of colloidal gold. Discussion of the Faraday Society, 11, 55–75.CrossRefGoogle Scholar
Vriens, B., Voegelin, A., Hug, S.J., Kaegi, R., Winkel, L.H.E., Buser, A.M. and Berg, M. (2017) Quantification of element fluxes in wastewaters: A nationwide survey in Switzerland. Environmental Science & Technology, 51, 10943–10953.CrossRefGoogle ScholarPubMed
Westerhoff, P., Lee, S., Yang, Y., Gordon, G.W., Hristovski, K., Halden, R.U. and Herckes, P. (2015) Characterisation, recovery opportunities and valuation of metals in municipal sludge from U.S. wastewater treatment plants nationwide. Environmental Science & Technology, 49, 9479–9488.CrossRefGoogle Scholar
Wu, Y., Zhou, G., Li, H., Liu, W., Wang, T. and Jiang, G. (2010) Effect of silver nanoparticles on the development and histopathology biomarkers of Japanese medaka (Oryziaslatipes) using the partial-life test. Aquatic Toxicology, 100, 160–167.CrossRefGoogle Scholar
Zhang, M., Yang, J., Cai, Z., Feng, Y., Wang, Y., Zhang, D. and Pan, X. (2019) Detection of engineered nanoparticles in aquatic environments: Current status and challenges in enrichment, separation, and analysis. Environmental Science Nano, 6, 709.CrossRefGoogle Scholar
Zhu, L., Letaief, F., Liu, Y., Gervais, F. and Detellier, F. (2009) Clay mineral-supported gold nanoparticles. Applied Clay Science, 43, 439–446.CrossRefGoogle Scholar