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Gold particle geomicrobiology: Using viable bacteria as a model for understanding microbe–mineral interactions

Part of: Frank Reith memorial issue

Published online by Cambridge University Press:  26 February 2021

Santonu Kumar Sanyal  and
Jeremiah Shuster Open the ORCID record for Jeremiah Shuster [Opens in a new window]
Santonu Kumar Sanyal*
Affiliation:
The University of Adelaide, School of Biological Sciences, North Terrace, Adelaide, South Australia5005, Australia Department of Microbiology, Faculty of Life and Earth Sciences, Jagannath University, Dhaka-1100, Bangladesh
Jeremiah Shuster*
Affiliation:
The University of Adelaide, School of Biological Sciences, North Terrace, Adelaide, South Australia5005, Australia Commonwealth Scientific and Industrial Research Organization: Land and Water, Environmental Protection and Technologies Team, Waite Road PMB2, Urrbrae, South Australia5064, Australia
*
*Authors for correspondence: Santonu Kumar Sanyal, Email: santonu@mib.jnu.ac.bd; Jeremiah Shuster, Email: jeremiah.shuster@adelaide.edu.au
*Authors for correspondence: Santonu Kumar Sanyal, Email: santonu@mib.jnu.ac.bd; Jeremiah Shuster, Email: jeremiah.shuster@adelaide.edu.au
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Abstract

The biogeochemical cycling of gold has been proposed from studies focusing on gold particle morphology, surface textures and associated bacteria living on the surface of gold particles. Additionally, it has been suggested that metabolically active bacteria on particles catalyse gold dissolution and gold re-precipitation processes, i.e. fluid–bacterial–mineral interaction within microenvironments surrounding particles. Therefore, the isolation and characterisation of viable bacteria from gold particles can be used as a model to improve the understanding of bacterial–gold interactions. In this study, classical microbiology methods were used to isolate a gold-tolerant bacterium (Acinetobacter sp. SK-43) directly from gold particles. The genome of this isolate contained diverse (laterally acquired) heavy-metal resistance genes and stress tolerance genes, suggesting that gene expression would confer resistance to a wide range of potentially toxic metals that could occur in the surrounding microenvironment. The presence of these genes, along with genes for nutrient cycling under nutrient-limited conditions highlights the genomic capacity of how Acinetobacter sp. SK-43 could survive on gold particles and remain viable. Laboratory experiments demonstrated that this isolate could grow in the presence of soluble gold up to 20 μM (AuCl3) and that >50% of soluble gold was reduced upon exposure. Collectively, these results suggest that Acinetobacter sp. SK-43 (and presumably similar bacteria) could survive the cytotoxic effects of soluble Au from particles undergoing dissolution. This study provides comprehensive insight on the possible bacterial contributions to gold biogeochemical cycling in natural environments.

Keywords

gold particlebiogeochemistryviable bacteriaAcinetobacter spmicrobe–mineral interaction
Type
Article - Frank Reith memorial issue
Information
Mineralogical Magazine , Volume 85 , Issue 1 , February 2021 , pp. 117 - 124
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

Africa, C.J., van Hille, R.P. and Harrison, S.T. (2013) Attachment of Acidithiobacillus ferrooxidans and Leptospirillum ferriphilum cultured under varying conditions to pyrite, chalcopyrite, low-grade ore and quartz in a packed column reactor. Applied Microbiology and Biotechnology, 97, 1317–1324.CrossRefGoogle Scholar
Banfield, J.F., Tyson, G.W., Allen, E.E. and Whitaker, R.J. (2005) The search for a molecular-level understanding of the processes that underpin the Earth's biogeochemical cycles. Pp. 1–7. in: Molecular Geomicrobiology (Banfield, J.F., Cervini-Silva, J. and Nealson, K.H., editors). Reviews in Mineralogy and Geochemistry, 59. Mineralogical Society of America and the Geochemical Society, Chantilly, Virginia, USA.CrossRefGoogle Scholar
Bütof, L., Wiesemann, N., Herzberg, M., Altzschner, M., Holleitner, A., Reith, F. and Nies, D.H. (2018) Synergistic gold–copper detoxification at the core of gold biomineralisation in Cupriavidus metallidurans. Metallomics, 10, 278–286.CrossRefGoogle ScholarPubMed
Carini, P., Marsden, P.J., Leff, J.W., Morgan, E.E., Strickland, M.S. and Fierer, N. (2016) Relic DNA is abundant in soil and obscures estimates of soil microbial diversity. Nature Microbiology, 2, 1–6.Google ScholarPubMed
Correa-Llantén, D.N., Muñoz-Ibacache, S.A., Castro, M.E., Muñoz, P.A. and Blamey, J.M. (2013) Gold nanoparticles synthesized by Geobacillus sp. strain ID17 a thermophilic bacterium isolated from Deception Island, Antarctica. Microbial Cell Factories, 12, 1–6.Google ScholarPubMed
Dubey, A.K., Baker, C.S., Suzuki, K., Jones, A.D., Pandit, P., Romeo, T. and Babitzke, P. (2003) CsrA regulates translation of the Escherichia coli carbon starvation gene, cstA, by blocking ribosome access to the cstA transcript. Journal of Bacteriology, 185, 4450–4460.CrossRefGoogle ScholarPubMed
Falconer, D. and Craw, D. (2009) Supergene gold mobility: a textural and geochemical study from gold placers in southern New Zealand. Economic Geology (Special Publication), 14, 77–93.Google Scholar
Falkowski, P.G., Fenchel, T. and Delong, E.F. (2008) The microbial engines that drive Earth's biogeochemical cycles. Science, 320, 1034–1039.CrossRefGoogle ScholarPubMed
Hough, R., Noble, R., Hitchen, G., Hart, R., Reddy, S., Saunders, M., Clode, P., Vaughan, D., Lowe, J. and Gray, D. (2008) Naturally occurring gold nanoparticles and nanoplates. Geology, 36, 571–574.CrossRefGoogle Scholar
Jaireth, S., Hoatson, D.M. and Miezitis, Y. (2014) Geological setting and resources of the major rare-earth-element deposits in Australia. Ore Geology Reviews, 62, 72–128.CrossRefGoogle Scholar
Kalabegishvili, T.L., Kirkesali, E.I., Rcheulishvili, A.N., Ginturi, E.N., Murusidze, I.G., Pataraya, D.T., Gurielidze, M.A., Tsertsvadze, G.I., Gabunia, V.N. and Lomidze, L.G. (2012) Synthesis of gold nanoparticles by some strains of Arthrobacter genera. Journal of Materials Science Engineering A, 2, 164–173.Google Scholar
Kenney, J.P., Song, Z., Bunker, B.A. and Fein, J.B. (2012) An experimental study of Au removal from solution by non-metabolizing bacterial cells and their exudates. Geochimica et Cosmochimica Acta, 87, 51–60.CrossRefGoogle Scholar
Langley, S. and Beveridge, T. (1999) Metal binding by Pseudomonas aeruginosa PAO1 is influenced by growth of the cells as a biofilm. Canadian Journal of Microbiology, 45, 616–622.CrossRefGoogle ScholarPubMed
Laub, M.T., McAdams, H.H., Feldblyum, T., Fraser, C.M. and Shapiro, L. (2000) Global analysis of the genetic network controlling a bacterial cell cycle. Science, 290, 2144–2148.CrossRefGoogle ScholarPubMed
Mann, A.W. (1984) Mobility of gold and silver in lateritic weathering profiles; some observations from Western Australia. Economic Ecology, 79, 38–49.Google Scholar
Mielke, R.E., Pace, D.L., Porter, T. and Southam, G. (2003) A critical stage in the formation of acid mine drainage: Colonization of pyrite by Acidithiobacillus ferrooxidans under pH-neutral conditions. Geobiology, 1, 81–90.CrossRefGoogle Scholar
Newman, D.K. and Banfield, J.F. (2002) Geomicrobiology: how molecular-scale interactions underpin biogeochemical systems. Science, 296, 1071–1077.CrossRefGoogle ScholarPubMed
Rea, M.A., Zammit, C.M. and Reith, F. (2016) Bacterial biofilms on gold grains-implications for geomicrobial transformations of gold. FEMS Microbiology Ecology, 92, fiw082.CrossRefGoogle Scholar
Rea, M.A., Shuster, J., Hoffmann, V.E., Schade, M., Bissett, A. and Reith, F. (2019a) Does the primary deposit affect the biogeochemical transformation of placer gold and associated biofilms? Gondwana Research, 73, 77–95.CrossRefGoogle Scholar
Rea, M.A.D., Wulser, P.A., Brugger, J., Etschmann, B., Bissett, A., Shuster, J. and Reith, F. (2019b) Effect of physical and biogeochemical factors on placer gold transformation in mountainous landscapes of Switzerland. Gondwana Research, 66, 77–92.CrossRefGoogle Scholar
Reith, F. and McPhail, D. (2007) Mobility and microbially mediated mobilization of gold and arsenic in soils from two gold mines in semi-arid and tropical Australia. Geochimica et Cosmochimica Acta, 71, 1183–1196.CrossRefGoogle Scholar
Reith, F., Rogers, S.L., McPhail, D. and Webb, D. (2006) Biomineralization of gold: biofilms on bacterioform gold. Science, 313, 233–236.CrossRefGoogle ScholarPubMed
Reith, F., Etschmann, B., Grosse, C., Moors, H., Benotmane, M.A., Monsieurs, P., Grass, G., Doonan, C., Vogt, S., Lai, B., Martinez-Criado, G., George, G.N., Nies, D.H., Mergeay, M., Pring, A., Southam, G. and Brugger, J. (2009) Mechanisms of gold biomineralization in the bacterium Cupriavidus metallidurans. Proceedings of the National Academy of Sciences, 106, 17757–17762.CrossRefGoogle ScholarPubMed
Reith, F., Fairbrother, L., Nolze, G., Wilhelmi, O., Clode, P.L., Gregg, A., Parsons, J.E., Wakelin, S.A., Pring, A. and Hough, R. (2010) Nanoparticle factories: Biofilms hold the key to gold dispersion and nugget formation. Geology, 38, 843–846.CrossRefGoogle Scholar
Reith, F., Rea, M.A.D., Sawley, P., Zammit, C.M., Nolze, G., Reith, T., Rantanen, K. and Bissett, A. (2018) Biogeochemical cycling of gold: Transforming gold particles from arctic Finland. Chemical Geology, 483, 511–529.CrossRefGoogle Scholar
Reith, F., Falconer, D., Van Nostrand, J., Craw, D., Shuster, J. and Wakelin, S. (2020) Functional capabilities of bacterial biofilms on gold particles. FEMS Microbiology Ecology, 96, fiz196.CrossRefGoogle ScholarPubMed
Sanyal, S.K., Shuster, J. and Reith, F. (2019a) Biogeochemical gold cycling selects metal-resistant bacteria that promote gold particle transformation. FEMS Microbiology Ecology, 95, fiz078.CrossRefGoogle Scholar
Sanyal, S.K., Shuster, J. and Reith, F. (2019b) Cycling of biogenic elements drives biogeochemical gold cycling. Earth-Science Reviews, 190, 131–147.CrossRefGoogle Scholar
Sanyal, S.K., Brugger, J., Etschmann, B., Pederson, S.M., Delport, P.J., Dixon, R., Tearle, R., Ludington, A., Reith, F. and Shuster, J. (2020a) Metal resistant bacteria on gold particles: Implications of how anthropogenic contaminants could affect natural gold biogeochemical cycling. Science of The Total Environment, 138698.CrossRefGoogle Scholar
Sanyal, S.K., Reith, F. and Shuster, J. (2020b) A genomic perspective of metal-resistant bacteria from gold particles: Possible survival mechanisms during gold biogeochemical cycling. FEMS Microbiology Ecology, 96, fiaa111CrossRefGoogle Scholar
Shuster, J. and Reith, F. (2018) Reflecting on gold geomicrobiology research: thoughts and considerations for future endeavors. Minerals, 8, 401.CrossRefGoogle Scholar
Shuster, J. and Southam, G. (2015) The in-vitro “growth” of gold grains. Geology, 43, 79–82.CrossRefGoogle Scholar
Shuster, J., Bolin, T., MacLean, L.C. and Southam, G. (2014) The effect of iron-oxidising bacteria on the stability of gold (I) thiosulphate complex. Chemical Geology, 376, 52–60.CrossRefGoogle Scholar
Shuster, J., Johnston, C.W., Magarvey, N.A., Gordon, R.A., Barron, K., Banerjee, N.R. and Southam, G. (2015) Structural and chemical characterization of placer gold grains: implications for bacterial contributions to grain formation. Geomicrobiology Journal, 32, 158–169.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) Application 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
Southam, G. and Beveridge, T.J. (1994) The in vitro formation of placer gold by bacteria. Geochimica et Cosmochimica Acta, 58, 4527–4530.CrossRefGoogle Scholar
Turkevich, J., Stevenson, P.C. and Hillier, J. (1951) A study of the nucleation and growth processes in the synthesis of colloidal gold. Discussions of the Faraday Society, 11, 55–75.CrossRefGoogle Scholar
Vuppada, R.K., Hansen, C.R., Strickland, K.A., Kelly, K.M. and McCleary, W.R. (2018) Phosphate signaling through alternate conformations of the PstSCAB phosphate transporter. BMC Microbiology, 18, 1–9.CrossRefGoogle ScholarPubMed
Wakelin, S.A., Anand, R.R., Reith, F., Gregg, A.L., Noble, R.R., Goldfarb, K.C., Andersen, G.L., DeSantis, T.Z., Piceno, Y.M. and Brodie, E.L. (2012) Bacterial communities associated with a mineral weathering profile at a sulphidic mine tailings dump in arid Western Australia. FEMS Microbiology Ecology, 79, 298–311.CrossRefGoogle Scholar
Webster, J. and Mann, A. (1984) The influence of climate, geomorphology and primary geology on the supergene migration of gold and silver. Journal of Geochemical Exploration, 22, 21–42.CrossRefGoogle Scholar
Wiesemann, N., Bütof, L., Herzberg, M., Hause, G., Berthold, L., Etschmann, B., Brugger, J., Martinez-Criado, G., Dobritzsch, D. and Baginsky, S. (2017) Synergistic toxicity of copper and gold compounds in Cupriavidus metallidurans. Applied and Environmental Microbiology, 83, e01679–17.CrossRefGoogle ScholarPubMed
Zammit, C.M., Weiland, F., Brugger, J., Wade, B., Winderbaum, L.J., Nies, D.H., Southam, G., Hoffmann, P. and Reith, F. (2016) Proteomic responses to gold (iii)-toxicity in the bacterium Cupriavidus metallidurans CH34. Metallomics, 8, 1204–1216.CrossRefGoogle ScholarPubMed