Mechanisms of gold biomineralization in the bacterium Cupriavidus metallidurans
- Frank Reitha,b,1,
- Barbara Etschmannc,d,e,
- Cornelia Grossef,
- Hugo Moorsg,
- Mohammed A. Benotmaneg,
- Pieter Monsieursg,
- Gregor Grassh,
- Christian Doonani,
- Stefan Vogtj,
- Barry Laij,
- Gema Martinez-Criadok,
- Graham N. Georgel,
- Dietrich H. Niesf,
- Max Mergeayg,
- Allan Pringc,
- Gordon Southamm and
- Joël Bruggera,c
- aCentre for Tectonics, Resources and Exploration, School of Earth and Environmental Sciences, University of Adelaide, North Terrace, SA 5000, Australia;
- bEnvironmental Biogeochemistry, Commonwealth Scientific and Industrial Research Organisation (CSIRO) Land and Water, PMB2, Glen Osmond, SA5064, Australia;
- cDepartment of Mineralogy, South Australian Museum, Adelaide, SA 5005, Australia;
- dCSIRO Exploration and Mining, c/o Mineralogy, South Australian Museum, Adelaide, SA 5000, Australia;
- eCODES Centre of Excellence, University of Tasmania, TAS 7001 Hobart, Australia;
- fMartin-Luther-Universität Halle-Wittenberg, Institut für Biologie/Mikrobiologie, DE-06120 Halle, Germany;
- gExpertise Group for Molecular and Cellular Biology, Unit for Microbiology, Nuclear Research Centre, Institute for Environment, Health and Safety, Boeretang 200, B-2400 MOL, Belgium;
- hSchool of Biological Sciences, University of Nebraska-Lincoln, Lincoln NE 68588-0666 ;
- iDepartment of Chemistry and Biochemistry, University of California, Los Angeles, CA 90095-1569;
- jAdvanced Photon Source, Argonne National Laboratory, Argonne, IL 60439;
- kExperiments Division, European Synchrotron Radiation Facility, 38043-Grenoble, France;
- lDepartment of Geological Sciences, University of Saskatchewan, 114 Science Place, Saskatoon, S7N 5E2, Canada; and
- mDepartment of Earth Sciences/Department of Biology, University of Western Ontario, London, ON, Canada N6A 5B7
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Edited by Douglas C. Rees, California Institute of Technology, Pasadena, CA, and approved August 27, 2009 (received for review April 29, 2009)
Abstract
While the role of microorganisms as main drivers of metal mobility and mineral formation under Earth surface conditions is now widely accepted, the formation of secondary gold (Au) is commonly attributed to abiotic processes. Here we report that the biomineralization of Au nanoparticles in the metallophillic bacterium Cupriavidus metallidurans CH34 is the result of Au-regulated gene expression leading to the energy-dependent reductive precipitation of toxic Au(III)-complexes. C. metallidurans, which forms biofilms on Au grains, rapidly accumulates Au(III)-complexes from solution. Bulk and microbeam synchrotron X-ray analyses revealed that cellular Au accumulation is coupled to the formation of Au(I)-S complexes. This process promotes Au toxicity and C. metallidurans reacts by inducing oxidative stress and metal resistances gene clusters (including a Au-specific operon) to promote cellular defense. As a result, Au detoxification is mediated by a combination of efflux, reduction, and possibly methylation of Au-complexes, leading to the formation of Au(I)-C-compounds and nanoparticulate Au0. Similar particles were observed in bacterial biofilms on Au grains, suggesting that bacteria actively contribute to the formation of Au grains in surface environments. The recognition of specific genetic responses to Au opens the way for the development of bioexploration and bioprocessing tools.
Footnotes
- 1To whom correspondence should be addressed. E-mail: frank.reith{at}csiro.au
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Author contributions: F.R., C.G., G.G., and J.B. designed research; F.R., B.E., C.G., H.M., C.D., A.P., G.S., and J.B. performed research; M.A.B., S.V., B.L., G.M.-C., G.N.G., D.H.N., G.S., and J.B. contributed new reagents/analytic tools; F.R., B.E., C.G., H.M., P.M., C.D., D.H.N., M.M., A.P., and J.B. analyzed data; and F.R. wrote the paper.
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The authors declare no conflict of interest.
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This article is a PNAS Direct Submission.
