Progressive biogeochemical transformation of placer gold particles drives compositional changes in associated biofilm communities.

Biofilms on placer gold (Au)-particle surfaces drive Au solubilization and re-concentration thereby progressively transforming the particles. Gold solubilization induces Au-toxicity; however, Au-detoxifying community members ameliorates Au-toxicity by precipitating soluble Au to metallic Au. We hypothesize that Au-dissolution and re-concentration (precipitation) place selective pressures on associated microbial communities, leading to compositional changes and subsequent Au-particle transformation. We analyzed Au-particles from eight United Kingdom sites using next generation sequencing, electron microscopy and micro-analyses. Gold particles contained biofilms composed of prokaryotic cells and extracellular polymeric substances intermixed with (bio)minerals. Across all sites communities were dominated by Proteobacteria (689, 97% Operational Taxonomic Units, 59.3% of total reads), with β-Proteobacteria being the most abundant. A wide range of Au-morphotypes including nanoparticles, micro-crystals, sheet-like Au and secondary rims, indicated that dissolution and re-precipitation occurred, and from this transformation indices were calculated. Multivariate statistical analyses showed a significant relationship between the extent of Au-particle transformation and biofilm community composition, with putative metal-resistant Au-cycling taxa linked to progressive Au transformation. These included the genera Pseudomonas, Leptothrix and Acinetobacter. Additionally, putative exoelectrogenic genera Rhodoferax and Geobacter were highly abundant. In conclusion, biogeochemical Au-cycling and Au-particle transformation occurred at all sites and exerted a strong influence on biofilm community composition.

[1]  J. T. Curtis,et al.  An Ordination of the Upland Forest Communities of Southern Wisconsin , 1957 .

[2]  N. Pace,et al.  Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[3]  G. Sayler,et al.  DNA adsorption to soils and sediments. , 1988, Environmental science & technology.

[4]  J. C. Groen,et al.  Gold-rich rim formation on electrum grains in placers , 1990 .

[5]  D. Lane 16S/23S rRNA sequencing , 1991 .

[6]  Adsorption of DNA on clay minerals: protection against DNaseI and influence on gene transfer , 1992 .

[7]  T. Tingle,et al.  An Improved Mean Atomic Number Background Correction for Quantitative Microanalysis , 1996, Microscopy and Microanalysis.

[8]  M. Khanna,et al.  Amplification of DNA bound on clay minerals , 1998 .

[9]  D. Nies,et al.  Microbial heavy-metal resistance , 1999, Applied Microbiology and Biotechnology.

[10]  K. Timmis,et al.  An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. , 2000, Environmental microbiology.

[11]  K. R. Clarke,et al.  A further biodiversity index applicable to species lists: variation in taxonomic distinctness , 2001 .

[12]  S. Karthikeyan,et al.  Pseudomonas aeruginosa biofilms react with and precipitate toxic soluble gold. , 2002, Environmental microbiology.

[13]  M. Styles,et al.  Platinum-group element occurrences in Britain: magmatic, hydrothermal and supergene , 2002 .

[14]  P. Parseval,et al.  Gold grain morphology and composition as an exploration tool: application to gold exploration in covered areas , 2003, Geochemistry: Exploration, Environment, Analysis.

[15]  J. Parnell,et al.  Crystalline Placer Gold from the Rio Neuquén, Argentina: Implications for the Gold Budget in Placer Gold Formation , 2003 .

[16]  D. Lovley,et al.  Electricity generation by direct oxidation of glucose in mediatorless microbial fuel cells , 2003, Nature Biotechnology.

[17]  C. Leang,et al.  Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens. , 2003, The Biochemical journal.

[18]  M. Parsek,et al.  Heavy Metal Resistance of Biofilm and Planktonic Pseudomonas aeruginosa , 2003, Applied and Environmental Microbiology.

[19]  S. E. Fratesi,et al.  Effects of SEM Preparation Techniques on the Appearance of Bacteria and Biofilms in the Carter Sandstone , 2004 .

[20]  Michael D. Abràmoff,et al.  Image processing with ImageJ , 2004 .

[21]  Paul Stoodley,et al.  Bacterial biofilms: from the Natural environment to infectious diseases , 2004, Nature Reviews Microbiology.

[22]  T. Mehta,et al.  Extracellular electron transfer via microbial nanowires , 2005, Nature.

[23]  H. Chen,et al.  Adsorption of DNA on clay minerals and various colloidal particles from an Alfisol , 2006 .

[24]  F. Reith,et al.  Effect of resident microbiota on the solubilization of gold in soil from the Tomakin Park Gold Mine, New South Wales, Australia , 2006 .

[25]  R. Nielsen,et al.  Statistical approaches for DNA barcoding. , 2006, Systematic biology.

[26]  Q. Huang,et al.  Interactions of DNA with clay minerals and soil colloidal particles and protection against degradation by DNase. , 2006, Environmental science & technology.

[27]  F. Reith,et al.  Biomineralization of Gold: Biofilms on Bacterioform Gold , 2006, Science.

[28]  D. Craw,et al.  The geomicrobiology of gold , 2007, The ISME Journal.

[29]  F. C. Soncini,et al.  Bacterial sensing of and resistance to gold salts , 2007, Molecular microbiology.

[30]  F. Reith,et al.  Mobility and microbially mediated mobilization of gold and arsenic in soils from two gold mines in semi-arid and tropical Australia , 2007 .

[31]  H. Ceri,et al.  Multimetal resistance and tolerance in microbial biofilms , 2007, Nature Reviews Microbiology.

[32]  J. Ascher,et al.  Extracellular DNA in soil and sediment: fate and ecological relevance , 2009, Biology and Fertility of Soils.

[33]  Vincent M Rotello,et al.  Electricity generation by Geobacter sulfurreducens attached to gold electrodes. , 2008, Langmuir : the ACS journal of surfaces and colloids.

[34]  Raymond N. Gorley,et al.  PERMANOVA+ for PRIMER. Guide to software and statistical methods , 2008 .

[35]  G. Southam,et al.  The Biogeochemistry of Gold , 2009 .

[36]  Stefan Vogt,et al.  Mechanisms of gold biomineralization in the bacterium Cupriavidus metallidurans , 2009, Proceedings of the National Academy of Sciences.

[37]  Martin Hartmann,et al.  Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities , 2009, Applied and Environmental Microbiology.

[38]  D. Craw,et al.  Supergene gold mobility; a textural and geochemical study from gold placers in southern New Zealand , 2009 .

[39]  J. Shapter,et al.  Effect of the cyanide-producing bacterium Chromobacterium violaceum on ultraflat Au surfaces , 2009 .

[40]  R. Hough,et al.  Nanoparticle factories: Biofilms hold the key to gold dispersion and nugget formation , 2010 .

[41]  T. Colman Gold in Britain: past, present and future , 2010 .

[42]  Kelly P. Nevin,et al.  Electrosynthesis of Organic Compounds from Carbon Dioxide Is Catalyzed by a Diversity of Acetogenic Microorganisms , 2011, Applied and Environmental Microbiology.

[43]  Steven Salzberg,et al.  BIOINFORMATICS ORIGINAL PAPER , 2004 .

[44]  Ryan Noble,et al.  Assessing microbiological surface expression over an overburden-covered VMS deposit , 2012 .

[45]  S. Wakelin,et al.  Supergene gold transformation: Secondary and nano-particulate gold from southern New Zealand , 2012 .

[46]  J. Laird,et al.  Supergene gold transformation: Biogenic secondary and nano-particulate gold from arid Australia , 2012 .

[47]  Eoin L. Brodie,et al.  Influence of geogenic factors on microbial communities in metallogenic Australian soils , 2012, The ISME Journal.

[48]  W. S. Rasband,et al.  ImageJ: Image processing and analysis in Java , 2012 .

[49]  A. Durand,et al.  Coproporphyrin III excretion identifies the anaerobic coproporphyrinogen III oxidase HemN as a copper target in the Cu+‐ATPase mutant copA− of Rubrivivax gelatinosus , 2013, Molecular microbiology.

[50]  Carla M. Zammit,et al.  Geobiological Cycling of Gold: From Fundamental Process Understanding to Exploration Solutions , 2013 .

[51]  M. D. Jonge,et al.  Can biological toxicity drive the contrasting behavior of platinum and gold in surface environments , 2013 .

[52]  H. Ceri,et al.  Mixed-Species Biofilms Cultured from an Oil Sand Tailings Pond can Biomineralize Metals , 2014, Microbial Ecology.

[53]  G. Hause,et al.  Influence of Copper Resistance Determinants on Gold Transformation by Cupriavidus metallidurans Strain CH34 , 2013, Journal of bacteriology.

[54]  Robert C. Edgar,et al.  UPARSE: highly accurate OTU sequences from microbial amplicon reads , 2013, Nature Methods.

[55]  Ashraf Ibrahim,et al.  Gold biomineralization by a metallophore from a gold-associated microbe. , 2013, Nature chemical biology.

[56]  Joël Brugger,et al.  Analysis of gold(I/III)-complexes by HPLC-ICP-MS demonstrates gold(III) stability in surface waters. , 2014, Environmental science & technology.

[57]  T. Bolin,et al.  The effect of iron-oxidising bacteria on the stability of gold (I) thiosulphate complex , 2014 .

[58]  Yi Lu,et al.  Metalloproteins Containing Cytochrome, Iron–Sulfur, or Copper Redox Centers , 2014, Chemical reviews.

[59]  R. Hocking,et al.  Effect of manganese oxide minerals and complexes on gold mobilization and speciation , 2015 .

[60]  Gürol M. Süel,et al.  Ion channels enable electrical communication in bacterial communities , 2015, Nature.

[61]  S. Wakelin,et al.  Geogenic Factors as Drivers of Microbial Community Diversity in Soils Overlying Polymetallic Deposits , 2015, Applied and Environmental Microbiology.

[62]  S. Koechler,et al.  Toxic metal resistance in biofilms: diversity of microbial responses and their evolution. , 2015, Research in microbiology.

[63]  G. Southam,et al.  The in-vitro “growth” of gold grains , 2015 .

[64]  B. Mueller Experimental Interactions Between Clay Minerals and Bacteria: A Review , 2015 .

[65]  Chad W. Johnston,et al.  Structural and Chemical Characterization of Placer Gold Grains: Implications for Bacterial Contributions to Grain Formation , 2015 .

[66]  M. Dopson,et al.  Possibilities for extremophilic microorganisms in microbial electrochemical systems , 2015, FEMS microbiology reviews.

[67]  D. Craw,et al.  Gold nugget morphology and geochemical environments of nugget formation, southern New Zealand , 2016 .

[68]  Carla M. Zammit,et al.  Bacterial biofilms on gold grains-implications for geomicrobial transformations of gold. , 2016, FEMS microbiology ecology.

[69]  J. Brugger,et al.  Applying the Midas touch: differing toxicity of mobile gold and platinum complexes drives biomineralization in the bacterium Cupriavidus metallidurans , 2016 .

[70]  Carla M. Zammit,et al.  Introducing BASE: the Biomes of Australian Soil Environments soil microbial diversity database , 2016, GigaScience.

[71]  N. Fierer,et al.  Relic DNA is abundant in soil and obscures estimates of soil microbial diversity , 2016, bioRxiv.

[72]  W. Röling,et al.  Resilience of Soil Microbial Communities to Metals and Additional Stressors: DNA-Based Approaches for Assessing “Stress-on-Stress” Responses , 2016, International journal of molecular sciences.

[73]  A. Meliani,et al.  Biofilm-Mediated Heavy Metals Bioremediation in PGPR Pseudomonas , 2016 .

[74]  Daniel S. Margulies,et al.  2015 Brainhack Proceedings , 2016, GigaScience.

[75]  Carla M. Zammit,et al.  Proteomic responses to gold(iii)-toxicity in the bacterium Cupriavidus metallidurans CH34. , 2016, Metallomics : integrated biometal science.

[76]  Lev Tsimring,et al.  Species-Independent Attraction to Biofilms through Electrical Signaling , 2017, Cell.

[77]  R. Hough,et al.  Low temperature recrystallisation of alluvial gold in paleoplacer deposits , 2017 .

[78]  G. Southam,et al.  Secondary gold structures: Relics of past biogeochemical transformations and implications for colloidal gold dispersion in subtropical environments , 2017 .

[79]  D. Craw,et al.  Morphological evolution of gold nuggets in proximal sedimentary environments, southern New Zealand , 2017 .

[80]  S. Baginsky,et al.  Synergistic Toxicity of Copper and Gold Compounds in Cupriavidus metallidurans , 2017, Applied and Environmental Microbiology.

[81]  F. Reith,et al.  Effect of soil properties on gold- and platinum nanoparticle mobility , 2017 .

[82]  Gürol M. Süel,et al.  Coupling between distant biofilms and emergence of nutrient time-sharing , 2017, Science.

[83]  G. Southam,et al.  Biogeochemical Cycling of Silver in Acidic, Weathering Environments , 2017 .

[84]  A. Holleitner,et al.  Synergistic gold-copper detoxification at the core of gold biomineralisation in Cupriavidus metallidurans. , 2018, Metallomics : integrated biometal science.

[85]  G. Nolze,et al.  Biogeochemical cycling of gold: Transforming gold particles from arctic Finland , 2018 .