Abstract
Bioleaching of metal sulfides is performed by a diverse group of microorganisms. The dissolution chemistry of metal sulfides follows two pathways, which are determined by the mineralogy and the acid solubility of the metal sulfides: the thiosulfate and the polysulfide pathways. Bacterial cells can effect this metal sulfide dissolution via iron(II) ion and sulfur compound oxidation. Thereby, iron(III) ions and protons, the metal sulfide-attacking agents, are available. Cells can be active either in planktonic state or in forming biofilms on the mineral surface; however, the latter is much more efficient in terms of bioleaching kinetics. In the case of Acidithiobacillus ferrooxidans, bacterial exopolymers contain iron(III) ions, each complexed by two uronic acid residues. The resulting positive charge allows an electrostatic attachment to the negatively charged pyrite. Thus, the first function of complexed iron(III) ions is the mediation of cell attachment, while their second function is oxidative dissolution of the metal sulfide, similar to the role of free iron(III) ions in non-contact leaching. In both cases, the electrons extracted from the metal sulfide reduce molecular oxygen via a redox chain forming a supercomplex spanning the periplasmic space and connecting both outer and inner membranes. In this review, we summarize some recent discoveries relevant to leaching bacteria which contribute to a better understanding of these fascinating microorganisms. These include surface science, biochemistry of iron and sulfur metabolism, anaerobic metabolism, and biofilm formation. The study of microbial interactions among multispecies leaching consortia, including cell-to-cell communication mechanisms, must be considered in order to reveal more insights into the biology of bioleaching microorganisms and their potential biotechnological use.
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References
Acuña J, Rojas J, Amaro AM, Toledo H, Jerez CA (1992) Chemotaxis of Leptospirillum ferrooxidans and other acidophilic chemolithotrophs: comparison with the Escherichia coli chemosensory system. FEMS Microbiol Lett 75:37–42
Alvarez S, Jerez CA (2004) Copper ions stimulate polyphosphate degradation and phosphate efflux in Acidithiobacillus ferrooxidans. Appl Environ Microbiol 70:5177–5182
Amouric A, Brochier-Armanet C, Johnson DB, Bonnefoy V, Hallberg KB (2010) Phylogenetic and genetic variation among Fe(II)-oxidizing acidithiobacilli supports the view that these comprise multiple species with different ferrous iron oxidation pathways. Microbiology 157:111–122
Andrews GF (1988) The selective adsorption of thiobacilli to dislocation sites on pyrite surfaces. Biotechnol Bioeng 31:378–381
Appia-Ayme C, Guiliani N, Ratouchniak J, Bonnefoy V (1999) Characterization of an operon encoding two c-type cytochromes, an aa(3)-type cytochrome oxidase, and rusticyanin in Thiobacillus ferrooxidans ATCC 33020. Appl Environ Microbiol 65:4781–4787
Bagdigian RM, Myerson AS (1986) The adsorption of Thiobacillus ferrooxidans on coal surfaces. Biotechnol Bioeng 28:467–479
Balci N, Shanks WC III, Mayer B, Mandernack KW (2007) Oxygen and sulfur isotope systematics of sulfate produced during bacterial and abiotic oxidation of pyrite. Geochim Cosmochim Acta 71:3796–3811
Balci N, Mayer B, Shanks WC III, Mandernack KW (2012) Oxygen and sulfur isotope systematics of sulfate produced during abiotic and bacterial oxidation of sphalerite and elemental sulfur. Geochim Cosmochim Acta 77:335–351
Bellenberg S, Leon-Morales CF, Sand W, Vera M (2012) Visualization of capsular polysaccharide induction in Acidithiobacillus ferrooxidans. Hydrometallurgy 129–130:82–89
Bevilaqua D, Leite ALLC, Garcia O Jr, Tuovinen OH (2002) Oxidation of chalcopyrite by Acidithiobacillus ferrooxidans and Acidithiobacillus thiooxidans in shake flasks. Process Biochem 38:587–592
Blake RC 2nd, Griff MN (2012) In situ spectroscopy on intact Leptospirillum ferrooxidans reveals that reduced cytochrome 579 is an obligatory intermediate in the aerobic iron respiratory chain. Front Microbiol 3:136–146
Blake RC, Shute EA, Howard GT (1994) Solubilization of minerals by bacteria: electrophoretic mobility of Thiobacillus ferrooxidans in the presence of iron, pyrite, and sulfur. Appl Environ Microbiol 60:3349–3357
Bond PL, Druschel GK, Banfield JF (2000) Comparison of acid mine drainage microbial communities in physically and geochemically distinct ecosystems. Appl Environ Microbiol 66:4962–4971
Bonnefoy V, Holmes DS (2011) Genomic insights into microbial iron oxidation and iron uptake strategies in extremely acidic environments. Environ Microbiol 14:1597–1611
Boon M, Heijnen JJ, Hansford GS (1998) The mechanism and kinetics of bioleaching sulphide minerals. Miner Process Extr Metall Rev 19:107–115
Borg RJ, Dienes GJ (1992) The physical chemistry of solids. Academic, Boston
Bosecker K (1997) Bioleaching: metal solubilization by microorganisms. FEMS Microbiol Rev 20:591–604
Bruscella P, Cassagnaud L, Ratouchniak J, Brasseur G, Lojou E, Amils R, Bonnefoy V (2005) The HiPIP from the acidophilic Acidithiobacillus ferrooxidans is correctly processed and translocated in Escherichia coli, in spite of the periplasm pH difference between these two micro-organisms. Microbiology 151:1421–1431
Castelle C, Guiral M, Malarte G, Ledgham F, Leroy G, Brugna M, Giudici-Orticoni MT (2008) A new iron-oxidizing/O2-reducing supercomplex spanning both inner and outer membranes, isolated from the extreme acidophile Acidithiobacillus ferrooxidans. J Biol Chem 283:25803–25811
Castelle C, Ilbert M, Infossi P, Leroy G, Giudici-Orticoni MT (2010) An unconventional copper protein required for cytochrome c oxidase respiratory function under extreme acidic conditions. J Biol Chem 285:21519–21525
Clark DA, Norris PR (1996) Acidimicrobium ferrooxidans gen. nov., sp. nov.: mixed-culture ferrous iron oxidation with Sulfobacillus species. Microbiology 142:785–790
Cox JC, Boxer DH (1978) The purification and some properties of rusticyanin, a blue copper protein involved in iron(II) oxidation from Thiobacillus ferrooxidans. Biochem J 174:497–502
Crundwell FK (1988) The influence of the electronic structure of solids on the anodic dissolution and leaching of semiconducting sulphide minerals. Hydrometallurgy 21:155–190
Das A, Mishra AK, Roy P (1992) Anaerobic growth on elemental sulfur using dissimilar iron reduction by autotrophic Thiobacillus ferrooxidans. FEMS Microbiol Lett 97:167–172
Dispirito AA, Dugan PR, Tuovinen OH (1983) Sorption of Thiobacillus ferrooxidans to particulate material. Biotechnol Bioeng 25:1163–1168
Dopson M, Johnson DB (2012) Biodiversity, metabolism and applications of acidophilic sulfur-metabolizing microorganisms. Environ Microbiol 14:2620–2631
Druschel GK (2002) Sulfur biogeochemistry: kinetics of intermediate sulfur species reactions in the environment. PhD thesis, University of Wisconsin
Druschel G, Borda M (2006) Comment on “Pyrite dissolution in acidic media” by M. Descostes, P. Vitorge, and C. Beaucaire. Geochim Cosmochim Acta 70:5246–5250
du Plessis CA, Slabbert W, Hallberg KB, Johnson DB (2011) Ferredox: a biohydrometallurgical processing concept for limonitic nickel laterites. Hydrometallurgy 109:221–229
Dutrizac JE, MacDonald RJC (1974) Ferric ion as a leaching medium. Miner Sci Eng 6:59–100
Dziurla MA, Achouak W, Lam BT, Heulin T, Berthelin J (1998) Enzyme-linked immunofiltration assay to estimate attachment of thiobacilli to pyrite. Appl Environ Microbiol 64:2937–2942
Edwards KJ, Bond PL, Gihring TM, Banfield JF (2000) An archaeal iron-oxidizing extreme acidophile important in acid mine drainage. Science 287:1796–1799
Edwards KJ, Hu B, Hamers RJ, Banfield JF (2001) A new look at microbial leaching patterns on sulfide minerals. FEMS Microbiol Ecol 34:197–206
Ehrlich HL (2009) Geomicrobiology, 5th edn. CRC, Boca Raton
Evangelou VPB (1995) Pyrite oxidation and its control. CRC, Boca Raton
Farah C, Vera M, Morin D, Haras D, Jerez CA, Guiliani N (2005) Evidence for a functional quorum-sensing type AI-1 system in the extremophilic bacterium Acidithiobacillus ferrooxidans. Appl Environ Microbiol 71:7033–7040
Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633
Fowler TA, Crundwell FK (1998) Leaching of zinc sulfide by Thiobacillus ferrooxidans: experiments with a controlled redox potential indicate no direct bacterial mechanism. Appl Environ Microbiol 64:3570–3575
Fowler TA, Holmes PR, Crundwell FK (1999) Mechanism of pyrite dissolution in the presence of Thiobacillus ferrooxidans. Appl Environ Microbiol 65:2987–2993
Gehrke T, Telegdi J, Thierry D, Sand W (1998) Importance of extracellular polymeric substances from Thiobacillus ferrooxidans for bioleaching. Appl Environ Microbiol 64:2743–2747
Gehrke T, Hallmann R, Kinzler K, Sand W (2001) The EPS of Acidithiobacillus ferrooxidans—a model for structure–function relationships of attached bacteria and their physiology. Water Sci Technol 43:159–167
Golyshina OV, Pivovarova TA, Karavaiko GI, Kondratéva TF, Moore ER, Abraham WR, Lünsdorf H, Timmis KN, Yakimov MM, Golyshin PN (2000) Ferroplasma acidiphilum gen. nov., sp. nov., an acidophilic, autotrophic, ferrous-iron-oxidizing, cell-wall-lacking, mesophilic member of the Ferroplasmaceae fam. nov., comprising a distinct lineage of the Archaea. Int J Syst Evol Microbiol 50(Pt 3):997–1006
González A, Bellenberg S, Mamani S, Ruiz L, Echeverría A, Soulère L, Doutheau A, Demergasso C, Sand W, Queneau Y, Vera M, Guiliani N (2012) AHL signaling molecules with a large acyl chain enhance biofilm formation on sulfur and metal sulfides by the bioleaching bacterium Acidithiobacillus ferrooxidans. Appl Microbiol Biotechnol 97:3729–3737
Hackl RP, Dreisinger DB, Peters E, King JA (1995) Passivation of chalcopyrite during oxidative leaching in sulfate media. Hydrometallurgy 39:25–48
Hallberg KB, Gonzalez-Toril E, Johnson DB (2009) Acidithiobacillus ferrivorans, sp. nov.; facultatively anaerobic, psychrotolerant iron-, and sulfur-oxidizing acidophiles isolated from metal mine-impacted environments. Extremophiles 14:9–19
Hallberg KB, Grail BM, du Plessis CA, Johnson DB (2011a) Reductive dissolution of ferric iron minerals: a new approach for bio-processing nickel laterites. Miner Eng 24:620–624
Hallberg KB, Hedrich S, Johnson DB (2011b) Acidiferrobacter thiooxydans, gen. nov. sp. nov.; an acidophilic, thermo-tolerant, facultatively anaerobic iron- and sulfur-oxidizer of the family Ectothiorhodospiraceae. Extremophiles 15:271–279
Hallmann R, Friedrich A, Koops HP, Pommerening-Röser A, Rohde K, Zenneck C, Sand W (1993) Physiological characteristics of Thiobacillus ferrooxidans and Leptospirillum ferrooxidans and physiochemical factors influence microbial metal leaching. Geomicrobiol J 10:193–206
Hansford GS (1997) Recent developments in modelling the kinetics of bioleaching sulphide minerals. In: Rawlings DE (ed) Biomining: theory, microbes and industrial processes. Springer, Berlin, pp 153–175
Harneit K, Göksel A, Kock D, Klock JH, Gehrke T, Sand W (2006) Adhesion to metal sulphide surfaces by cells of Acidithiobacillus ferrooxidans, Acidithiobacillus thiooxidans and Leptospirillum ferrooxidans. Hydrometallurgy 83:245–254
Harrison AP Jr (1982) Genomic and physiological diversity amongst strains of Thiobacillus ferrooxidans, and genomic comparison with Thiobacillus thiooxidans. Arch Microbiol 131:68–76
Hedrich S, Schlömann M, Johnson DB (2011) The iron-oxidizing proteobacteria. Microbiology 157:1551–1564
Hiraishi A, Nagashima KV, Matsuura K, Shimada K, Takaichi S, Wakao N, Katayama Y (1998) Phylogeny and photosynthetic features of Thiobacillus acidophilus and related acidophilic bacteria: its transfer to the genus Acidiphilium as Acidiphilium acidophilum comb. nov. Int J Syst Bacteriol 48:1389–1398
Hiraishi A, Matsuzawa Y, Kanbe T, Wakao N (2000) Acidisphaera rubrifaciens gen. nov., sp. nov., an aerobic bacteriochlorophyll-containing bacterium isolated from acidic environments. Int J Syst Evol Microbiol 50:1539–1546
Hiraishi A, Shimada K (2001) Aerobic anoxygenic photosynthetic bacteria with zinc-bacteriochlorophyll. J Gen Appl Microbiol 47:161–180
Ingledew WJ, Cobley JG (1980) A potentiometric and kinetic study on the respiratory chain of ferrous-iron-grown Thiobacillus ferrooxidans. Biochim Biophys Acta 590:141–158
Johnson DB, Hallberg KB (2005) Acid mine drainage remediation options: a review. Sci Total Environ 338:3–14
Johnson DB (2011) Geomicrobiology of extremely acidic subsurface environments. FEMS Microbiol Ecol 81:2–12
Johnson DB, Kanao T, Hedrich S (2012) Redox transformations of iron at extremely low pH: fundamental and applied aspects. Front Microbiol 3:96
Kelly DP, Wood AP (2000) Reclassification of some species of Thiobacillus to the newly designated genera Acidithiobacillus gen. nov., Halothiobacillus gen. nov. and Thermithiobacillus gen. nov. Int J Syst Evol Microbiol 50:511–516
Korehi H, Blöthe M, Sitnikova MA, Dold B, Schippers A (2013) Metal mobilization by iron- and sulfur-oxidizing bacteria in a multiple extreme mine tailings in the Atacama Desert, Chile. Environ Sci Technol 47:2189–2196
Liljeqvist M, Valdes J, Holmes DS, Dopson M (2011) Draft genome of the psychrotolerant acidophile Acidithiobacillus ferrivorans SS3. J Bacteriol 193:4304–4305
Liljeqvist M, Rzhepishevska OI, Dopson M (2012) Gene identification and substrate regulation provide insights into sulfur accumulation during bioleaching with the psychrotolerant acidophile Acidithiobacillus ferrivorans. Appl Environ Microbiol 79:951–957
Little B, Ray B, Pope R, Franklin M, White DC (2000) Spatial and temporal relationships between localised corrosion and bacterial activity on iron-containing substrata. In: Sequeira CAC (ed) Microbial corrosion. European Federation of Corrosion Publications, no. 29. Institute of Materials, London, pp 21–35
Lowson RT (1982) Aqueous oxidation of pyrite by molecular oxygen. Chem Rev 82:461–497
Luther GW III (1987) Pyrite oxidation and reduction: molecular orbital theory considerations. Geochim Cosmochim Acta 51:3193–3199
McGuire MM, Edwards KJ, Banfield JF, Hamers RJ (2001) Kinetics, surface chemistry, and structural evolution of microbially mediated sulfide mineral dissolution. Geochim Cosmochim Acta 65:1243–1258
Medvedev D, Stuchebrukhov A (2001) DNA repair mechanism by photolyase: electron transfer path from the photolyase catalytic cofactor FADH− to DNA thymine dimer. J Theor Biol 210:237–248
Meruane G, Salhe C, Wiertz J, Vargas T (2002) Novel electrochemical–enzymatic model which quantifies the effect of the solution E h on the kinetics of ferrous iron oxidation with Acidithiobacillus ferrooxidans. Biotechnol Bioeng 80:280–288
Meyer G, Schneider-Merck T, Böhme S, Sand W (2002) A simple method for investigations on the chemotaxis of A. ferrooxidans and D. vulgaris. Acta Biotechnol 22:391–399
Moses CO, Nordstrom DK, Herman JS, Mills AL (1987) Aqueous pyrite oxidation by dissolved oxygen and by ferric iron. Geochim Cosmochim Acta 51:1561–1571
Mustin C, de Donato P, Berthelin J, Marion P (1993) Surface sulphur as promoting agent of pyrite leaching by Thiobacillus ferrooxidans. FEMS Microbiol Rev 11:71–78
NIST (2004) NIST critical selected stability constants of metal complexes database. NIST standard reference database 46, ver 8.0. National Institute of Standards and Technology, Gaithersburg, MD. http://www.nist.gov/srd/upload/46_8.htm
Nordstrom DK (1982) Aqueous pyrite oxidation and the consequent formation of secondary iron minerals. In: Hossner LR, Kittrick JA, Fanning DF (eds) Acid sulfate weathering, pedogeochemistry and relationship to manipulation of soil minerals. Soil Science Society of America Press, Madison, WI, pp 37–55
Norris PR, Barr DW, Hinson D (1988) Iron and mineral oxidation by acidophilic bacteria: affinities for iron and attachment to pyrite. In: Norris PR, Kelly DP (eds) Biohydrometallurgy. Proceedings of the International Symposium. Science and Technology Letters, Kew, pp 43–59
Norris PR, Burton NP, Foulis NAM (2000) Acidophiles in bioreactor mineral processing. Extremophiles 4:71–76
Ohmura N, Kitamura K, Saiki H (1993) Selective adhesion of Thiobacillus ferrooxidans to pyrite. Appl Environ Microbiol 59:4044–4050
Ohmura N, Sasaki K, Matsumoto N, Saiki H (2002) Anaerobic respiration using Fe(3+), S(0), and H(2) in the chemolithoautotrophic bacterium Acidithiobacillus ferrooxidans. J Bacteriol 184:2081–2087
Olson GJ, Brierley JA, Brierley CL (2003) Bioleaching review part B: progress in bioleaching: applications of microbial processes by the minerals industries. Appl Microbiol Biotechnol 63:249–257
Orell A, Navarro CA, Arancibia R, Mobarec JC, Jerez CA (2010) Life in blue: copper resistance mechanisms of bacteria and archaea used in industrial biomining of minerals. Biotechnol Adv 28:839–848
Orell A, Navarro CA, Rivero M, Aguilar JS, Jerez CA (2012) Inorganic polyphosphates in extremophiles and their possible functions. Extremophiles 16:573–583
Osorio H, Mangold S, Denis Y, Nancucheo I, Esparza M, Johnson DB, Bonnefoy V, Dopson M, Holmes DS (2013) Anaerobic sulfur metabolism coupled to dissimilatory iron reduction in the extremophile Acidithiobacillus ferrooxidans. Appl Environ Microbiol 79:2172–2181
Pronk JT, de Bruyn JC, Bos P, Kuenen JG (1992) Anaerobic growth of Thiobacillus ferrooxidans. Appl Environ Microbiol 58:2227–2230
Quatrini R, Appia-Ayme C, Denis Y, Jedlicki E, Holmes DS, Bonnefoy V (2009) Extending the models for iron and sulfur oxidation in the extreme acidophile Acidithiobacillus ferrooxidans. BMC Genomics 10:394
Rawlings DE (1997) Biomining: theory, microbes and industrial processes. Springer, Berlin
Rawlings DE, Tributsch H, Hansford GS (1999) Reasons why ‘Leptospirillum’-like species rather than Thiobacillus ferrooxidans are the dominant iron-oxidizing bacteria in many commercial processes for the biooxidation of pyrite and related ores. Microbiology 145(Pt 1):5–13
Rawlings DE (2002) Heavy metal mining using microbes. Annu Rev Microbiol 56:65–91
Remonsellez F, Orell A, Jerez CA (2006) Copper tolerance of the thermoacidophilic archaeon Sulfolobus metallicus: possible role of polyphosphate metabolism. Microbiology 152:59–66
Rimstidt JD, Vaughan DJ (2003) Pyrite oxidation: a state-of-the-art assessment of the reaction mechanism. Geochim Cosmochim Acta 67:873–880
Rodriguez-Leiva M, Tributsch H (1988) Morphology of bacterial leaching patterns by Thiobacillus ferrooxidans on synthetic pyrite. Arch Microbiol 149:401–405
Rohwerder T, Gehrke T, Kinzler K, Sand W (2003) Bioleaching review part A: progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation. Appl Microbiol Biotechnol 63:239–248
Rohwerder T, Sand W (2003) The sulfane sulfur of persulfides is the actual substrate of the sulfur-oxidizing enzymes from Acidithiobacillus and Acidiphilium spp. Microbiology 149:1699–1710
Rossi G (1990) Biohydrometallurgy. McGraw-Hill, Hamburg
Rossi G (1993) Biodepyritization of coal: achievements and problems. Fuel 72:1581–1592
Ruiz L, Valenzuela S, Castro M, Gonzalez A, Frezza M, Soulère L, Rohwerder T, Queneau Y, Doutheau A, Sand W, Jerez CA, Guiliani N (2008) AHL communication is a widespread phenomenon in biomining bacteria and seems to be involved in mineral-adhesion efficiency. Hydrometallurgy 94:133–137
Ruiz LM, Castro M, Barriga A, Jerez CA, Guiliani N (2011) The extremophile Acidithiobacillus ferrooxidans possesses a c-di-GMP signalling pathway that could play a significant role during bioleaching of minerals. Lett Appl Microbiol 54:133–139
Sampson MI, Phillips CV, Blake RC II (2000) Influence of the attachment of acidophilic bacteria during the oxidation of mineral sulfides. Min Eng 13:373–389
Sand W, Rohde K, Sobotke B, Zenneck C (1992) Evaluation of Leptospirillum ferrooxidans for leaching. Appl Environ Microbiol 58:85–92
Sand W, Gehrke T, Hallmann R, Schippers A (1995) Sulfur chemistry, biofilm, and the (in)direct attack mechanism—a critical evaluation of bacterial leaching. Appl Microbiol Biotechnol 43:961–966
Sand W, Gehrke T, Jozsa PG, Schippers A (2001) (Bio)chemistry of bacterial leaching—direct vs. indirect bioleaching. Hydrometallurgy 59:159–175
Sand W, Jozsa PG, Kovacs ZM, Săsăran N, Schippers A (2007) Long-term evaluation of acid rock drainage mitigation measures in large lysimeters. J Geochem Explor 92:205–211
Sanhueza A, Ferrer IJ, Vargas T, Amils R, Sánchez C (1999) Attachment of Thiobacillus ferrooxidans on synthetic pyrite of varying structural and electronic properties. Hydrometallurgy 51:115–129
Schippers A, Jozsa P, Sand W (1996) Sulfur chemistry in bacterial leaching of pyrite. Appl Environ Microbiol 62:3424–3431
Schippers A, Rohwerder T, Sand W (1999) Intermediary sulfur compounds in pyrite oxidation: implications for bioleaching and biodepyritization of coal. Appl Microbiol Biotechnol 52:104–110
Schippers A, Sand W (1999) Bacterial leaching of metal sulfides proceeds by two indirect mechanisms via thiosulfate or via polysulfides and sulfur. Appl Environ Microbiol 65:319–321
Schippers A, Jozsa PG, Kovacs ZM, Jelea M, Sand W (2001) Large-scale experiments for microbiological evaluation of measures for safeguarding sulfidic mine waste. Waste Manage 21:139–146
Schippers A (2004) Biogeochemistry of metal sulfide oxidation in mining environments, sediments and soils. In: Amend JP, Edwards KJ, Lyons TW (eds) Sulfur biogeochemistry—past and present. Special Paper 379. Geological Society of America, Boulder, CO, pp 49–62
Schippers A, Breuker A, Blazejak A, Bosecker K, Kock D, Wright TL (2010) The biogeochemistry and microbiology of sulfidic mine waste and bioleaching dumps and heaps, and novel Fe(II)-oxidizing bacteria. Hydrometallurgy 104:342–350
Schrenk MO, Edwards KJ, Goodman RM, Hamers RJ, Banfield JF (1998) Distribution of Thiobacillus ferrooxidans and Leptospirillum ferrooxidans: implications for generation of acid mine drainage. Science 279:1519–1522
Shrihari RK, Modak JM, Kumar R, Gandhi KS (1995) Dissolution of particles of pyrite mineral by direct attachment of Thiobacillus ferrooxidans. Hydrometallurgy 38:175–187
Singer PC, Stumm W (1970) Acidic mine drainage: the rate-determining step. Science 167:1121–1123
Singer SW, Erickson BK, VerBerkmoes NC, Hwang M, Shah MB, Hettich RL, Banfield JF, Thelen MP (2010) Posttranslational modification and sequence variation of redox-active proteins correlate with biofilm life cycle in natural microbial communities. ISME J 4:1398–1409
Smart RSC, Jasieniak M, Prince KE, Skinner WM (2000) SIMS studies of oxidation mechanisms and polysulfide formation in reacted sulfide surfaces. Miner Eng 13:857–870
Smith JA, Lovley DR, Tremblay PL (2012) Outer cell surface components essential for Fe(III) oxide reduction by Geobacter metallireducens. Appl Environ Microbiol 79:901–907
Solari JA, Huerta G, Escobar B, Vargas T, Badilla-Ohlbaum R, Rubio J (1992) Interfacial phenomena affecting the adhesion of Thiobacillus ferrooxidans to sulphide mineral surfaces. Colloid Surf 69:159–166
Taylor ES, Lower SK (2008) Thickness and surface density of extracellular polymers on Acidithiobacillus ferrooxidans. Appl Environ Microbiol 74:309–311
Thomas JE, Jones CF, Skinner WM, Smart RSC (1998) The role of surface sulfur species in the inhibition of pyrrhotite dissolution in acid conditions. Geochim Cosmochim Acta 62:1555–1565
Thomas JE, Skinner WM, Smart RSC (2001) A mechanism to explain sudden changes in rates and products for pyrrhotite dissolution in acid solution. Geochim Cosmochim Acta 65:1–12
Thurston RS, Mandernack KW, Shanks WC III (2010) Laboratory chalcopyrite oxidation by Acidithiobacillus ferrooxidans: oxygen and sulfur isotope fractionation. Chem Geol 269:252–261
Tributsch H, Bennett JC (1981a) Semiconductor–electrochemical aspects of bacterial leaching. 1. Oxidation of metal sulphides with large energy gaps. J Chem Technol Biotechnol 31:565–577
Tributsch H, Bennett JC (1981b) Semiconductor–electrochemical aspects of bacterial leaching. Part 2. Survey of rate-controlling sulphide properties. J Chem Technol Biotechnol 31:627–635
Tributsch H (2001) Direct versus indirect bioleaching. Hydrometallurgy 59:177–185
Vandevivere P, Kirchman DL (1993) Attachment stimulates exopolysaccharide synthesis by a bacterium. Appl Environ Microbiol 59:3280–3286
Vaughan DJ, Craig JR (1978) Mineral chemistry of metal sulfides. Cambridge University Press, Cambridge
Vera M, Guiliani N, Jerez CA (2003) Proteomic and genomic analysis of the phosphate starvation response of Acidithiobacillus ferrooxidans. Hydrometallurgy 71:125–132
Vera M, Pagliai F, Guiliani N, Jerez CA (2008) The chemolithoautotroph Acidithiobacillus ferrooxidans can survive under phosphate-limiting conditions by expressing a C-P lyase operon that allows it to grow on phosphonates. Appl Environ Microbiol 74:1829–1835
Vera M, Krok B, Bellenberg S, Sand W, Poetsch A (2013) Shotgun proteomics study of early biofilm formation process of Acidithiobacillus ferrooxidans on pyrite. Proteomics 13:133–1144
Williamson MA, Rimstidt JD (1994) The kinetics and electrochemical rate-determing step of aqueous pyrite oxidation. Geochim Cosmochim Acta 58:5443–5454
Xu Y, Schoonen MAA (2000) The absolute energy positions of conduction and valence bands of selected semiconductiong minerals. Am Mineral 85:543–556
Yarzabal A, Brasseur G, Bonnefoy V (2002a) Cytochromes c of Acidithiobacillus ferrooxidans. FEMS Microbiol Lett 209:189–195
Yarzábal A, Brasseur G, Ratouchniak J, Lund K, Lemesle-Meunier D, DeMoss JA, Bonnefoy V (2002b) The high-molecular-weight cytochrome c Cyc2 of Acidithiobacillus ferrooxidans is an outer membrane protein. J Bacteriol 184:313–317
Yarzabal A, Appia-Ayme C, Ratouchniak J, Bonnefoy V (2004) Regulation of the expression of the Acidithiobacillus ferrooxidans rus operon encoding two cytochromes c, a cytochrome oxidase and rusticyanin. Microbiology 150:2113–2123
Zammit CM, Mangold S, Vr J, Mutch LA, Watling HR, Dopson M, Watkin EL (2011) Bioleaching in brackish waters—effect of chloride ions on the acidophile population and proteomes of model species. Appl Microbiol Biotechnol 93:319–329
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The authors want to thank Andrzej Kuklinski and Sören Bellenberg for providing KPFM-AFM and CLSM images, respectively.
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Vera, M., Schippers, A. & Sand, W. Progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation—part A. Appl Microbiol Biotechnol 97, 7529–7541 (2013). https://doi.org/10.1007/s00253-013-4954-2
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DOI: https://doi.org/10.1007/s00253-013-4954-2