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Bioleaching review part A:

Progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation

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Abstract

Bioleaching of metal sulfides is caused by astonishingly diverse groups of bacteria. Today, at least 11 putative prokaryotic divisions can be related to this phenomenon. In contrast, the dissolution (bio)chemistry of metal sulfides follows only two pathways, which are determined by the acid-solubility of the sulfides: the thiosulfate and the polysulfide pathway. The bacterial cell can effect this sulfide dissolution by “contact” and “non-contact” mechanisms. The non-contact mechanism assumes that the bacteria oxidize only dissolved iron(II) ions to iron(III) ions. The latter can then attack metal sulfides and be reduced to iron(II) ions. The contact mechanism requires attachment of bacteria to the sulfide surface. The primary mechanism for attachment to pyrite is electrostatic in nature. In the case of Acidithiobacillus ferrooxidans, bacterial exopolymers contain iron(III) ions, each complexed by two uronic acid residues. The resulting positive charge allows attachment to the negatively charged pyrite. Thus, the first function of complexed iron(III) ions in the contact mechanism is 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 the non-contact mechanism. In both cases, the electrons extracted from the metal sulfide reduce molecular oxygen via a complex redox chain located below the outer membrane, the periplasmic space, and the cytoplasmic membrane of leaching bacteria. The dominance of either At. ferrooxidans or Leptospirillum ferrooxidans in mesophilic leaching habitats is highly likely to result from differences in their biochemical iron(II) oxidation pathways, especially the involvement of rusticyanin.

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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 96:37–42

    Article  Google Scholar 

  • Alfreider A, Vogt C, Babel W (2002) Microbial diversity in an in situ reactor system treating monochlorobenzene-contaminated groundwater as revealed by 16S ribosomal DNA analysis. Syst Appl Microbiol 25:232–240

    CAS  PubMed  Google Scholar 

  • Andrews GF (1988) The selective adsorption of thiobacilli to dislocation sites on pyrite surfaces. Biotechnol Bioeng 31:378–381

    CAS  Google Scholar 

  • Appia-Ayme C, Guiliani N, Ratouchniak J, Bonnefoy V (1999) Characterization of an operon encoding two c-type cytochromes, an aa3-type cytochrome oxidase, and rusticyanin in Thiobacillus ferrooxidans ATCC 33020. Appl Environ Microbiol 65:4781–4787

    CAS  PubMed  Google Scholar 

  • Bagdigian RM, Meyerson AS (1986) The adsorption of Thiobacillus ferrooxidans on coal surfaces. Biotechnol Bioeng 28:467–479

    CAS  Google Scholar 

  • Baker BJ, Banfield JF (2003) Microbial communities in acid mine drainage. FEMS Microbiol Ecol 44:139–152

    Article  CAS  Google Scholar 

  • Barr DW, Ingledew WJ, Norris PR (1990) Respiratory chain components of iron-oxidizing, acidophilic bacteria. FEMS Microbiol Lett 70:85–90

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Blake RC II, Shute EA, Greenwood MM, Spencer GH, Ingledew WJ (1993a) Enzymes of aerobic respiration on iron. FEMS Microbiol Rev 11:9–18

    Article  CAS  PubMed  Google Scholar 

  • Blake RC II, Shute EA, Waskovsky J, Harrison AP Jr (1993b) Respiratory components in acidophilic bacteria that respire on iron. Geomicrobiol J 10:173–192

    Google Scholar 

  • Blake RC II, 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

    CAS  Google Scholar 

  • Bond PL, Druschel GK, Banfield JF (2000a) Comparison of acid mine drainage microbial communities in physically and geochemically distinct ecosystems. Appl Environ Microbiol 66:4962–4971

    CAS  PubMed  Google Scholar 

  • Bond PL, Smriga SP, Banfield JF (2000b) Phylogeny of microorganisms populating a thick, subaerial, predominantly lithotrophic biofilm at an extreme acid mine drainage site. Appl Environ Microbiol 66:3842–3849

    CAS  PubMed  Google Scholar 

  • Boon M, Heijnen JJ, Hansford GS (1998) The mechanism and kinetics of bioleaching sulphide minerals. Miner Process Extract Metal Rev 19:107–115

    CAS  Google Scholar 

  • Bosecker K (1997) Bioleaching: metal solubilization by microorganisms. FEMS Microbiol Rev 20:591–604

    Article  CAS  Google Scholar 

  • Clark DA, Norris PR (1996) Acidimicrobium ferrooxidans gen. nov., sp. nov.: mixed-culture ferrous iron oxidation with Sulfobacillus species. Microbiology 142:785–790

    CAS  Google Scholar 

  • Coram NJ, Rawlings DE (2002) Molecular relationship between two groups of the genus Leptospirillum and the finding that Leptospirillum ferriphilum sp. nov. dominates South African commercial biooxidation tanks that operate at 40 degrees C. Appl Environ Microbiol 68:838–845

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • DiSpirito AA, Dugan PR, Tuovinen OH (1983) Sorption of Thiobacillus ferrooxidans to particulate material. Biotechnol Bioeng 25:1163–1168

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Edwards KJ, Rutenberg AD (2001) Microbial response to surface microtopography: the role of metabolism in localized mineral dissolution. Chem Geol 180:19–32

    Article  CAS  Google Scholar 

  • Edwards KJ, Schrenk MO, Hamers R, Banfield JF (1998) Microbial oxidation of pyrite: experiments using microorganisms from an extreme acidic environment. Am Mineral 83:1444–1453

    CAS  Google Scholar 

  • Edwards KJ, Goebel BM, Rodgers TM, Schrenk MO, Gihring TM, Cardona MM, Mcguire MM, Hamers RJ, Pace NR, Banfield JF (1999) Geomicrobiology of pyrite (FeS2) dissolution: case study at Iron Mountain, California. Geomicrobiol J 16:155–179

    Article  CAS  Google Scholar 

  • Edwards KJ, Bond PL, Gihring TM, Banfield JF (2000) An archaeal iron-oxidizing extreme acidophile important in acid mine drainage. Science 279:1796–1799

    Article  Google Scholar 

  • Ehrlich HL (2002) Geomicrobiology, 4th edn. Dekker, New York

  • 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

    CAS  PubMed  Google Scholar 

  • Fowler TA, Crundwell FK (1999) Leaching of zinc sulfide by Thiobacillus ferrooxidans: bacterial oxidation of the sulfur product layer increases the rate of zinc sulfide dissolution at high concentrations of ferrous ions. Appl Environ Microbiol 65:5285–5292

    Google Scholar 

  • Fowler TA, Holmes PR, Crundwell FK (1999) Mechanism of pyrite dissolution in the presence of Thiobacillus ferrooxidans. Appl Environ Microbiol 65:2987–2993

    CAS  PubMed  Google Scholar 

  • Fuchs T, Huber H, Teiner K, Burggraf S, Stetter KO (1995) Metallosphaera prunae, sp. nov., a novel metal-mobilizing, thermoacidophilic archaeum, isolated from a uranium mine in Germany. Syst Appl Microbiol 18:560–566

    Google Scholar 

  • Fuchs T, Huber H, Burggraf S, Stetter KO (1996) 16S rDNA-based phylogeny of the archaeal order Sulfolobales and reclassification of Desulfurolobus ambivalens as Acidianus ambivalens comb. nov. Syst Appl Microbiol 19:56–60

    CAS  Google Scholar 

  • Gehrke T (1998) Bedeutung extrazellulärer polymerer Substanzen von Thiobacillus ferrooxidans für die mikrobielle Besiedelung und Laugung von Pyrit und Schwefel. Dissertation, University of Hamburg, Hamburg

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Giudici-Orticoni MT, Guerlesquin F, Bruschi M, Nitschke W (1999) Interaction-induced redox switch in the electron transfer complex rusticyanin-cytochrome c 4. J Biol Chem 274:30365–30369

    Article  CAS  PubMed  Google Scholar 

  • Golyshina OV, Pivovarova TA, Karavaiko GI, Kondrateva TF, Moore ER, Abraham WR, Lunsdorf 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 50:997–1006

    CAS  PubMed  Google Scholar 

  • Grützner T (2001) Auswirkungen von Acidithiobacillus ferrooxidans auf die Flotierbarkeit sulfidischer Minerale. Diploma thesis, TU Clausthal, Clausthal-Zellerfeld

  • Hallberg KB, Johnson DB (2001) Biodiversity of acidophilic prokaryotes. Adv Appl Microbiol 49:37–84

    CAS  PubMed  Google Scholar 

  • Hallmann R, Friedrich A, Koops H-P, Pommerening-Röser A, Rohde K, Zenneck C, Sand W (1993) Physiological characteristics of Thiobacillus ferrooxidans and Leptospirillum ferrooxidans and pyhsiochemical factors influence microbial metal leaching. Geomicrobiol J 10:193–206

    Google Scholar 

  • 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 Heidelberg New York, pp 153–175

  • Hippe H (2000) Leptospirillum gen. nov. (ex Markosyan 1972), nom. rev., including Leptospirillum ferrooxidans sp. nov. (ex Markosyan 1972), nom. rev. and Leptospirillum thermoferrooxidans sp. nov. (Golovacheva et al. 1992). Int J Syst Evol Microbiol 50:501–503

    PubMed  Google Scholar 

  • Hiraishi A, Shimada K (2001) Aerobic anoxygenic photosynthetic bacteria with zinc-bacteriochlorophyll. J Gen Appl Microbiol 47:161–180

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Hiraishi A, Matsuzawa Y, Kanbe T, Wakao N (2000) Acidisphaera rubrifaciens gen. nov., sp. nov., an aerobic bacteriophyll-containing bacterium isolated from acidic environments. Int J Syst Evol Microbiol 50:1539–1546

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Johnson DB (1998) Biodiversity and ecology of acidophilic microoganisms. FEMS Microbiol Ecol 27:307–317

    CAS  Google Scholar 

  • Johnson B, Roberto FF (1997) Heterotrophic acidophiles and their roles in the bioleaching of sulfide minerals. In: Rawlings DE (ed) Biomining: theory, microbes and industrial processes. Springer, Berlin Heidelberg New York, pp 259–279

  • Kai M, Yano T, Fukumori Y, Yamanaka T (1989) Cytochrome oxidase of an acidophilic iron-oxidizing bacterium, Thiobacillus ferrooxidans, functions at pH 3.5. Biochem Biophys Res Commun 160:839–843

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Kurosawa N, Itoh YH, Iwai T, Sugai A, Uda I, Kimura N, Horiuchi T, Itoh T (1998) Sulfurisphaera ohwakuensis gen. nov., sp. nov., a novel extremely thermophilic acidophile of the order Sulfolobales. Int J Syst Bacteriol 48:451–456

    PubMed  Google Scholar 

  • Lemesle-Meunier D, Brasseur G, Tron P, Bennaroch D, Nitschke W, Elbehti A (2001) The membrane-bound c type cytochromes and the interaction between the downhill and uphill electron transfer pathways in the acidophilic chemolithotrophic ferrous ion-oxidizing bacterium Thiobacillus ferrooxidans. In: Ciminelli VST, Garcia O Jr (eds) Process metallurgy, vol 9A. Elsevier, Amsterdam, pp 299–308

  • 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

  • Luther GW III (1987) Pyrite oxidation and reduction: molecular orbital theory considerations. Geochim Cosmochim Acta 51:3193–3199

    Article  CAS  Google Scholar 

  • Medvedev D, Stuchebrukhov AA (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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • NIST (2003) NIST critical selected stability constants of metal complexes database. NIST standard reference database 46, ver 7.0. National Institute of Standards and Technology, Gaithersburg, Md.

  • 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, Clark DA, Owen JP, Waterhouse S (1996) Characteristics of Sulfobacillus acidophilus sp. nov. and other moderately thermophilic mineral-sulphide-oxidizing bacteria. Microbiology 142:775–783

    CAS  PubMed  Google Scholar 

  • Norris PR, Burton NP, Foulis NAM (2000) Acidophiles in bioreactor mineral processing. Extremophiles 4:71–76

    Article  CAS  PubMed  Google Scholar 

  • Ohmura N, Kitamura K, Saiki H (1993) Selective adhesion of Thiobacillus ferrooxidans to pyrite. Appl Environ Microbiol 59:4044–4050

    Google Scholar 

  • Ohmura N, Sasaki K, Matsumoto N, Saiki H (2002) Anaerobic respiration using Fe3+, S0, and H2 in the chemolithoautotrophic bacterium Acidithiobacillus ferrooxidans. J Bacteriol 184:2081–2087

    Article  CAS  PubMed  Google Scholar 

  • Olson GJ, Brierley JA, Brierley CL (2003) Progress in bioleaching: applications of microbial processes by the minerals industries. Appl Microbiol Biotechnol DOI 10.2007/s00253-003-1404-6

    Google Scholar 

  • Pronk JT, Meulenberg R, Hazeu W, Bos P, Kuenen JG (1990) Oxidation of reduced inorganic sulphur compounds by acidophilic thiobacilli. FEMS Microbiol Rev 75:293–306

    Article  CAS  Google Scholar 

  • Pronk JT, de Bruyn JC, Bos P, Kuenen JG (1992) Anaerobic growth of Thiobacillus ferrooxidans. Appl Environ Microbiol 58:2227–2230

    CAS  Google Scholar 

  • Rawlings DE (1997) Biomining: theory, microbes and industrial processes. Springer, Berlin Heidelberg New York

  • Rawlings DE (2002) Heavy metal mining using microbes. Annu Rev Microbiol 56:65–91

    Article  CAS  PubMed  Google Scholar 

  • 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 145:5–13

    CAS  PubMed  Google Scholar 

  • Rimstidt JD, Vaughan DJ (2003) Pyrite oxidation: a state-of-the-art assessment of the reaction mechanism. Geochim Cosmochim Acta 67:873–880

    Article  CAS  Google Scholar 

  • Rodriguez-Leiva M, Tributsch H (1988) Morphology of bacterial leaching patterns by Thiobacillus ferrooxidans on synthetic pyrite. Arch Microbiol 149:401–405

    CAS  Google Scholar 

  • 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 149:1699–1709

    Article  CAS  PubMed  Google Scholar 

  • Rohwerder T, Jozsa P-G, Gehrke T, Sand W (2002) Bioleaching. In: Bitton G (ed) Encyclopedia of environmental microbiology, vol 2. Wiley, New York, pp 632–641

  • 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

    Article  CAS  Google Scholar 

  • Sand W, Rohde K, Sobotke B, Zenneck C (1992) Evaluation of Leptospirillum ferrooxidans for leaching. Appl Environ Microbiol 58:85–92

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Sand W, Gehrke T, Jozsa P-G, Schippers A (2001) (Bio)chemistry of bacterial leaching—direct vs indirect bioleaching. Hydrometallurgy 59:159–175

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Schippers A, Sand W (1999) Bacterial leaching of metal sulfide proceeds by two indirect mechanisms via thiosulfate or via polysulfides and sulfur. Appl Environ Microbiol 65:319–321

    CAS  PubMed  Google Scholar 

  • Schippers A, Jozsa P-G, Sand W (1996) Sulfur chemistry in bacterial leaching of pyrite. Appl Environ Microbiol 62:3424–3431

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Singer PC, Stumm W (1970) Acidic mine drainage: the rate-determining step. Science 167:1121–1123

    CAS  Google Scholar 

  • SME (2000) Proceedings from the fifth international conference on acid rock drainage (ICARD), vol 1–2. Society for Mining, Metallurgy, and Exploration, Littleton, Colo.

  • 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

    Article  CAS  Google Scholar 

  • Steudel R (1996) Mechanism for the formation of elemental sulfur from aqueous sulfide in chemical and microbiological desulfurization processes. Ind Eng Chem Res 35:1417–1423

    Article  CAS  Google Scholar 

  • Vandevivere P, Kirchman DL (1993) Attachment stimulates exopolysaccharide synthesis by a bacterium. Appl Environ Microbiol 59:3280–3286

    CAS  Google Scholar 

  • Yamanaka T, Fukumori Y (1995) Molecular aspects of the electron transfer system which participates in the oxidation of ferrous ion by Thiobacillus ferrooxidans. FEMS Microbiol Rev 17:401–413

    Article  CAS  PubMed  Google Scholar 

  • Yamanaka T, Yano T, Kai M, Tamegai H, Sato A, Fukumori Y (1991) The electron transfer system in an acidophilic iron-oxidizing bacterium. In: Mukohata (ed) New era of bioenergetics. Academic Press, Tokyo, pp 223–246

  • Yarzábal A, Brasseur G, Bonnefoy V (2002a) Cytochromes c of Acidithiobacillus ferrooxidans. FEMS Microbiol Lett 209:189–195

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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Acknowledgements

Work in our laboratory was supported by grants from the German Bundesministerium für Bildung und Forschung (no. 1490954) and Deutsche Bundesstiftung Umwelt (no. 02042 and 05333) to W. Sand. We would like to thank A. Schippers (BGR, Hannover, Germany) for generously providing original drawings. We also gratefully acknowledge the helpful comments of two anonymous reviewers.

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  1. T. Rohwerder

    Present address: Center for Environmental Research Leipzig-Halle, Permoserstrasse 15, 04318 , Leipzig, Germany

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  1. Institut für Allgemeine Botanik und Botanischer Garten, Abteilung Mikrobiologie, Universität Hamburg, Ohnhorststrasse 18, 22609 , Hamburg, Germany

    T. Rohwerder, T. Gehrke, K. Kinzler & W. Sand

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Rohwerder, T., Gehrke, T., Kinzler, K. et al. Bioleaching review part A:. Appl Microbiol Biotechnol 63, 239–248 (2003). https://doi.org/10.1007/s00253-003-1448-7

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