Progress in bioleaching: Fundamentals and mechanisms of bacterial metal sulfide oxidation-part A

Applied Microbiology and Biotechnology

Volumn 97, Issue 17, 2013, Pages 7529-7541

  Vera, Mario ^a   Schippers, Axel ^b   Sand, Wolfgang ^a  

^a UNIVERSITY OF DUISBURG ESSEN   (Germany)

^b FEDERAL INSTITUTE FOR GEOSCIENCES AND NATURAL RESOURCES BGR   (Germany)

Author keywords

Acidithiobacillus; Bioleaching; Extracellular polymeric substances; Metal sulfides

Indexed keywords

BACTERIA; BIOFILMS; BIOLEACHING; CELLS; CYTOLOGY; DISSOLUTION; IONS; METABOLISM; METALS; MOLECULAR OXYGEN; PYRITES;

ACIDITHIOBACILLUS; ACIDITHIOBACILLUS FERROOXIDANS; BIOLEACHING MICROORGANISMS; CELL-TO-CELL COMMUNICATION; EXTRA-CELLULAR POLYMERIC SUBSTANCES; METAL SULFIDE OXIDATIONS; METAL SULFIDES; MICROBIAL INTERACTIONS;

SULFUR COMPOUNDS;

IRON; METAL; POLYSULFIDE; PYRITE; SULFIDE; SULFUR; THIOSULFATE; UNCLASSIFIED DRUG;

BACTERIUM; BIOFILM; BIOTECHNOLOGY; CELL ORGANELLE; DISSOLUTION; ELECTRON; LEACHING; METABOLISM; MINERALOGY; MOLECULAR ANALYSIS; OXIDATION; PLANKTON; POLYMER; PYRITE; REDOX CONDITIONS; SULFIDE;

ANAEROBIC METABOLISM; BIOCHEMISTRY; BIOFILM; BIOLEACHING; CELL CONTACT; IRON METABOLISM; LEACHING; MICROORGANISM; NONHUMAN; ORGANISMAL INTERACTION; OXIDATION; POLYMERIZATION; REVIEW; SULFATE METABOLISM; SURFACE PROPERTY;

ACIDITHIOBACILLUS; ACIDITHIOBACILLUS FERROOXIDANS; BACTERIA (MICROORGANISMS);

BACTERIA; INDUSTRIAL MICROBIOLOGY; METALS; OXIDATION-REDUCTION; SULFIDES;

EID: 84892602773     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-4954-2     Document Type: Review

References (133)

1. 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
2. Alvarez S, Jerez CA (2004) Copper ions stimulate polyphosphate degradation and phosphate efflux in Acidithiobacillus ferrooxidans. Appl Environ Microbiol 70:5177-5182
3. 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
4. Andrews GF (1988) The selective adsorption of thiobacilli to dislocation sites on pyrite surfaces. Biotechnol Bioeng 31:378-381
5. 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
6. Bagdigian RM, Myerson AS (1986) The adsorption of Thiobacillus ferrooxidans on coal surfaces. Biotechnol Bioeng 28:467-479
7. 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
8. 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
9. Bellenberg S, Leon-Morales CF, Sand W, Vera M (2012) Visualization of capsular polysaccharide induction in Acidithiobacillus ferrooxidans. Hydrometallurgy 129-130:82-89
10. 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
11. 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
12. 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
13. 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
14. Bonnefoy V, Holmes DS (2011) Genomic insights into microbial iron oxidation and iron uptake strategies in extremely acidic environments. Environ Microbiol 14:1597-1611
15. Boon M, Heijnen JJ, Hansford GS (1998) The mechanism and kinetics of bioleaching sulphide minerals. Miner Process Extr Metall Rev 19:107-115
16. Borg RJ, Dienes GJ (1992) The physical chemistry of solids. Academic, Boston
17. Bosecker K (1997) Bioleaching: metal solubilization by microorganisms. FEMS Microbiol Rev 20:591-604
18. 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
19. 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
20. 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
21. Clark DA, Norris PR (1996) Acidimicrobium ferrooxidans gen. nov., sp. nov.: mixed-culture ferrous iron oxidation with Sulfobacillus species. Microbiology 142:785-790
22. 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
23. 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
24. 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
25. Dispirito AA, Dugan PR, Tuovinen OH (1983) Sorption of Thiobacillus ferrooxidans to particulate material. Biotechnol Bioeng 25:1163-1168
26. Dopson M, Johnson DB (2012) Biodiversity, metabolism and applications of acidophilic sulfur-metabolizing microorganisms. Environ Microbiol 14:2620-2631
27. Druschel GK (2002) Sulfur biogeochemistry: kinetics of intermediate sulfur species reactions in the environment. PhD thesis, University of Wisconsin
28. 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
29. du Plessis CA, Slabbert W, Hallberg KB, Johnson DB (2011) Ferredox: a biohydrometallurgical processing concept for limonitic nickel laterites. Hydrometallurgy 109:221-229
30. Dutrizac JE, MacDonald RJC (1974) Ferric ion as a leaching medium. Miner Sci Eng 6:59-100
31. 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
32. Edwards KJ, Bond PL, Gihring TM, Banfield JF (2000) An archaeal iron-oxidizing extreme acidophile important in acid mine drainage. Science 287:1796-1799
33. 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
34. Ehrlich HL (2009) Geomicrobiology, 5th edn. CRC, Boca Raton
35. Evangelou VPB (1995) Pyrite oxidation and its control. CRC, Boca Raton
36. 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
37. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623-633
38. 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
39. Fowler TA, Holmes PR, Crundwell FK (1999) Mechanism of pyrite dissolution in the presence of Thiobacillus ferrooxidans. Appl Environ Microbiol 65:2987-2993
40. 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
41. 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
42. 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, cellwall-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
43. 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
44. Hackl RP, Dreisinger DB, Peters E, King JA (1995) Passivation of chalcopyrite during oxidative leaching in sulfate media. Hydrometallurgy 39:25-48
45. Hallberg KB, Gonzalez-Toril E, Johnson DB (2009) Acidithiobacillus ferrivorans, sp. nov.; facultatively anaerobic, psychrotolerant iron-, and sulfur-oxidizing acidophiles isolated from metal mineimpacted environments. Extremophiles 14:9-19
46. 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
47. 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
48. 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
49. 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
50. 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
51. Harrison AP Jr (1982) Genomic and physiological diversity amongst strains of Thiobacillus ferrooxidans, and genomic comparison with Thiobacillus thiooxidans. Arch Microbiol 131:68-76
52. Hedrich S, Schlömann M, Johnson DB (2011) The iron-oxidizing proteobacteria. Microbiology 157:1551-1564
53. 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
54. Hiraishi A, Matsuzawa Y, Kanbe T, Wakao N (2000) Acidisphaera rubrifaciens gen. nov., sp. nov., an aerobic bacteriochlorophyllcontaining bacterium isolated from acidic environments. Int J Syst Evol Microbiol 50:1539-1546
55. Hiraishi A, Shimada K (2001) Aerobic anoxygenic photosynthetic bacteria with zinc-bacteriochlorophyll. J Gen Appl Microbiol 47:161-180
56. 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
57. Johnson DB, Hallberg KB (2005) Acid mine drainage remediation options: a review. Sci Total Environ 338:3-14
58. Johnson DB (2011) Geomicrobiology of extremely acidic subsurface environments. FEMS Microbiol Ecol 81:2-12
59. Johnson DB, Kanao T, Hedrich S (2012) Redox transformations of iron at extremely low pH: fundamental and applied aspects. Front Microbiol 3:96
60. 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
61. 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
62. Liljeqvist M, Valdes J, Holmes DS, Dopson M (2011) Draft genome of the psychrotolerant acidophile Acidithiobacillus ferrivorans SS3. J Bacteriol 193:4304-4305
63. 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
64. 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
65. Lowson RT (1982) Aqueous oxidation of pyrite by molecular oxygen. Chem Rev 82:461-497
66. Luther GW III (1987) Pyrite oxidation and reduction: molecular orbital theory considerations. Geochim Cosmochim Acta 51:3193-3199
67. 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
68. 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
69. Meruane G, Salhe C, Wiertz J, Vargas T (2002) Novel electrochemical- enzymatic model which quantifies the effect of the solution Eh on the kinetics of ferrous iron oxidation with Acidithiobacillus ferrooxidans. Biotechnol Bioeng 80:280-288
70. 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
71. 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
72. 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
73. 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
74. 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
75. 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
76. Norris PR, Burton NP, Foulis NAM (2000) Acidophiles in bioreactor mineral processing. Extremophiles 4:71-76
77. Ohmura N, Kitamura K, Saiki H (1993) Selective adhesion of Thiobacillus ferrooxidans to pyrite. Appl Environ Microbiol 59:4044-4050
78. 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
79. 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
80. 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
81. Orell A, Navarro CA, Rivero M, Aguilar JS, Jerez CA (2012) Inorganic polyphosphates in extremophiles and their possible functions. Extremophiles 16:573-583
82. 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
83. Pronk JT, de Bruyn JC, Bos P, Kuenen JG (1992) Anaerobic growth of Thiobacillus ferrooxidans. Appl Environ Microbiol 58:2227-2230
84. 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
85. Rawlings DE (1997) Biomining: theory, microbes and industrial processes. Springer, Berlin
86. 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
87. Rawlings DE (2002) Heavy metal mining using microbes. Annu Rev Microbiol 56:65-91
88. Remonsellez F, Orell A, Jerez CA (2006) Copper tolerance of the thermoacidophilic archaeon Sulfolobus metallicus: possible role of polyphosphate metabolism. Microbiology 152:59-66
89. Rimstidt JD, Vaughan DJ (2003) Pyrite oxidation: a state-of-the-art assessment of the reaction mechanism. Geochim Cosmochim Acta 67:873-880
90. Rodriguez-Leiva M, Tributsch H (1988) Morphology of bacterial leaching patterns by Thiobacillus ferrooxidans on synthetic pyrite. Arch Microbiol 149:401-405
91. Rohwerder T, Gehrke T, Kinzler K, SandW(2003) Bioleaching review part A: progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation. Appl Microbiol Biotechnol 63:239-248
92. 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
93. Rossi G (1990) Biohydrometallurgy. McGraw-Hill, Hamburg
94. Rossi G (1993) Biodepyritization of coal: achievements and problems. Fuel 72:1581-1592
95. 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 mineraladhesion efficiency. Hydrometallurgy 94:133-137
96. 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
97. 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
98. Sand W, Rohde K, Sobotke B, Zenneck C (1992) Evaluation of Leptospirillum ferrooxidans for leaching. Appl Environ Microbiol 58:85-92
99. 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
100. Sand W, Gehrke T, Jozsa PG, Schippers A (2001) (Bio)chemistry of bacterial leaching-direct vs. indirect bioleaching. Hydrometallurgy 59:159-175
101. Sand W, Jozsa PG, Kovacs ZM, Sǎsǎran N, Schippers A (2007) Longterm evaluation of acid rock drainage mitigation measures in large lysimeters. J Geochem Explor 92:205-211
102. 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
103. Schippers A, Jozsa P, Sand W (1996) Sulfur chemistry in bacterial leaching of pyrite. Appl Environ Microbiol 62:3424-3431
104. 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
105. 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
106. Schippers A, Jozsa PG, Kovacs ZM, Jelea M, Sand W (2001) Largescale experiments for microbiological evaluation of measures for safeguarding sulfidic mine waste. Waste Manage 21:139-146
107. 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
108. 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
109. 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
110. 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
111. Singer PC, Stumm W (1970) Acidic mine drainage: the ratedetermining step. Science 167:1121-1123
112. 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
113. 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
114. 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
115. 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
116. Taylor ES, Lower SK (2008) Thickness and surface density of extracellular polymers on Acidithiobacillus ferrooxidans. Appl Environ Microbiol 74:309-311
117. 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
118. 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
119. Thurston RS, Mandernack KW, Shanks WC III (2010) Laboratory chalcopyrite oxidation by Acidithiobacillus ferrooxidans: oxygen and sulfur isotope fractionation. Chem Geol 269:252-261
120. 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
121. 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
122. Tributsch H (2001) Direct versus indirect bioleaching. Hydrometallurgy 59:177-185
123. Vandevivere P, Kirchman DL (1993) Attachment stimulates exopolysaccharide synthesis by a bacterium. Appl Environ Microbiol 59:3280-3286
124. Vaughan DJ, Craig JR (1978) Mineral chemistry of metal sulfides. Cambridge University Press, Cambridge
125. Vera M, Guiliani N, Jerez CA (2003) Proteomic and genomic analysis of the phosphate starvation response of Acidithiobacillus ferrooxidans. Hydrometallurgy 71:125-132
126. 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
127. 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
128. Williamson MA, Rimstidt JD (1994) The kinetics and electrochemical rate-determing step of aqueous pyrite oxidation. Geochim Cosmochim Acta 58:5443-5454
129. Xu Y, Schoonen MAA (2000) The absolute energy positions of conduction and valence bands of selected semiconductiong minerals. Am Mineral 85:543-556
130. Yarzabal A, Brasseur G, Bonnefoy V (2002a) Cytochromes c of Acidithiobacillus ferrooxidans. FEMS Microbiol Lett 209:189-195
131. 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
132. 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
133. 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