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Biomining Microorganisms: Molecular Aspects and Applications in Biotechnology and Bioremediation

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Advances in Applied Bioremediation

Part of the book series: Soil Biology ((SOILBIOL,volume 17))

Abstract

The microbial solubilization of metals using chemolithoautotrophic microorganisms has successfully been used in industrial processes called biomining to extract metals such as copper, gold, uranium and others. The most studied leaching bacteria are from the genus Acidithiobacillus belonging to the Gram-negative γ-proteobacteria. Acidithiobacillus spp. obtain their energy from the oxidation of ferrous iron, elemental sulfur, or partially oxidized sulfur compounds. Other thermophilic archaeons capable of oxidizing sulfur and iron (II) have also been known for many years, and they are mainly from the genera Sulfolobus, Acidianus, Metallosphaera and Sulfurisphaera. Recently, some mesophilic iron (II)-oxidizing archaeons such as Ferroplasma acidiphilium and F. acidarmanus belonging to the Thermoplasmales have also been isolated and characterized. Recent studies of microorganisms consider them in their consortia, integrating fundamental biological knowledge with metagenomics, metaproteomics, and other data to obtain a global picture of how a microbial community functions. The understanding of microbial growth and activities in oxidizing metal ions will be useful for improving applied microbial biotechnologies such as biomining, bioshrouding, biomonitoring and bioremediation of metals in acidic environments.

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References

  • Akcil A, Koldas S (2006) Acid mine drainage (AMD): causes, treatment and case studies. J Clean Prod 14:1139–1145

    Article  Google Scholar 

  • Alvarez S, Jerez CA (2004) Copper ions stimulate polyphosphate degradation and phosphate efflux in Acidithiobacillus ferrooxidans. Appl Environ Microbiol 70:5177–5182

    Article  CAS  Google Scholar 

  • Barnes LJ, Janssen FJ, Sherren J, Versteegh JH, Koch RO, Scheeren PJH (1991) A new process for the microbial removal of sulphate and heavy metal from contaminated waters extracted by a geohydrological control system. Chem Eng Res Des 69A:184–186

    Google Scholar 

  • Bosio V, Viera M, Donati E (2007) Integrated bacterial process for the treatment of a spent nickel catalyst. J Hazard Mater 154:804–810

    Article  CAS  Google Scholar 

  • Bruscella P, Appia-Ayme C, Levicán G, Ratouchniak J, Jedlicki E, Holmes DS, Bonnefoy V (2007) Differential expression of two bc1 complexes in the strict acidophilic chemolithoautotrophic bacterium Acidithiobacillus ferrooxidans suggests a model for their respective roles in iron or sulfur oxidation. Microbiology 153:102–110

    Article  CAS  Google Scholar 

  • Butcher BG, Deane SM, Rawlings DE (2000) The chromosomal arsenic resistance genes of Thiobacillus ferrooxidans have an unusual arrangement and confer increased arsenic and antimony resistance to Escherichia coli. Appl Environ Microbiol 66:1826–1833

    Article  CAS  Google Scholar 

  • Cabrera G, Viera M, Gómez JM, Cantero D, Donati D (2007) Bacterial removal of chromium (VI) and (III) in a continuous system. Biodegradation 18:505–513

    Article  CAS  Google Scholar 

  • Cerruti C, Curutchet G, Donati E (1998) Bio-dissolution of spent nickel–cadmium batteries using Thiobacillus ferrooxidans. J Biotechnol 62:209–219

    Article  CAS  Google Scholar 

  • Chi A, Valenzuela L, Beard S, Mackey AJ, Shabanowitz J, Hunt DF, Jerez CA (2007) Periplasmic proteins of the extremophile Acidithiobacillus ferrooxidans: a high throughput proteomic analysis. Mol Cell Proteomics 6:2239–2251

    Article  CAS  Google Scholar 

  • Choi MS, Cho KS, Kim DS, Kim DJ (2004) Microbial recovery of copper from printed circuit boards of waste computer by Acidithiobacillus ferrooxidans. J Environ Sci Health A Tox Subst Environ Eng 39:2973–2982

    Article  CAS  Google Scholar 

  • Collinet MN, Morin D (1990) Characterization of arsenopyrite oxidizing Thiobacillus. Tolerance to arsenite, arsenate, ferrous and ferric iron. Anton van Leeuwenh 57:237–244

    CAS  Google Scholar 

  • Darkwah L, Rowson NA, Hewitt CJ (2005) Laboratory scale bioremediation of acid mine water drainage from a disused tin mine. Biotechnol Lett 17:1251–1257

    Article  CAS  Google Scholar 

  • Das A, Modak JM, Natarajan KA (1998) Surface chemical studies of Thiobacillus ferrooxidans with reference to copper tolerance. Anton van Leeuwenh 73:215–222

    Article  CAS  Google Scholar 

  • Dopson M, Baker-Austin C, Koppineedi PR, Bond PL (2003) Growth in sulfidic mineral environments: metal resistance mechanisms in acidophilic micro-organisms. Microbiology 149:1959–1970

    Article  CAS  Google Scholar 

  • Dove PM, Rimstidt JD (1985) The solubility and stability of scorodite, FeAsO4• 2H2O. Am Mineralog 70:838–844

    CAS  Google Scholar 

  • Duquesne K, Lebrun S, Casiot C, Bruneel O, Personné JC, Leblanc M, Elbaz-Poulichet F, Morin G, Bonnefoy V (2003) Immobilization of arsenite and ferric iron by Acidithiobacillus ferrooxidans and its relevance to acid mine drainage. Appl Environ Microbiol 69:6165–6173

    Article  CAS  Google Scholar 

  • Ehrlich HL (1964) Bacterial oxidation of arsenopyrite and enargite. Econ Geol 59:1306–1312

    Article  CAS  Google Scholar 

  • Guiliani N, Casanova A, Demergasso C, Jerez CA (2001) Bacterial biosensor for arsenic biomonitoring: applications in Northern Chile. Biol Res 34:R–126

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Handelsman J (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68:669–685

    Article  CAS  Google Scholar 

  • Harms H, Wells MC, van der Meer JR (2006) Whole-cell living biosensors — are they ready for environmental application? Appl Microbiol Biotechnol 70:273–280

    Article  CAS  Google Scholar 

  • Jerez CA (2008) The use of genomics, proteomics and other OMIC technologies for the global understanding of biomining microorganisms. Hydrometallurgy 94:162–169

    Google Scholar 

  • Johnson DB, Hallberg KB (2005) Acid mine drainage remediation options: a review. Sci Total Environ 338:3–14

    Article  CAS  Google Scholar 

  • Johnson DB, Yajie L, Okibe N (2008) “Bioshrouding”: a novel approach for securing reactive mineral tailings. Biotechnol Lett 30:445–449

    Article  CAS  Google Scholar 

  • Kaur P, Rosen BP (1992) Plasmid-encoded resistance to arsenic and antimony. Plasmid 27:29–40

    Article  CAS  Google Scholar 

  • Kelly DP, Shergill JK, Lu W-P, Wood AP (1997) Oxidative metabolism of inorganic sulfur compounds by bacteria. Anton van Leeuwenh 71:95–107

    Article  CAS  Google Scholar 

  • Lloyd JR, Anderson RT, Macaskie LE (2005) Bioremediation of metals and radionuclids. In: Atlas RM, Philp J (eds) Bioremediation. Applied microbial solutions for real-world environmental cleanup. ASM Press, Washington DC, pp 293–317

    Google Scholar 

  • Lo I, Denef VJ, VerBerkmoes NC, Shah MB, Goltsman D, DiBartolo G, Tyson GW, Allen EE, Ram RJ, Detter JC, Richardson P, Thelen MP, Hettich RL, Banfield JF (2007) Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria. Nature 446:537–541

    Article  CAS  Google Scholar 

  • Lundgren DG (1980) Ore leaching by bacteria. Annu Rev Microbiol 34:263–283

    Article  CAS  Google Scholar 

  • Mishra D, Kim DJ, Ralph DE, Ahn JG, Rhee YH (2008) Bioleaching of metals from spent lithium ion secondary batteries using Acidithiobacillus ferrooxidans. Waste Manage 28:333–338

    Article  CAS  Google Scholar 

  • Müller FH, Bandeiras TM, Urich T, Teixeira M, Gomes CM, Kletzin A (2004) Coupling of the pathway of sulphur oxidation to dioxygen reduction: characterization of a novel membrane-bound thiosulphate:quinone oxidoreductase. Mol Microbiol 53:1147–1160

    Article  CAS  Google Scholar 

  • Norman NC (1998) Chemistry of arsenic, antimony and bismuth. J Natl Cancer Inst 40:453–463.

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Outten FW, Huffman DL, Hale JA, O’Halloran TV (2001) The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J Biol Chem 276:30670–30677

    Article  CAS  Google Scholar 

  • Puig S, Rees EM, Thiele DJ (2002) The ABCDs of periplasmic copper trafficking. Structure 10:1292–1295

    Article  CAS  Google Scholar 

  • Quatrini R, Lefimil C, Veloso FA, Pedroso I, Holmes DS, Jedlicki E (2007) Bioinformatic prediction and experimental verification of Fur-regulated genes in the extreme acidophile Acidithiobacillus ferrooxidans. Nucleic Acids Res 35:2153–2166

    Article  CAS  Google Scholar 

  • Quatrini R, Appia-Ayme C, Dennis Y, Ratouchniak J, Veloso F, Valdes J, Lefimil C, Silver S, Roberto F, Orellana O, Denizot F, Jedlicki E, Holmes D, Bonnefoy V (2006) Insights into the iron and sulfur energetic metabolism of Acidithiobacillus ferrooxidans by microarray transcriptome profiling. Hydrometallurgy 83:263–272

    Article  CAS  Google Scholar 

  • Ram RJ, VerBerkmoes NC, Thelen MP, Tyson GW, Baker BJ, Blake II RC, Shah M, Hettich RL, Banfield JF (2005) Community proteomics of a natural microbial biofilm. Science 308:1915–1920

    Article  CAS  Google Scholar 

  • Ramirez P, Guiliani N, Valenzuela L, Beard S, Jerez CA (2004) Differential protein expression during growth of Acidithiobacillus ferrooxidans on ferrous iron, sulfur compounds, or metal sulfides. Appl Environ Microbiol 70:4491–4498

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Rawlings DE (2005) Characteristics and adaptability of iron- and sulfur-oxidizing microorganisms used for the recovery of metals from minerals and their concentrates. Microb Cell Fact 4:13

    Article  CAS  Google Scholar 

  • Rawlings DE, Johnson DB (2007) The microbiology of biomining: development and optimization of mineral-oxidizing microbial consortia. Microbiology 153:315–324

    Article  CAS  Google Scholar 

  • Remonsellez F, Orell A, Jerez CA (2006) Copper tolerance of the thermoacidophilic archaeon Sulfolobus metallicus: possible role of polyphosphate metabolism. Microbiology 152:59–66

    Article  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  Google Scholar 

  • Rohwerder T, Sand W (2007) Oxidation of inorganic sulfur compounds in acidophilic prokaryotes. Eng Life Sci 7:301–309

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ruitenberg R, Buisman CJN (2000) Process for immobilizing arsenic waste. WO/2000/078402

    Google Scholar 

  • Ruiz LM, Valenzuela S, Castro M, Gonzalez A, Frezza M, Soulère L, Rohwerder T, Queneau Y, Doutheau A, Sand CW, Jerez CA, Guiliani N (2008) AHL communication is a widespread phenomenon in biomining bacteria species and seems to be involved in mineral-adhesion efficiency. Hydrometallurgy 94:133–137.

    Google Scholar 

  • Schippers A (2007) Microorganisms involved in bioleaching and nucleic acid-based molecular methods for their identification and quantification. In: Donati ER, Sand W (eds) Microbial processing of metal sulfides. Springer, Berlin, pp 3–33

    Chapter  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Silver M, Lundgren DG (1968) Sulfur-oxidizing enzyme of Ferrobacillus ferrooxidans (Thiobacillus ferrooxidans). Can J Biochem 46:457–461

    Article  CAS  Google Scholar 

  • Stocker J, Balluch D, Gsell M, Harms H, Feliciano J, Daunert S, Malik KA, van der Meer JR (2003) Development of a set of simple bacterial sensors for quantitative and rapid measurements of arsenite and arsenate in potable water. Environ Sci Technol 37:4743–4750

    Article  CAS  Google Scholar 

  • Streit WR, Schmitz RA (2005) Metagenomics — the key to the uncultured microbes. Curr Opin Microbiol 7:492–498

    Article  CAS  Google Scholar 

  • Sugio T, Katagiri T, Moriyama M, Zhèn YL, Inagaki K, Tano T (1987) Existence of a new type of sulfite oxidase which utilizes ferric ions as an electron acceptor in Thiobacillus ferrooxidans. Appl Environ Microbiol 54:153–157

    Google Scholar 

  • Suzuki I (1999) Oxidation of inorganic sulfur compounds: chemical and enzymatic reactions. Can J Microbiol 45:97–105

    Article  CAS  Google Scholar 

  • Suzuki I (2001) Microbial leaching of metals from sulfide minerals. Biotechnol Adv 19:119–132

    Article  CAS  Google Scholar 

  • Takeuchi F, Sugio T (2006) Volatilization and recovery of mercury from mercury-polluted soils and wastewaters using mercury-resistant Acidithiobacillus ferrooxidans strains SUG 2-2 and MON-1. Environ Sci 13:305–316

    CAS  Google Scholar 

  • Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM, Solovyev VV, Rubin EM, Rokhsar DS, Banfield JF (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37–43

    Article  CAS  Google Scholar 

  • Valenzuela L, Chi A, Beard S, Orell A, Guiliani N, Shabanowitz J, Hunt DF, Jerez CA (2006) Genomics, metagenomics and proteomics in biomining microorganisms. Biotechnol Adv 24:197–211

    Article  CAS  Google Scholar 

  • Valenzuela L, Chi A, Beard S, Shabanowitz J, Hunt DF, Jerez CA (2007) Differential-expression proteomics for the study of sulfur metabolism in the chemolithoautotrophic Acidithiobacillus ferrooxidans. In: Friedrich C, Dahl C (eds) Microbial sulfur metabolism. Springer, Berlin, pp 77–86

    Google Scholar 

  • Vera M, Pagliai F, Guiliani N, Jerez CA (2008) The chemolithoautotroph Acidithiobacillus ferrooxidans can survive under phosphate-limiting conditions by the expression of a C-P lyase operon allowing it to grow in phosphonates. Appl Environ Microbiol 74:1829–1835

    Article  CAS  Google Scholar 

  • Watling HR (2006) The bioleaching of sulphide minerals with emphasis on copper sulphides — a review. Hydrometallurgy 84:81–108

    Article  CAS  Google Scholar 

  • White CA, Sharman AK, Gadd GM (1998) An integrated microbial process for the bioremediation of soil contaminated with toxic metals. Nat Biotechnol 16:572–575

    Article  CAS  Google Scholar 

  • Wu J, Rosen BP (1991) The ArsR protein is a trans-acting regulatory protein. Mol Microbiol 5:1331–1336

    Article  CAS  Google Scholar 

  • Xu C, Rosen BP (1997) Dimerization is essential for DNA binding and repression by the ArsR metalloregulatory protein of Escherichia coli. J Biol Chem 272:15734–15738

    Article  CAS  Google Scholar 

  • Yagi K (2007) Applications of whole-cell bacterial sensors in biotechnology and environmental science. Appl Microbiol Biotechnol 73:1251–1258

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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Acknowledgements

Part of our work was supported by FONDECYT1030767 and 1070986, FONDEF D99I1026 and ICM P-05-001-F projects.

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Correspondence to Carlos A. Jerez .

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Jerez, C.A. (2009). Biomining Microorganisms: Molecular Aspects and Applications in Biotechnology and Bioremediation. In: Singh, A., Kuhad, R., Ward, O. (eds) Advances in Applied Bioremediation. Soil Biology, vol 17. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-89621-0_13

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