Redox transformations of iron at extremely low pH: Fundamental and applied aspects

Frontiers in Microbiology

Volumn 3, Issue MAR, 2012, Pages

  Johnson, D Barrie ^a   Kanao, Tadayoshi ^a,b   Hedrich, Sabrina ^a  

^a BANGOR UNIVERSITY   (United Kingdom)

^b OKAYAMA UNIVERSITY   (Japan)

Author keywords

Acidophiles; Iron; Oxidation; Reduction

Indexed keywords

EID: 84868361590     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00096     Document Type: Article

References (61)

1. Amouric, A., Appia-Ayme, C., Yarzabal, A., and Bonnefoy, V. (2009). Regulation of the iron and sulfur oxidation pathways in the acidophilic Acidithiobacillus ferrooxidans. Adv. Mat. Res. 71-73; 163-166.
2. Amouric, A., Brochier-Armanet, C., Johnson, D. B., Bonnefoy, V., and Hallberg, K. B. (2011). 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.
3. Baker, B. J., Tyson, G. W., Webb, R. I., Flanagan, J., Hugenholtz, P., Allen, E. E., and Banfield, J. F. (2006). Lineages of acidophilic archaea revealed by community genomic analysis. Science 314, 1933-1935.
4. Bigham, J. M., Schwertmann, U., Traina, S. J., Winland, R. L., and Wolf, M. (1996). Schwertmannite and the chemical modeling of iron in acid sulfate waters. Geochim. Cosmochim. Acta 60,2111-2121.
5. Bonnefoy, V., and Holmes, D. S. (2011). Genomic insights into microbial iron oxidation and iron uptake strategies in extremely acidic environments. Environ. Microbiol. doi:10.1111/j.1462-2920.2011.02626.x
6. Bradford, M. M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
7. Bridge, T. A. M., and Johnson, D. B. (2000). Reductive dissolution of ferric iron minerals by Acidiphilium SJH. Geomicrobiol. J. 17, 193-206.
8. Brock, T. D., and Gustafson, J. (1976). Ferric iron reduction by sulfur- and iron-oxidizing bacteria. Appl. Environ. Microbiol. 32, 567-571.
9. Coupland, K., and Johnson, D. B. (2008). Evidence that the potential for dissimilatory ferric iron reduction is widespread among acidophilic heterotrophic bacteria. FEMS Microbiol. Lett. 279, 30-35.
10. Denef, V. J., Mueller, R. S., and Ban-field, J. F. (2010). AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature. ISME J. 4, 599-610.
11. Diez Ercilla, M., López Pamo, E., and Sánchez España, J. (2009). Pho-toreduction of Fe(III) in the acidic mine pit lake of San Telmo (Iberian Pyrite Belt): field and experimental work. Aquat. Geochem. 15, 391-419.
12. Dopson, M., Baker-Austin, C., Hind, A., Bowman, J. P., and Bond, P. L. (2004). Characterization of Fer-roplasma isolates and Ferroplasma acidarmanus sp. nov., extreme acidophiles from acid mine drainage and industrial bioleaching environments. Appl. Environ. Microbiol. 70, 2079-2088.
13. Drobner, E., Huber, H., and Stetter, K. O. (1990). Thiobacillus ferrooxidans, afacultative hydrogen oxidizer. Appl. Environ. Microbiol. 56, 2922-2923.
14. du Plessis, C. A., Slabbert, W., Hallberg, K. B., and Johnson, D. B. (2011). Ferredox: a biohydrometallurgical processing concept for limonitic nickel laterites. Hydrometallurgy 109,221-229.
15. Geller, W., Klapper, H., and Salomons, W. (eds). (1998). Acid Mining Lakes - Acid Mine Drainage, Limnology and Reclamation. Environmental Science Series. Berlin, Springer.
16. Golyshina, O. V.,Yakimov, M. M., Lüns-dorf, H., Ferrer, M., Nimtz, M., Timmis, K. N., Wray, V., Tindall, B. J., and Golyshin, P. N. (2009). Acidiplasma aeolicum gen. nov., sp. nov., a euryarchaeon of the family Ferroplasmaceae isolated from a hydrothermal pool, and transfer of Ferroplasma cupricumulans to Acidiplasma cupricumulans comb, nov. Int. J. Syst. Evol. Microbiol. 59, 2815-2823.
17. González-Toril, E., Llobet-Brossa, E., Casamayor, E. O., Amman, R., and Amils, R. (2003). Microbial ecology of an extreme acidic environment, the Tinto river. Appl. Environ. Microbiol. 69, 4853-4865.
18. Gross, W. (2000). Ecophysiology of algae living in highly acidic environments. Hydrobiology 433, 31-37.
19. Hallberg, K. B., Hedrich, S., and Johnson, D. B. (2011a). Acidiferribacter thiooxydans, gen. nov. sp. nov.; an acidophilic, thermo-tolerant, facultatively anaerobic iron- and sulfur-oxidizer of the family Ectoth-iorhodospiraceae. Extremophiles 15, 271-279.
20. Hallberg, K. B., Grail, B. M., Du Plessis, C., and Johnson, D. B. (2011b). Reductive dissolution of ferric iron minerals: a new approach for bioprocessing nickel laterites. Miner. Eng. 24, 620-624.
21. Hallberg, K. B., Thomson, H. E. C., Boeselt, I., and Johnson, D. B. (2001). Aerobic and anaerobic sulfur metabolism by acidophilic bacteria, in Biohydrometallurgy: Fundamentals, Technology and Sustainable Development, Pro cess Metallurgy 11A, eds V. S. T. Ciminelli and O. Garcia Jr. (Amsterdam: Elsevier), 423-431.
22. Hedrich, S., and Johnson, D. B. (2012). A modular continuous flow reactor system for the selective bio-oxidation and precipitation of iron in mine-impacted waters. Bioresour. Technol. 106, 44-49.
23. Hedrich, S., Schlömann, M., and Johnson, D. B. (2011). The iron-oxidizing proteobacteria. Microbiology 157, 1551-1564.
24. Heinzel, E., Hedrich, S., Janneck, E., Glombitza, F., Seifert, J., and Schlömann, M. (2009). Bacterial diversity in a mine water treatment plant. Appl. Environ. Microbiol. 75, 858-861.
25. Janneck, E., Arnold, I., Koch, T., Meyer, J., Burghard, D., Ehinger, S. (2010). Microbial synthesis of schwertman-nite from lignite mine water and its utilization for removal of arsenic from mine waters and for production of iron pigments, in Proceedings of the International Mine Water Association Symposium 2010: Mine Water and Innovative Thinking, eds C. Wolkersdorfer and A. Freund (Sydney: Cape Breton University Press), 131-134.
26. Johnson, D. B. (1995). Selective solid media for isolating and enumerating acidophilic bacteria. J. Microbiol. Methods 23, 205-218.
27. Johnson, D. B. (2010). The biogeochemistry of biomining, in Geomicrobiology: Molecular and Environmental Perspective, eds L. Barton and M. Mandl (Dordrecht: Springer), 401-426.
28. Johnson, D. B., and Bridge, T. A. M. (2002). Reduction of ferric iron by acidophilic heterotrophic bacteria: evidence for constitutive and inducible enzyme systems in Acidiphilium spp. J. Appl. Microbiol. 92,315-321.
29. Johnson, D. B., and Hallberg, K. B. (2009). Carbon, iron and sulfur metabolism in acidophilic microorganisms. Adv. Microb. Physiol. 54, 202-256.
30. Johnson, D. B., and McGinness, S. (1991). Ferric iron reduction by acidophilic heterotrophic bacteria. Appl. Environ. Microbiol. 57, 207-211.
31. Johnson, D. B., McGinness, S., and Ghauri, M. A. (1993). Biogeochem-ical cycling of iron and sulfur in leaching environments. FEMS Microbiol. Rev.11, 63-70.
32. Kanao, T., Kamimura, K., and Sugio, T. (2007). Identification of a gene encoding a tetrathionate hydrolase in Acidithiobacillus ferrooxidans. J. Biotechnol. 132, 16-22.
33. Kelly, D. P. (1978). Bioenergetics of chemolithotrophic bacteria, in Companion to Microbiology; Selected Topics for Further Discussion, eds A. T. Bull and P. M. Meadow (London: Longman), 363-386.
34. Kimura, S., Bryan, C. G., Hallberg, K. B., and Johnson, D. B. (2011). Biodiversity and geochemistry of an extremely acidic, low temperature subterranean environment sustained by chemolithotro-phy. Environ. Microbiol. 13, 2092-2104.
35. Küsel, K. (2003). Microbial cycling of iron and sulfur in acidic coal mining lake sediments. Water Air Soil Pollut. 3, 67-90.
36. Küsel, K., Dorsch, T., Acker, G., and Stackebrandt, E. (1999). Microbial reduction of Fe(III) in acidic sediments: isolation of Acidiphilium cryptum JF-5 capable of coupling the reduction of Fe(III) to the oxidation of glucose. Appl. Environ. Microbiol. 65, 3633-3640.
37. Küsel, K., Roth, U., and Drake, H. (2002). Microbial reduction of Fe(III) in the presence of oxygen under low pH conditions. Environ. Microbiol. 4, 414-421.
38. Lovley, D. R., and Phillips, E. J. P. (1987). Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl. Environ. Microbiol. 53, 1536-1540
39. Lu, S., Gischkat, S., Reiche, M., Akob, D. M., Hallberg, K. B., and Küsel, K. (2010). Ecophysiology of Fe-cycling bacteria in acidic sedi ments. Appl. Environ. Microbiol. 76, 8174-8183.
40. Macalady, J. L., Jones, D. S., and Lyon, E H. (2007). Extremely acidic, pen dulous cave wall biofilms from the Frasassi cave system, Italy. Environ. Microbiol. 9, 1402-1414.
41. Magnuson, T. S., Swenson, M. W., Paszczynski, A. J., Deobald, L. A., Kerk, D., and Cummings, D. E. (2010). Proteogenomic and functional analysis of chro-mate reduction in Acidiphilium cryptum JF-5, an Fe(III)-respiring acidophile. Biometals 23, 1129-1138.
42. Meier, J., Babenzien, H. D., and Wendt-Potthoff, K. (2004). Microbial cycling of iron and sulfur in sediments of acidic and pH-neutral mining lakes in Lusatia (Brandenburg, Germany). Biogeochemistry 67, 135-156.
43. Monhemius, A. J. (1977). Precipitation diagrams for metal hydroxides, sulfides, arsenates and phosphates. Trans. Inst. Min. Metall. 86, C202-C206.
44. Nancucheo, I., and Johnson, D. B. (2010). Production of glycolic acid by chemolithotrophic iron- and sulfur-oxidizing bacteria and its role in delineating and sustaining acidophilic sulfide mineral-oxidizing consortia. Appl. Environ. Microbiol. 76, 461-467.
45. Nancucheo, I., and Johnson, D. B. (2011). Safeguarding reactive mine tailings by ecological engineering: the significance of microbial communities and interactions. Appl. Environ. Microbiol. 77, 8201-8208.
46. Nicolle, J. L. C., Simmons, S., Bathe, S., and Norris, P. R. (2009). Ferrous iron oxidation and rusticyanin in halotolerant, acidophilic Thiobacil-lus prosperous. Microbiology 155, 1302-1309.
47. 2 in the chemolithotrophic bacterium Acidithiobacillus ferrooxidans. J. Bac-teriol. 184,2081-2087.
48. Okibe, N., and Johnson, D. B. (2004). Biooxidation of pyrite by defined mixed cultures of moderately thermophilic acidophiles in pH-controlled bioreactors: the significance of microbial interactions. Biotechnol. Bioeng. 87, 574-583.
49. Okibe, N., and Johnson, D. B. (2011). A rapid ATP-based method for determining active microbial populations in mineral leach liquors. Hydrometallurgy 108, 195-198.
50. Pronk, J. T., Liem, K., Bos, P., and Kuenen, J. G. (1991). Energy trans-duction by anaerobic ferric iron reduction in Thiobacillus ferrooxidans. Appl. Environ. Microbiol. 57, 2063-2068.
51. Rawlings, D. E. (2002). Heavy metal mining using microbes. Annu. Rev. Microbiol. 56,65-91.
52. Rawlings, D. E., and Johnson, D. B. (eds). (2007a). Biomining. Heidelberg: Springer-Verlag.
53. Rawlings, D. E., and Johnson, D. B. (2007b). The microbiology of biomining: development and optimization of mineral-oxidizing microbial consortia. Microbiology 153, 315-324.
54. Regenspurg, S., Brand, A., and Peiffer, S. (2004). Formation and stability of schwertmannite in acidic mining lakes. Geochim. Cosmochim. Acta 68, 1185-1197.
55. Rohwerder, T., Gehrke, T., Kinzler, K., and Sand, W. (2003). Bioleaching review part A: progress in bioleaching: fundamentals and mechanisms of bacterial metal sufide oxidation. Appl. Microbiol. Biotechnol. 63, 239-248.
56. Rowe, O. F., and Johnson, D. B. (2008). Comparison of ferric iron generation by different species of acidophilic bacteria immobilised in packed-bed reactors. Syst. Appl. Microbiol. 31,68-77.
57. Rowe, O. F., Sánchez-España, J., Hall-berg, K. B., and Johnson, D. B. (2007). Microbial communities and geochemical dynamics in an extremely acidic, metal-rich stream at an abandoned sulfide mine (Huelva, Spain) underpinned by two functional primary production systems. Environ. Microbiol. 9, 1761-1771.
58. San Martin-Uriz, P., Gomez, M. J., Arcas, A., Bargiela, R., and Amils, R. (2011). Draft genome Sequence of the electricigen Acidiphilium sp. strain PM (DSM 24941).J. Bacteriol. 193,5585-5586.
59. Stumm, W., and Morgan, J. J. (1981). Aquatic Chemistry: An Introduction Emphasizing Chemical Equilibria in Natural Waters. New York: Wiley.
60. Welham, N. J., Malatt, K. A., and Vukcevic, S. (2000). The effect of solution speciation on iron-sulfur-arsenic-chloride systems at 298 K. Hydrometallurgy 57, 209-223.
61. Yarzábal, A., Appia-Ayme, C., Ratouchniak, J., and 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.