Toward a mechanistic understanding of anaerobic nitrate-dependent iron oxidation: Balancing electron uptake and detoxification

Frontiers in Microbiology

Volumn 3, Issue FEB, 2012, Pages

  Carlson, Hans K ^a   Clark, lain C ^a,b   Melnyk, Ryan A ^a   Coates, John D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Berkeley   (United States)

Author keywords

Acidovorax; Electron sparing; Fe(II) oxidoreductase; NDFO; Nitrate dependent ferrous iron oxidation

Indexed keywords

EID: 84870229708     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00057     Document Type: Article

References (54)

1. Bartberger, M. D., Liu, W., Ford, E., Miranda, K. M., Switzer, C, Fukuto, J. M., Farmer, P. J., Wink, D. A., and Houk, K. N. (2002). The reduction potential of nitric oxide (NO) and its importance to NO biochemistry. Proc. Natl. Acad. Sci. U.S.A. 99, 10958-10963.
2. Beckman, J. S., and Koppenol, W. H. (1996). Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am. J. Pkysiol. 271, C1424-C1437.
3. Bird, L. J., Bonnefoy, V., and Newman, D. K. (2011). Bioenergetic challenges of microbial iron metabolisms. Trends Microbiol. 19, 330-340.
4. Brons, H. J., Hagen, W. R., and Zehn-der, A. J. (1991). Ferrous iron dependent nitric oxide production in nitrate reducing cultures of Escherichia colt. Arch. Microbiol. 155, 341-347.
5. Chakraborty, A., Roden, E. E., Schieber, J., and Picardal, F. (2011). Enhanced growth of Acidovomx sp. strain 2AN during nitrate-dependent Fe(II) oxidation in batch and continuous-flow systems. Appl. Environ. Microbiol. 77, 8548-8556.
6. Chalamet, A. (1973). Reduction sous atmosphere inerte de l'acide nitreux par les ions ferreux. Ann. Chimie 8, 353-358.
7. Chaudhuri,S. K., Lack, J. G.,andCoates, J. D. (2001). Biogenic magnetite formation through anaerobic biooxida-tion of Fe(II). Appl. Environ. Microbiol. 67, 2844-2848.
8. 2+. Appl. Environ. Microbiol. 71, 5267-5274.
9. Cooper, D. C, Picardal, F. W., Schim-melmann,A.,andCoby,A. J. (2003).Chemical and biological interactions during nitrate and goethite reduction by Shewanellaputrefaciens 200. Appl. Environ. Microbiol. 69, 3517-3525.
10. Crichton, R. R. (2009). Iron Metabolism: From Molecular Mechanisms to Clinical Consequences. Chichester: John Wiley & Sons.
11. Croal, L. R., Jiao, Y. Q., and Newman, D. K. (2007). The fox operon from Rhodobacter strain SW2 promotes phototrophic Fe(II) oxidation in Rhodobacter capsulatus SB1003. J. Bacterial. 189, 1774-1782.
12. Dutton, A. S., Fukuto, J. M., and Houk, K. N. (2005). Theoretical reduction potentials for nitrogen oxides from CBS-QB3 energetics and (C)PCM solvation calculations. Inorg. Chem. 44, 4024-4028.
13. Emerson, D., Fleming, E. J., and McBeth, J. M. (2010). Iron-oxidizing bacteria:an environmental and genomic perspective. Annu. Rev. Microbiol. 64, 561-583.
14. Feelisch, M. (1991). The biochemical pathways of nitric-oxide formation from nitrovaso dilators - appropriate choice of exogenous NO donors and aspects of preparation and handling of aqueous NO solutions. J. Cardiovasc. Pharmacol. 17, S25-S33.
15. Ferguson, S. J., and Ingledew, W J. (2008). Energetic problems faced by micro-organisms growing or surviving on parsimonious energy sources and at acidic pH: I. Acidithiobacillus ferrooxidans as a paradigm. Biochim. Biophys. Acta 1777, 1471-1479.
16. Finneran, K. T., Housewright, M. E., and Lovley, D. R. (2002). Multiple influences of nitrate on uranium solubility during bioremedia-tion of uranium-contaminated subsurface sediments. Environ. Microbiol. 4,510-516.
17. Flores-Santana, W., Salmon, D. J., Donzelli, S., Switzer, C. H., Basud-har, D., Ridnour, L., Cheng, R., Glynn, S. A., Paolocci, N., Fukuto, J. M., Miranda, K. M., and Wink, D. A. (2011). The specificity of nitroxyl chemistry is unique among nitrogen oxides in biological systems. Antioxid. Redox Signal. 14, 1659-1674.
18. Gardner, A. M., Helmick, R. A., and Gardner, P. R. (2002). Flavorubre-doxin, an inducible catalyst for nitric oxide reduction and detoxification in Escherichia coli. J. Biol Chem. 277, 8172-8177.
19. Gomes, C. M., Giuffre, A., Forte, E., Vicente, J. B., Saraiva, L. M., Brunori, M., and Teixeira, M. (2002). A novel type of nitric-oxide reductase. Escherichia coli flavorubredoxin. J. Biol. Chem. 277, 25273-25276.
20. 2+ at neutral pH under anoxic conditions. Arch. Microbiol. 166, 308-314.
21. Hansen, H. C. B., Borggaard, O. K., and Sorensen, J. (1994). Evaluation of the free-energy of formation of Fe(II)-Fe(III) hydroxide-sulfate (green rust) and its reduction of nitrite. Geochitn. Cosmochim. Acta 58,2599-2608.
22. Hansen, H. C. B., Guldberg, S., Erbs, M., and Koch, C. B. (2001). Kinetics of nitrate reduction by green rusts - effects of inter layer anion and Fe(II): Fe(III) ratio. Appl. Clay Sci. 18,81-91.
23. Hansen, H. C. B., Koch, C. B., Nanck-ekrogh, H., Borggaard, O. K., and Sorensen, J. (1996). Abiotic nitrate reduction to ammonium: key role of green rust. Environ. Sci. Technol. 30, 2053-2056.
24. Jiao, Y., and Newman, D. K. (2007). The pio operon is essential for phototrophic Fe(II) oxidation in Rhodopseudomonas palustris TIE-1. J. Bacterial. 189, 1765-1773.
25. Kappler, A., Johnson, C. M., Crosby, H. A., Beard, B. L., and Newman, D. K. (2010). Evidence for equilibrium iron isotope fractionation by nitrate-reducing iron(II)-oxidizing bacteria. Geochitn. Cosmochim. Acta 74, 2826-2842.
26. Kappler, A., and Newman, D. K. (2004). Formation of Fe(III)-minerals by Fe(II)-oxidizing photoautotrophic bacteria. Geochim. Cosmochim. Acta 68,1217-1226.
27. Kappler, A., Schink, B., and Newman, D. K. (2005). Fe(III)-mineralformation and cell encrustation by the nitrate-dependent Fe(II)-oxidizer strain BoFeNl. Geobiology 3, 235-245.
28. Koppenol, W. H. (1996). Thermodynamics of reactions involving nitrogen-oxygen compounds. Meth. Enzymol. 268, 7-12.
29. Kraft, B., Strous, M., and Tegetmeyer, H. E. (2011). Microbial nitrate respiration - genes, enzymes and environmental distribution. J. Biotechnol. 155, 104-117.
30. Lack, J. G., Chaudhuri, S. K., Chakraborty, R., Achenbach, L. A., and Coates, J. D. (2002). Anaerobic biooxidation of Fe(II) by Dechlorosoma suillum. Microbiol. Ecol. 43,424-431.
31. Machulla, G., Thieme, J., and Niemeyer, J. (1998). Interaction of microorganisms with soil colloids observed by X-ray microscopy, in X-Ray Microscopy and Spectroscopy, eds J. Thieme, G. Schmahl, D. Rudolph, and E. Umbach (Heidelberg: Springer-Verlag), 11-21-11-28.
32. Mills, P. C, Rowley, G., Spiro, S., Hinton, J. C, and Richardson, D. J. (2008). A combination of cytochrome c nitrite reductase (NrfA) and flavorubredoxin (NorV) protects Salmonella enterica serovar Typhimurium against killing by NO in anoxic environments. Microbiology 154, 1218-1228.
33. Miot, J., Benzerara, K., Morin, G., Bernard, S., Beyssac, O., Larquet, E., Kappler, A., and Guyot, F. (2009a). Transformation of vivianite by anaerobic nitrate-reducing iron-oxidizing bacteria. Geobiology 7, 373-384.
34. Miot, J., Benzerara, K., Morin, G., Kappler, A., Obst, M., Brown, G. E., and Guyot, F. (2009b). Iron biomineralization by neutrophilic nitrate-reducing iron-oxidizing bacteria. Geochim. Cosmochim. Acta 73, A884-A884.
35. Miot, J., MacLellan, K., Benzerara, K., and Boisset, N. (2011). Preservation of protein globules and pep-tidoglycan in the mineralized cell wall of nitrate-reducing, iron(II)-oxidizing bacteria: a cryo-electron microscopy study. Geobiology 9, 459-470.
36. Moraghan, J.T.,and Buresh.R.J. (1977). Chemical reduction of nitrite and nitrous-oxide by ferrous iron. Soil Sci. Soc. Am. J. 41,47-50.
37. Muehe, E. M., Gerhardt, S., Schink, B., and Kappler, A. (2009). Eco-physiology and the energetic benefit of mixotrophic Fe(II) oxidation by various strains of nitrate-reducing bacteria. FEMS Microbiol. Ecol. 70, 335-343.
38. Nies, D. H. (2003). Efflux-mediated heavy metal resistance in prokary-otes. FEMS Microbiol. Rev. 27, 313-339.
39. Ottley, C. J., Davison,W., and Edmunds, W. M. (1997). Chemical catalysis of nitrate reduction by iron(II). Geochim. Cosmochim. Acta 61, 1819-1828.
40. Poulain, A. J., and Newman, D. K. (2009). Rhodobacter capsulatus catalyzes light-dependent Fe(II) oxidation under anaerobic conditions as a potential detoxification mechanism. Appl. Environ. Microbiol. 75, 6639-6646.
41. Rodionov, D. A., Dubchak, I. L., Arkin, A P., Aim, E. J., and Gelfand, M. S. (2005). Dissimilatory metabo lism of nitrogen oxides in bacteria: comparative reconstruction of tran-scriptionalnetworks. PLoS Corn-put. Biol. 1, e55. doi:10.1371/jour-nal.pcbi.0010055
42. Schoepp-Cothenet, B., Lieutaud, C, Baymann, E, Vermeglio, A., Friedrich, T., Kramer, D. M., and Nitschke, W. (2009). Menaquinone as pool quinone in a purple bacterium. Proc. Natl. Acad. Sci. U.S.A 106,8549-8554.
43. Shafirovich, V., and Lymar, S. V. (2002). Nitroxyl and its anion in aqueous solutions: spin states, protic equilibria, and reactivities toward oxygen and nitric oxide. Proc. Natl. Acad. Sci. U.S.A. 99, 7340-7345.
44. Straub, K. L., Benz, M., Schink, B., and Widdel, F. (1996). Anaerobic, nitrate-dependent microbial oxidation of ferrous iron. Appl. Environ. Microbiol. 62, 1458-1460.
45. Straub, K.L., and Buchholz-Cleven, B E. E. (1998). Enumeration and detection of anaerobic ferrous iron-oxidizing, nitrate-reducing bacte riafrom diverse European sedi ments. Appl. Environ. Microbiol. 64, 4846-4856.
46. Summers, D. P., and Chang, S. (1993). Prebiotic ammonia from reduction of nitrite by iron (II) on the early Earth. Nature 365, 630-633.
47. Turk, T., and Hollocher, T. C. (1992). Oxidation of dithiothreitol during turnover of nitric oxide reductase: evidence for generation of nitroxyl with the enzyme from Paracoccus denitrificans. Biochem. Biophys. Res. Commun. 183, 983-988.
48. Wagner, G. C, Kassner, R. J., and Kamen, M. D. (1974). Redox potentials of certain vitamins K: implications for a role in sulfite reduction by obligately anaerobic bacteria. Proc. Natl. Acad. Sci. U.S.A. 71, 253-256.
49. Weber, K. A., Achenbach, L. A., and Coates, J. D. (2006a). Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat. Rev. Microbiol. 4, 752-764.
50. Weber, K. A., Pollock, J., Cole, K. A., O'Connor, S. M., Achenbach, L. A., and Coates, J. D. (2006b). Anaerobic nitrate-dependent iron(II) bio-oxidation by a novel lithoautotrophic betaproteobacterium, strain 2002. Appl. Environ. Microbiol. 72, 686-694.
51. Weber, K. A., Urrutia, M. M., Churchill, P. E, Kukkadapu, R. K., and Roden, E. E. (2006c). Anaerobic redox cycling of iron by freshwater sediment microorganisms. Environ. Microbiol. 8, 100-113.
52. Weber, K. A., Hedrick, D. B., Peacock, A. D., Thrash, J. C, White, D. C, Achenbach, L. A., and Coates, J. D. (2009). Physiological and taxonomic description of the novel autotrophic, metal oxidizing bacterium, Pseudogulbenkiania sp. strain 2002. Appl. Microbiol. Biotechnol. 83, 555-565.
53. Weber, K. A., Picardal, F. W., and Roden.E. E. (2001). Microbially catalyzed nitrate-dependent oxidation of biogenic solid-phase Fe(II) compounds. Environ. Sci. Technol. 35, 1644-1650.
54. Widdel, E, Schnell, S., Heising, S., Ehrenreich, A., Assmus, B., and Schink, B. (1993). Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362, 834-836.