Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction

Nature Reviews Microbiology volume 4, pages 752–764 (2006)Cite this article

Key Points

  • The recent identification of anaerobic microbial Fe(II) oxidation closed a gap in the iron redox cycle. Together with microbial Fe(III) reduction, these metabolisms are now known to transcend phylogenetic boundaries and have been shown to contribute significantly to soil and sediment biogeochemistry and mineralogy in anaerobic environments.

  • It is now accepted that microorganisms primarily control iron redox chemistry in most environments. Under anoxic conditions, Fe(III) oxide minerals are reduced by Fe(III)-reducing microorganisms (FRM). The ubiquity of FRM and their phylogenetic diversity makes this microbial metabolism globally significant. FRM can use both organic (CO2) and inorganic (H2) electron donors. The microbially mediated reduction of Fe(III) oxide minerals can generate both aqueous and solid-phase Fe(II)-bearing minerals such as siderite.

  • Microbially mediated Fe(II) oxidation is carried out by Fe(II)-oxidizing microorganisms (FOM). FOM are ubiquitous and have been identified in many different environments. The aerobic microbial oxidation of Fe(II) has been known for more than 100 years, but anaerobic Fe(II) oxidation by FOM was only identified in the early 1990s. Anaerobic Fe(II) oxidation by FOM can occur in both the presence and absence of light. FOM can couple Fe(II) oxidation to the reduction of nitrate, perchlorate and chlorate. Nitrate-dependent FOM can oxidize solid-phase Fe(II), including Fe(II) associated with structural Fe in minerals such as almandine and staurolite. Biogenic Fe(II) oxide minerals include magnetite and hematite, and nitrate-dependent Fe(II) oxidation has been implicated as having a direct role in the formation of banded iron formations in Precambrian Earth.

  • Recent evidence indicates that both of these metabolic processes have direct bioremediative and biotechnological applications. Anaerobic oxidation of Fe(II) by FOM can lead to the precipitation of biogenic Fe(III) oxides such as goethite and hematite. This provides a mechanism for the immobilization of heavy metals and metalloids through co-precipitation or physical envelopment. The anaerobic formation of biogenic Fe(III)-oxide-containing minerals has therefore been identified as a plausible bioremediation strategy for heavy metals and radionuclides. In addition to the ability to utilize insoluble Fe(III) as an electron acceptor, FRM such as Geobacter spp. can alternatively pass electrons onto the surface of an electrode (anode). This has led to the development of microbial fuel cells for the generation of electricity. FRM can also transform various organic contaminants (including benzene, toluene and phenol) and heavy metal and radionuclide contaminants (including uranium) and so might also be useful in bioremediation.

Abstract

Iron (Fe) has long been a recognized physiological requirement for life, yet for many microorganisms that persist in water, soils and sediments, its role extends well beyond that of a nutritional necessity. Fe(II) can function as an electron source for iron-oxidizing microorganisms under both oxic and anoxic conditions and Fe(III) can function as a terminal electron acceptor under anoxic conditions for iron-reducing microorganisms. Given that iron is the fourth most abundant element in the Earth's crust, iron redox reactions have the potential to support substantial microbial populations in soil and sedimentary environments. As such, biological iron apportionment has been described as one of the most ancient forms of microbial metabolism on Earth, and as a conceivable extraterrestrial metabolism on other iron-mineral-rich planets such as Mars. Furthermore, the metabolic versatility of the microorganisms involved in these reactions has resulted in the development of biotechnological applications to remediate contaminated environments and harvest energy.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The microbially mediated iron redox cycle.
Figure 2: Potential electron donors and acceptors: a redox tower.
Figure 3: Phylogenetic affiliation of microorganisms contributing to iron redox cycling.
Figure 4: Microbial strategies mediating electron transfer to insoluble Fe(III) oxides.
Figure 5: Physiological model of the biochemistry involved in microbial Fe(III) reduction by Shewanella and Geobacter spp.

Similar content being viewed by others

References

  1. Cornell, R. M. & Schwertmann, U. The Iron Oxides: Structure, Properties, Reactions, Occurrences and Uses (Wiley-VCH, Weinheim, 2003).

    Book  Google Scholar 

  2. Stumm, W. & Morgan, J. J. Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters (John Wiley & Sons, New York, 1996).

    Google Scholar 

  3. Baker, B. J. & Banfield, J. F. Microbial communities in acid mine drainage. FEMS Microbiol. Ecol. 44, 139–152 (2003).

    Article  CAS  PubMed  Google Scholar 

  4. Chaudhuri, S. K., Lack, J. G. & Coates, J. D. Biogenic magnetite formation through anaerobic biooxidation of Fe(II). Appl. Environ. Microbiol. 67, 2844–2848 (2001). This paper gives the first demonstration of magnetite formation through anaerobic iron bio-oxidation and the first demonstration of the bioavailability of Fe( II ) in silicaceous minerals.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Lack, J. G. et al. Immobilization of radionuclides and heavy metals through anaerobic bio-oxidation of Fe(II). Appl. Environ. Microbiol. 68, 2704–2710 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Lovley, D. R., Holmes, D. E. & Nevin, K. P. Dissimilatory Fe(III) and Mn(IV) reduction. Adv. Microb. Physiol. 49, 219–286 (2004).

    Article  CAS  PubMed  Google Scholar 

  7. Canfield, D. E. et al. Pathways of organic carbon oxidation in three continental margin sediments. Mar. Geol. 113, 27–40 (1993). This paper gives the first demonstration of the importance of microbial Fe( III ) reduction for the oxidation of organic matter in marine sediments.

    Article  CAS  PubMed  Google Scholar 

  8. Clement, J., Shrestha, J., Ehrenfeld, J. & Jaffe, P. Ammonium oxidation coupled to dissimilatory reduction of iron under anaerobic conditions in wetland soils. Soil Biol. Biochem. 37, 2323–2328 (2005).

    Article  CAS  Google Scholar 

  9. Lovley, D. R. Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol. Rev. 55, 259–287 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Kukkadapu, R. K., Zachara, J. M., Smith, S. C., Fredrickson, J. K. & Liu, C. X. Dissimilatory bacterial reduction of Al-substituted goethite in subsurface sediments. Geochim. Cosmochim. Acta 65, 2913–2924 (2001).

    Article  CAS  Google Scholar 

  11. Mendelssohn, I. A., Kleiss, B. A. & Wakeley, J. S. Factors controlling the formation of oxidized root channels. Wetlands 15, 37–46 (1995).

    Article  Google Scholar 

  12. Furukawa, Y., Smith, A. C., Kostka, J. E., Watkins, J. & Alexander, C. R. Quantification of macrobenthic effects on diagenesis using a multicomponent inverse model in salt marsh sediments. Limnol. Oceanogr. 49, 2058–2072 (2004).

    Article  CAS  Google Scholar 

  13. Emerson, D., Weiss, J. V. & Megonigal, J. P. Iron-oxidizing bacteria are associated with ferric hydroxide precipitates (Fe-plaque) on the roots of wetland plants. Appl. Environ. Microbiol. 65, 2758–2761 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Weiss, J. V., Emerson, D., Backer, S. M. & Megonigal, J. P. Enumeration of Fe(II)-oxidizing and Fe(III)-reducing bacteria in the root zone of wetland plants: Implications for a rhizosphere iron cycle. Biogeochemistry 64, 77–96 (2003).

    Article  CAS  Google Scholar 

  15. Weiss, J. V., Emerson, D. & Megonigal, J. P. Rhizosphere iron(III) deposition and reduction in a Juncus effusus L.-dominated wetland. Soil Sci. Soc. Am. J. 69, 1861–1870 (2005).

    Article  CAS  Google Scholar 

  16. Ghiorse, W. C. Biology of iron-depositing and manganese-depositing bacteria. Ann. Rev. Microbiol. 38, 515–550 (1984).

    Article  CAS  Google Scholar 

  17. Emerson, D. & Moyer, C. L. Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH. Appl. Environ. Microbiol. 63, 4784–4792 (1997). This paper demonstrates the unsuspected ubiquity and diversity of organisms capable of microaerophilic Fe( II ) bio-oxidation at circumneutral pH.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Sobolev, D. & Roden, E. E. Suboxic deposition of ferric iron by bacteria in opposing gradients of Fe(II) and oxygen at circumneutral pH. Appl. Environ. Microbiol. 1328–1334 (2001).

  19. Edwards, K. J., Rogers, D. R., Wirsen, C. O. & McCollom, T. M. Isolation and characterization of novel psychrophilic, neutrophilic, Fe-oxidizing, chemolithoautotrophic α- and γ-Proteobacteria from the deep sea. Appl. Environ. Microbiol. 69, 2906–2913 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Widdel, F. et al. Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362, 834–836 (1993). This paper gives the first demonstration of anaerobic, phototrophic Fe( II ) oxidation and suggests the importance of this metabolism in the Earth's early history.

    Article  CAS  Google Scholar 

  21. Straub, K. L., Benz, M., Schink, B. & Widdel, F. Anaerobic, nitrate-dependent microbial oxidation of ferrous iron. Appl. Environ. Microbiol. 62, 1458–1460 (1996). This paper gives the first clear demonstration of anaerobic, mesophilic nitrate-dependent Fe( II ) oxidation.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Senn, D. B. & Hemond, H. F. Nitrate controls on iron and arsenic in an urban lake. Science 296, 2373–2376 (2002).

    Article  CAS  PubMed  Google Scholar 

  23. Straub, K. L., Schonhuber, W., Buchholz-Cleven, B. & Schink, B. Diversity of ferrous iron-oxidizing, nitrate-reducing bacteria and their involvement in oxygen-independent iron cycling. Geomicrobiol. J. 21, 371–378 (2004).

    Article  CAS  Google Scholar 

  24. Weber, K. A., Urrutia, M. M., Churchill, P. F., Kukkadapu, R. K. & Roden, E. E. Anaerobic redox cycling of iron by freshwater sediment microorganisms. Environ. Microbiol. 8, 100–113 (2006).

    Article  CAS  PubMed  Google Scholar 

  25. Weber, K. A., Picardal, F. W. & Roden, E. E. Microbially catalyzed nitrate-dependent oxidation of biogenic solid-phase Fe(II) compounds. Environ. Sci. Technol. 35, 1644–1650 (2001).

    Article  CAS  PubMed  Google Scholar 

  26. Bruce, R. A., Achenbach, L. A. & Coates, J. D. Reduction of (per)chlorate by a novel organism isolated from paper mill waste. Environ. Microbiol. 1, 319–329 (1999).

    Article  CAS  PubMed  Google Scholar 

  27. Shelobolina, E. S., VanPraagy, C. G. & Lovley, D. R. Use of ferric and ferrous iron containing minerals for respiration by Desulfitobacterium frappieri. Geomicrobiol. J. 20, 143–156 (2003).

    Article  CAS  Google Scholar 

  28. Harrison Jr, A. P. The acidophilic Thiobacilli and other acidophilic bacteria that share their habitat. Ann. Rev. Microbiol. 38, 265–292 (1984).

    Article  CAS  Google Scholar 

  29. Davison, W. & Seed, G. The kinetics of the oxidation of ferrous iron in synthetic and natural waters. Geochim. Cosmochim. Acta 47, 67–79 (1983).

    Article  CAS  Google Scholar 

  30. Emerson, D. & Weiss, J. V. Bacterial iron oxidation in circumneutral freshwater habitats: findings from the field and the laboratory. Geomicrobiol. J. 21, 405–414 (2004).

    Article  CAS  Google Scholar 

  31. Hafenbradl, D. et al. Ferroglobus placidus gen. nov., sp. nov. a novel hyperthermophilic archaeum that oxidizes Fe(II) at neutral pH under anoxic conditions. Arch. Microbiol. 166, 308–314 (1996). This paper describes the first isolation of a hyperthermophilic anaerobic, nitrate-dependent Fe( II )-oxidizing organism and the only archaeum known to be capable of this metabolism.

    Article  CAS  PubMed  Google Scholar 

  32. Jiao, Y., Kappler, A., Croal, L. R. & Newman, D. K. Isolation and characterization of a genetically tractable photoautotrophic Fe(II)-oxidizing bacterium, Rhodopseudomonas palustris strain TIE-1. Appl. Environ. Microbiol. 71 4487–4496 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Ehrenreich, A. & Widdel, F. Anaerobic oxidation of ferrous iron by purple bacteria, a new type of phototrophic metabolism. Appl. Environ. Microbiol. 60, 4517–4526 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Heising, S. & Schink, B. Phototrophic oxidation of ferrous iron by a Rhodomicrobium vannielii strain. Microbiology 144, 2263–2269 (1998).

    Article  CAS  PubMed  Google Scholar 

  35. Heising, S., Richter, L., Ludwig, W. & Schink, B. Chlorobium ferrooxidans sp. nov., a phototrophic green sulfur bacterium that oxidizes iron in coculture with a 'Geospirillum' sp. strain. Arch. Microbiol. 172, 116–124 (1999).

    Article  CAS  PubMed  Google Scholar 

  36. Straub, K. L., Rainey, F. A. & Widdel, F. Rhodovulum iodosum sp. nov, and Rhodovulum robiginosum sp. nov., two new marine phototrophic ferrous-iron-oxidizing purple bacteria. Int. J. Syst. Bacteriol. 49, 729–735 (1999).

    Article  CAS  PubMed  Google Scholar 

  37. Straub, K. L., Benz, M. & Schink, B. Iron metabolism in anoxic environments at near neutral pH. FEMS Microbiol. Ecol. 34, 181–186 (2001).

    Article  CAS  PubMed  Google Scholar 

  38. Kappler, A. & Newman, D. K. Formation of Fe(III)-minerals by Fe(II)-oxidizing photoautotrophic bacteria. Geochim. Cosmochim. Acta 68, 1217–1226 (2004).

    Article  CAS  Google Scholar 

  39. Ciania, A., Gossa, K.-U. & Schwarzenbach, R. P. Light penetration in soil and particulate minerals. Eur. J. Soil Sci. 53, 561–574 (2005).

    Article  CAS  Google Scholar 

  40. Straub, K. L., Hanzlik, M. & Buchholz-Cleven, B. E. E. The use of biologically produced ferrihydrite for the isolation of novel iron-reducing bacteria. Syst. Appl. Microbiol. 21, 442–449 (1998).

    Article  CAS  PubMed  Google Scholar 

  41. Kluber, H. D. & Conrad, R. Effects of nitrate, nitrite, NO and N2O on methanogenesis and other redox processes in anoxic rice field soil. FEMS Microbiol. Ecol. 25, 301–318 (1998).

    Article  CAS  Google Scholar 

  42. Ratering, S. & Schnell, S. Nitrate-dependent iron(II) oxidation in paddy soil. Environ. Microbiol. 3, 100–109 (2001).

    Article  CAS  PubMed  Google Scholar 

  43. Finneran, K. T., Housewright, M. E. & Lovley, D. R. Multiple influences of nitrate on uranium solubility during bioremediation of uranium-contaminated subsurface sediments. Environ. Microbiol. 4, 510–516 (2002).

    Article  CAS  PubMed  Google Scholar 

  44. Weber, K. A. & Coates, J. D. in Manual of Environmental Microbiology, 3rd edn (eds Hurst, C. J., Crawford, R. L., Knudsen, G. R., McInerney, M. J. & Stetzenbach, L. D.) in the press (ASM Press).

  45. Weber, K. A. et al. Anaerobic nitrate-dependent iron(II) bio-oxidation by a novel, lithoautotrophic, β-proteobacterium, strain 2002. Appl. Environ. Microbiol. 72, 686–694 (2006). The first description of the only organism that has been clearly demonstrated to grow by mesophilic autotrophic nitrate-dependent Fe( II ) oxidation.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Beller, H. R. Anaerobic, nitrate-dependent oxidation of U(IV) oxide minerals by the chemolithoautotrophic bacterium Thiobacillus denitrificans. Appl. Environ. Microbiol. 71, 2170–2174 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Lack, J. G., Chaudhuri, S. K., Chakraborty, R., Achenbach, L. A. & Coates, J. D. Anaerobic biooxidation of Fe(II) by Dechlorosoma suillum. Microb. Ecol. 43, 424–431 (2002).

    Article  CAS  PubMed  Google Scholar 

  48. Coates, J. D. & Achenbach, L. A. Microbial perchlorate reduction: rocket-fuelled metabolism. Nature Rev. Microbiol. 2, 569–580 (2004).

    Article  CAS  Google Scholar 

  49. Vorholt, J. A., Hafenbradl, D., Stetter, K. O. & Thauer, R. K. Pathways of autotrophic CO2 fixation and dissimilatory nitrate reduction to N2O in Ferroglobus placidus. Arch. Microbiol. 167, 19–23 (1997).

    Article  CAS  PubMed  Google Scholar 

  50. Gold, T. The deep, hot biosphere. Proc. Natl Acad. Sci. USA 89, 6045–6049 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Cairns-Smith, A. G. Precambrian solution photochemistry, inverse segregation, and banded iron formations. Nature 276, 807–808 (1978).

    Article  CAS  Google Scholar 

  52. Vargas, M., Kashefi, K., Blunt-Harris, E. L. & Lovley, D. R. Microbiological evidence for Fe(III) reduction on early Earth. Nature 395, 65–67 (1998). Describes the first demonstration of dissimilatory Fe( III ) reduction by hyperthermophilic Archaea.

    Article  CAS  PubMed  Google Scholar 

  53. Lovley, D. R. in Origins: Genesis, Evolution and Diversity of Life (ed. Seckbach, J.) 707 (Kluwer Dordrecht, Boston, 2004).

    Google Scholar 

  54. Kashefi, K. & Lovley, D. R. Extending the upper temperature limit for life. Science 301, 934 (2003). Provides a description of the most heat-tolerant organism known, strain 121, which grows at 121oC.

    Article  CAS  PubMed  Google Scholar 

  55. Kashefi, K. & Lovley, D. Reduction of Fe(III), Mn(IV), and toxic metals at 100 degrees C by Pyrobaculum islandicum. Appl. Environ. Microbiol. 66, 1050–1056 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Tor, J. M., Kashefi, K. & Lovley, D. R. Acetate oxidation coupled to Fe(III) reduction in hyperthermophilic microorganisms. Appl. Environ. Microbiol. 67, 1363–1365 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Kostka, J. E., Stucki, J. W., Nealson, K. H. & Wu, J. Reduction of structural Fe(III) in smectite by a pure cultrue of Shewanella putrefaciens strain MR-1. Clays Clay Miner. 44, 522–529 (1996). This paper gives the first demonstration that structural Fe( III ) in clay minerals is bioavailable for dissimilatory microbial Fe( III ) reduction.

    Article  CAS  Google Scholar 

  58. Kostka, J. E. & Nealson, K. H. Dissolution and reduction of magnetite by bacteria. Environ. Sci. Technol. 29, 2535–2540 (1995).

    Article  CAS  PubMed  Google Scholar 

  59. Fredrickson, J. K. et al. Biogenic iron mineralization accompanying the dissimilatory reduction of hydrous ferric oxide by a groundwater bacterium. Geochim. Cosmochim. Acta 62, 3239–3257 (1998).

    Article  CAS  Google Scholar 

  60. Glasauer, S., Weidler, P. G., Langley, S. & Beveridge, T. J. Controls on Fe reduction and mineral formation by a subsurface bacterium. Geochim. Cosmochim. Acta 67, 1277–1288 (2003).

    Article  CAS  Google Scholar 

  61. Nevin, K. P. & Lovley, D. R. Lack of production of electron-shuttling compounds or solubilization of Fe(III) during reduction of insoluble Fe(III) oxide by Geobacter metallireducens. Appl. Environ. Microbiol. 66, 2248–2251 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Childers, S. E., Ciufo, S. & Lovley, D. R. Geobacter metallireducens accesses insoluble Fe(III) oxide by chemotaxis. Nature 416, 767–769 (2002).

    Article  CAS  PubMed  Google Scholar 

  63. Reguera, G. et al. Extracellular electron transfer via microbial nanowires. Nature 435, 1098–1101 (2005). Provides the first description of the nanowire concept involved in the transfer of electrons onto insoluble electron acceptors during microbial respiration.

    Article  CAS  PubMed  Google Scholar 

  64. Gorby, Y. A. et al. Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc. Natl. Acad. Sci. USA 103, 11358–11363 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Lovley, D. R., Coates, J. D., Blunt-Harris, E. L., Phillips, E. J. P. & Woodward, J. C. Humic substances as electron acceptors for microbial respiration. Nature 382, 445–448 (1996). This paper provides the first demonstration that bacteria can mediate the reduction of insoluble electron acceptors through the use of redox-active natural organic matter.

    Article  CAS  Google Scholar 

  66. Newman, D. K. & Kolter, R. A role for excreted quinones in extracellular electron transfer. Nature 405, 94–97 (2000).

    Article  CAS  PubMed  Google Scholar 

  67. Nevin, K. P. & Lovley, D. R. Mechanisms for accessing insoluble Fe(III) oxide during dissimilatory Fe(III) reduction by Geothrix fermentans. Appl. Environ. Microbiol. 68, 2294–2299 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Turick, C. E., Tisa, L. S. & Caccavo, F. Melanin production and use as a soluble electron shuttle for Fe(III) oxide reduction and as a terminal electron acceptor by Shewanella algae BrY. Appl. Environ. Microbiol. 68, 2436–2444 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Nevin, K. P. & Lovley, D. R. Potential for nonenzymatic reduction of Fe(III) via electron shuttling in subsurface sediments. Environ. Sci. Technol. 34, 2472–2478 (2000).

    Article  CAS  Google Scholar 

  70. Hernandez, M. E., Kappler, A. & Newman, D. K. Phenazines and other redox-active antibiotics promote microbial mineral reduction. Appl. Environ. Microbiol. 70, 921–928 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Hernandez, M. E. & Newman, D. K. Extracellular electron transfer. Cell. Mol. Life Sci. 58, 1562–1571 (2001).

    Article  CAS  PubMed  Google Scholar 

  72. Nevin, K. P. & Lovley, D. R. Mechanisms for Fe(III) oxide reduction in sedimentary environments. Geomicrobiol. J. 19, 141–159 (2002).

    Article  CAS  Google Scholar 

  73. Lovley, D. R., Fraga, J. L., Coates, J. D. & Blunt-Harris, E. L. Humics as an electron donor for anaerobic respiration. Environ. Microbiol. 1, 89–98 (1999).

    Article  CAS  PubMed  Google Scholar 

  74. Coates, J. D., Cole, K. A., Chakraborty, R., O'Connor, S. M. & Achenbach, L. A. The diversity and ubiquity of bacteria utilizing humic substances as an electron donor for anaerobic respiration. Appl. Environ. Microbiol. 68, 2445–2452 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Roh, Y. et al. Isolation and characterization of metal-reducing Thermoanaerobacter strains from deep subsurface environments of the Piceance Basin, Colorado. Appl. Environ. Microbiol. 68, 6013–6020 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Bowman, J. P. et al. Shewanella gelidimarina sp. nov. and Shewanella frigidimarina sp. nov., novel Antarctic species with the ability to produce eicosapentaenoic acid (20:5 omega 3) and grow anaerobically by dissimilatory Fe(III) reduction. Int. J. Syst. Bacteriol. 4, 1040–1047 (1997).

    Article  Google Scholar 

  77. Kusel, K., Dorsch, T., Acker, G. & Stackebrandt, E. 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 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Ye, Q. et al. Alkaline anaerobic respiration: Isolation and characterization of a novel alkaliphilic and metal-reducing bacterium. Appl. Environ. Microbiol. 70, 5595–5602 (2004).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. Gorlenko, V. et al. Anaerobranca californiensis sp nov., an anaerobic, alkalithermophilic, fermentative bacterium isolated from a hot spring on Mono Lake. Int. J. Syst. Evol. Microbiol. 54, 739–743 (2004).

    Article  CAS  PubMed  Google Scholar 

  80. Myers, C. R. & Nealson, K. H. Bacterial manganese reduction and growth with manganese oxide as the sole electron-acceptor. Science 240, 1319–1321 (1988).

    Article  CAS  PubMed  Google Scholar 

  81. Caccavo F. Jr, Blakemore, R. P. & Lovely, D. R. A hydrogen-oxidizing, Fe(III)-reducing microorganism from the Great Bay Estuary, New Hampshire. Appl. Environ. Microbiol. 58, 3211–3216 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Zachara, J. M. et al. Bacterial reduction of crystalline Fe(III) oxides in single phase suspensions and subsurface materials. Am. Mineral. 83, 1426–1443 (1998).

    Article  CAS  Google Scholar 

  83. Stein, L., La Duc, M., Grundl, T. & Nealson, K. Bacterial and archaeal populations associated with freshwater ferromanganous micronodules and sediments. Environ. Microbiol. 3, 10–18 (2001).

    Article  CAS  PubMed  Google Scholar 

  84. Snoeyenbos-West, O. L., Nevin, K. P., Anderson, R. T. & Lovley, D. R. Enrichment of Geobacter species in response to stimulation of Fe(III) reduction in sandy aquifer sediments. Microb. Ecol. 39, 153–167 (2000).

    Article  CAS  PubMed  Google Scholar 

  85. Roling, W., van Breukelen, B., Braster, M., Lin, B. & van Verseveld, H. Relationships between microbial community structure and hydrochemistry in a landfill leachate-polluted aquifer. Appl. Envir. Microbiol. 67, 4619–4629 (2001).

    Article  CAS  Google Scholar 

  86. Todorova, S. G. & Costello, A. M. Design of Shewanella specific 16S rRNA primers and application to analysis of Shewanella in a minerotrophic wetland. Environ. Microbiol. 8, 426–432 (2006).

    Article  CAS  PubMed  Google Scholar 

  87. Cummings, D., Caccavo, F., Spring, S. & Rosenzweig, R. Ferribacterium limneticum, gen. nov., sp. nov., an Fe(III)-reducing microorganism isolated from mining-impacted freshwater lake sediments. Arch. Microbiol. 171, 183–188 (1999).

    Article  CAS  Google Scholar 

  88. Finneran, K., Johnsen, C. & Lovley, D. Rhodoferax ferrireducens sp nov., a psychrotolerant, facultatively anaerobic bacterium that oxidizes acetate with the reduction of Fe(III). Int. J. Syst. Evol. Microbiol. 53, 669–673 (2003).

    Article  CAS  PubMed  Google Scholar 

  89. Coates, J. D., Ellis, D. J., Gaw, C. V. & Lovley, D. R. Geothrix fermentans gen. nov. sp. nov. a novel Fe(III)-reducing bacterium from a hydrocarbon contaminated aquifer. Int. J. Syst. Bacteriol. 49, 1615–1622 (1999).

    Article  CAS  PubMed  Google Scholar 

  90. Anderson, R. T., Rooney-Varga, J. N., Gaw, C. V. & Lovely, D. R. Anaerobic benzene oxidation in the Fe(III) reduction zone of petroleum-contaminated aquifers. Environ. Sci. Technol. 32, 1222–1229 (1998).

    Article  CAS  Google Scholar 

  91. Hugenholtz, P., Goebel, B. M. & Pace, N. R. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J. Bacteriol. 180, 4765–4774 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Barns, S. M., Takala, S. L. & Kuske, C. R. Wide distribution and diversity of members of the bacterial kingdom Acidobacterium in the environment. Appl. Environ. Microbiol. 65, 1731–1737 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Roberts, J. L. Reduction of ferric hydroxide by strains of Bacillus polymyxa. Soil Sci. 63, 135–140 (1947).

    Article  CAS  Google Scholar 

  94. Lovley, D. R. & Phillips, E. J. P. Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl. Environ. Microbiol. 51, 683–689 (1986).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Dobbin, P. S. et al. Dissimilatory Fe(III) reduction by Clostridium beijerinckii isolated from freshwater sediment using Fe(III) maltol enrichment. FEMS Microbiol. Lett. 176, 131–138 (1999).

    Article  CAS  PubMed  Google Scholar 

  96. Coleman, M. L., Hedrick, D. B., Lovley, D. R., White, D. C. & Pye, K. Reduction of Fe(III) in sediments by sulphate-reducing bacteria. Nature 361, 436–438 (1993).

    Article  CAS  Google Scholar 

  97. Lovley, D. R., Roden, E. E., Phillips, E. J. P. & Woodward, J. C. Enzymatic iron and uranium reduction by sulfate-reducing bacteria. Mar. Geol. 113, 41–53 (1993).

    Article  CAS  Google Scholar 

  98. Bond, D. R. & Lovley, D. Reduction of Fe(III) oxide by methanogens in the presence and absence of extracellular quinones. Environ. Microbiol. 4, 115–124 (2002).

    Article  CAS  PubMed  Google Scholar 

  99. Lovley, D. & Phillips, E. Competitive mechanisms for inhibition of sulfate reduction and methane production in the zone of ferric iron reduction in sediments. Appl. Environ. Microbiol. 53, 2636–2641 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Roden, E. E. & Wetzel, R. G. Organic carbon oxidation and supression of methane production by microbial Fe(III) oxide reduction in vegetated and unvegetated freshwater wetland sediments. Limnol. Oceanogr. 41, 1733–1748 (1996).

    Article  CAS  Google Scholar 

  101. Madigan, M. T., Martinko, J. M. & Parker, J. Brock Biology of Microorganisms (Pearson Education, New Jersey, 2002).

    Google Scholar 

  102. Reid, G. A. et al. Structure and function of flavocytochrome c(3), the soluble fumarate reductase from Shewanella NCIMB400. Biochem. Soc. Trans. 26, 418–421 (1998).

    Article  CAS  PubMed  Google Scholar 

  103. Lovley, D. R. et al. Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic-compounds to the reduction of iron and other metals. Arch. Microbiol. 159, 336–344 (1993).

    Article  CAS  PubMed  Google Scholar 

  104. Myers, C. R. & Myers, J. M. Role of menaquinone in the reduction of fumarate, nitrate, iron(III) and manganese(IV) by Shewanella putrefaciens Mr-1. FEMS Microbiol. Lett. 114, 215–222 (1993).

    Article  CAS  Google Scholar 

  105. Saffarini, D. A., Blumerman, S. L. & Mansoorabadi, K. J. Role of menaquinones in Fe(III) reduction by membrane fractions of Shewanella putrefaciens. J. Bacteriol. 184, 846–848 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Myers, C. R. & Myers, J. A. Shewanella oneidensis MR-1 restores menaquinone synthesis to a menaquinone-negative mutant. Appl. Environ. Microbiol. 70, 5415–5425 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Heidelberg, J. F. et al. Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nature Biotechnol. 20, 1118–1123 (2002).

    Article  CAS  Google Scholar 

  108. Methe, B. A. et al. Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science 302, 1967–1969 (2003).

    Article  CAS  PubMed  Google Scholar 

  109. Leang, C. et al. Adaptation to disruption of the electron transfer pathway for Fe(III) reduction in Geobacter sulfurreducens. J. Bacteriol. 187, 5918–5926 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Myers, C. R. & Myers, J. M. Cloning and sequence of cymA a gene encoding a tetraheme cytochrome c required for reduction of iron(III), fumarate, and nitrate by Shewanella putrefaciens MR-1. J. Bacteriol. 179, 1143–1152 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Myers, J. M. & Myers, C. R. Role of the tetraheme cytochrome CymA in anaerobic electron transport in cells of Shewanella putrefaciens MR-1 with normal levels of menaquinone. J. Bacteriol. 182, 67–75 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Beliaev, A. S. & Saffarini, D. A. Shewanella putrefaciens mtrB encodes an outer membrane protein required for Fe(III) and Mn(IV) reduction. J. Bacteriol. 180, 6292–6297 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Beliaev, A. S., Saffarini, D. A., McLaughlin, J. L. & Hunnicutt, D. MtrC, an outer membrane decahaem c cytochrome required for metal reduction in Shewanella putrefaciens MR-1. Mol. Microbiol. 39, 722–730 (2001).

    Article  CAS  PubMed  Google Scholar 

  114. Pitts, K. E. et al. Characterization of the Shewanella oneidensis MR-1 decaheme cytochrome MtrA. J. Biol. Chem. 278, 27758–27765 (2003).

    Article  CAS  PubMed  Google Scholar 

  115. Dobbin, P. S., Butt, J. N., Powell, A. K., Reid, G. A. & Richardson, D. J. Characterization of a flavocytochrome that is induced during the anaerobic respiration of Fe(III) by Shewanella frigidimarina NCIMB400. Biochem. J. 342, 439–448 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Gordon, E. H. J. et al. Identification and characterization of a novel cytochrome c(3) from Shewanella frigidimarina that is involved in Fe(III) respiration. Biochem. J. 349, 153–158 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Leys, D. et al. Crystal structures at atomic resolution reveal the novel concept of 'electron-harvesting' as a role for the small tetraheme cytochrome c. J. Biol. Chem. 277, 35703–35711 (2002).

    Article  CAS  PubMed  Google Scholar 

  118. Myers, C. R. & Myers, J. M. Cell surface exposure of the outer membrane cytochromes of Shewanella oneidensis MR-1. Lett. Appl. Microbiol. 37, 254–258 (2003).

    Article  CAS  PubMed  Google Scholar 

  119. Myers, J. M. & Myers, C. R. Overlapping role of the outer membrane cytochromes of Shewanella oneidensis MR-1 in the reduction of manganese(IV) oxide. Lett. Appl. Microbiol. 37, 21–25 (2003).

    Article  CAS  PubMed  Google Scholar 

  120. Butler, J. E., Kaufmann, F., Coppi, M. V., Nunez, C. & Lovley, D. R. MacA a diheme c-type cytochrorne involved in Fe(III) reduction by Geobacter sulfurreducens. J. Bacteriol. 186, 4042–4045 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Lloyd, J. R. et al. Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens. Biochem. J. 369, 153–161 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Leang, C., Coppi, M. V. & Lovley, D. R. OmcB, a c-type polyheme cytochrome, involved in Fe(III) reduction in Geobacter sulfurreducens. J. Bacteriol. 185, 2096–2103 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Lovely, D. Cleaning up with genomics: applying molecular biology to bioremediation. Nature Rev. Microbiol. 1, 35–44 (2003).

    Article  CAS  Google Scholar 

  124. Mahadevan, R. et al. Characterization of metabolism in the Fe(III)-reducing organism Geobacter sulfurreducens by constraint-based modeling. Appl. Environ. Microbiol. 72, 1558–1568 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Cloud, P. E. Paleoecological significance of the banded iron-formation. Econ. Geol. 68, 1135–1143 (1973).

    Article  CAS  Google Scholar 

  126. Braterman, P. S., Cairns-Smith, A. G. & Sloper, R. W. Photo-oxidation of hydrated Fe(II) — significance for banded iron formations. Nature 303, 163–164 (1983).

    Article  CAS  Google Scholar 

  127. Cloud, P. E. Significance of the Gunflint (Precambrian) microflora. Science 148, 27–35 (1965).

    Article  PubMed  Google Scholar 

  128. Lovley, D. R., Stolz, J. F., Nord, G. L. & Phillips, E. J. P. Anaerobic production of magnetite by a dissimilatory iron-reducing microorganism. Nature 330, 252–254 (1987). This paper gives the first demonstration of extracellular biogenic magnetite formation.

    Article  CAS  Google Scholar 

  129. Kohnauser, K. O. et al. Could bacteria have formed the Precambrian banded iron formations? Geology 20, 1079–1082 (2002).

    Article  Google Scholar 

  130. Kappler, A., Pasquero, C., Konhauser, K. O. & Newman, D. K. Deposition of banded iron formations by anoxygenic phototrophic Fe(II)-oxidizing bacteria. Geology 33, 865–868 (2005).

    Article  CAS  Google Scholar 

  131. Holm, N. G. The 13C/12C ratios of siderite and organic matter from a modern metalliferrous hydrothermal sediment and their implications for banded iron formations. Chem. Geol. 77, 41–45 (1989).

    Article  CAS  Google Scholar 

  132. Towe, K. M. Early Precambrian oxygen: a case against photosynthesis. Nature 274, 657–661 (1978).

    Article  CAS  Google Scholar 

  133. Canfield, D. E. & Teske, A. Late Proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies. Nature 382, 127–132 (1996).

    Article  CAS  PubMed  Google Scholar 

  134. Yung, Y. L. & McElroy, M. B. Fixation of nitrogen in the prebiotic atmosphere. Science 203, 1002–1004 (1979).

    Article  CAS  PubMed  Google Scholar 

  135. Mancinelli, R. L. & McKay, C. P. The evolution of nitrogen cycle. Orig. Life Evol. Biosph. 18, 311–325 (1988).

    Article  CAS  PubMed  Google Scholar 

  136. Walker, J. C. G. Suboxic diagenesis in banded iron formations. Nature 309, 340–342 (1984).

    Article  CAS  PubMed  Google Scholar 

  137. Coates, J. D. & Chakraborty, R. in Bioremediation: A Critical Review (eds Head, I. M., Singleton, I. & Milner, M. G.) 227–257 (Horizon Scientific, Wymondham UK, 2003).

    Google Scholar 

  138. Kim, H. J. et al. A mediator-less microbial fuel cell using a metal reducing bacterium. Enzyme Microbiol. Technol. 30, 145–152 (2002).

    Article  CAS  Google Scholar 

  139. Bond, D., Holmes, D., Tender, L. & Lovely, D.R. Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295, 483–485 (2002).

    Article  CAS  PubMed  Google Scholar 

  140. Tender, L. et al. Harnessing microbially generated power on the seafloor. Nature Biotechnol. 20, 821–825 (2002).

    Article  CAS  Google Scholar 

  141. Bond, D. & Lovley, D. Electricity production by Geobacter sulfurreducens attached to electrodes. Appl. Environ. Microbiol. 69, 1548–1555 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Bond, D. & Lovley, D. Evidence for involvement of an electron shuttle in electricity generation by Geothrix fermentans. Appl. Envir. Microbiol. 71, 2186–2189 (2005).

    Article  CAS  Google Scholar 

  143. Lovley, D. et al. Oxidation of aromatic contaminants coupled to microbial iron reduction. Nature 339, 297–299 (1989).

    Article  CAS  Google Scholar 

  144. Coates, J., Anderson, R., Woodward, J., Phillips, E. & Lovely, D. R. Anaerobic hydrocarbon degradation in petroleum-contaminated harbor sediments under sulfate-reducing and artificially imposed iron-reducing conditions. Environ. Sci. Technol. 30, 2784–2789 (1996).

    Article  CAS  Google Scholar 

  145. Coates, J., Anderson, R. & Lovley, D. Oxidation of polycyclic aromatic hydrocarbons under sulfate-reducing conditions. Appl. Environ. Microbiol. 62, 1099–1101 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Anderson, R. T. & Lovley, D. Naphthalene and benzene degradation under Fe(III)-reducing conditions in petroleum-contaminated aquifers. Bioremediation J. 3, 121–135 (1999).

    Article  CAS  Google Scholar 

  147. Lovley, D. R., Phillips, E. J. P., Gorby, Y. A. & Landa, E. R. Microbial reduction of uranium. Nature 350, 413–416 (1991). This paper gives the first description of the microbially mediated reduction of hexavalent uranium.

    Article  CAS  Google Scholar 

  148. Lovley, D. R. & Coates, J. D. Novel forms of anaerobic respiration of environmental relevance. Curr. Opin. Microbiol. 3, 252–256 (2000).

    Article  CAS  PubMed  Google Scholar 

  149. Langmuir, D. Aqueous Environmental Geochemistry (Prentice-Hall, New Jersey, 1997).

    Google Scholar 

  150. Thamdrup, B. in Advanced Microbial Ecology (ed. Schink, B.) 41–84 (Kluwer Academic/Plenum Publishers, New York, 2000).

    Book  Google Scholar 

  151. Dutton, P. L. & Prince, R. C. in The Photosynthetic Bacteria (eds Clayton, R. A. & Sistrom, W. R.) 525–570 (Plenum, New York, 1978).

    Google Scholar 

Download references

Acknowledgements

Research on microbial redox cycling of iron in the laboratories of J.D.C. and L.A.A. is supported by grants from the US Department of Energy Environmental Remediation Sciences Program.

Author information

Authors and Affiliations

  1. Department of Plant and Microbial Biology, 271 Koshland Hall, University of California, Berkeley, Berkeley, 94720, California, USA

    Karrie A. Weber & John D. Coates

  2. Department of Microbiology, Southern Illinois University, Carbondale, 62901, Illinois, USA

    Laurie A. Achenbach

Authors
  1. Karrie A. Weber
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laurie A. Achenbach
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John D. Coates
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John D. Coates.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

DATABASES

Entrez Genome Project

Chlorobium ferrooxidans

Dechloromonas aromatica

Geobacter metallireducens

Geothrix fermentans

Marinobacter aquaeolei

Rhodopseudomonas palustris

Shewanella frigidimarina

Shewanella oneidensis

Shewanella putrefaciens

Thiobacillus denitrificans

FURTHER INFORMATION

John D. Coates' homepage

Glossary

Lithotrophic

A lithotrophic organism uses an inorganic substrate (usually of mineral origin) to obtain energy for growth.

Heterotrophic

A heterotrophic organism requires organic compounds as a carbon source.

Suboxic

An environment with a partial pressure of oxygen that is substantially lower than the atmospheric oxygen content.

Anoxic

An environment lacking oxygen.

Neoteric environments

Modern environments.

Electron sink

A compound that receives electrons as an endpoint of an oxidative reaction.

Bioturbation

The disturbance of sediment layers by biological activity.

Microaerophilic

An organism that is an obligate anaerobe but can survive in environments where the partial pressure of oxygen is substantially lower than in the atmosphere.

Phototrophic

A phototrophic organism obtains energy for growth from sunlight; carbon is derived from inorganic carbon (carbon dioxide) or organic carbon.

Neutrophilic Fe(II) oxidation

Microbial Fe(II) oxidation that occurs at circumneutral pH values (∼pH 7).

Psychrophilic

An organism that grows optimally in a cold environment (<15°C).

Mesophilic

An organism that grows optimally in a moderate environment (∼25–45°C).

Hyperthermophilic

An organism that grows optimally in hot environments (>80°C).

Autotrophic

An autotrophic organism uses inorganic carbon (carbon dioxide) as a carbon source.

Chemolithoautotrophic

An organism that obtains energy from inorganic compounds and carbon from carbon dioxide.

Mixotrophy

A mixotrophic organism uses an inorganic chemical energy source and organic compounds as a carbon source.

Eutrophic

Eutrophic waters are rich in minerals and organic nutrients.

Oligotrophic environment

An environment that is relatively low in nutrients and cannot support much plant life.

Thermophilic

An organism that grows optimally at temperatures ranging from 45–80°C.

Acidophilic

An organism that grows in an acid environment (<pH 6).

Alkaliphilic

An organism that grows in an alkaline environment (pH 9–pH 11).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weber, K., Achenbach, L. & Coates, J. Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4, 752–764 (2006). https://doi.org/10.1038/nrmicro1490

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro1490

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing