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.
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
Subscribe to Journal
Get full journal access for 1 year
only $8.25 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Cornell, R. M. & Schwertmann, U. The Iron Oxides: Structure, Properties, Reactions, Occurrences and Uses (Wiley-VCH, Weinheim, 2003).
Stumm, W. & Morgan, J. J. Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters (John Wiley & Sons, New York, 1996).
Baker, B. J. & Banfield, J. F. Microbial communities in acid mine drainage. FEMS Microbiol. Ecol. 44, 139–152 (2003).
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.
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).
Lovley, D. R., Holmes, D. E. & Nevin, K. P. Dissimilatory Fe(III) and Mn(IV) reduction. Adv. Microb. Physiol. 49, 219–286 (2004).
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.
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).
Lovley, D. R. Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol. Rev. 55, 259–287 (1991).
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).
Mendelssohn, I. A., Kleiss, B. A. & Wakeley, J. S. Factors controlling the formation of oxidized root channels. Wetlands 15, 37–46 (1995).
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).
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).
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).
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).
Ghiorse, W. C. Biology of iron-depositing and manganese-depositing bacteria. Ann. Rev. Microbiol. 38, 515–550 (1984).
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.
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).
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).
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.
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.
Senn, D. B. & Hemond, H. F. Nitrate controls on iron and arsenic in an urban lake. Science 296, 2373–2376 (2002).
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).
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).
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).
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).
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).
Harrison Jr, A. P. The acidophilic Thiobacilli and other acidophilic bacteria that share their habitat. Ann. Rev. Microbiol. 38, 265–292 (1984).
Davison, W. & Seed, G. The kinetics of the oxidation of ferrous iron in synthetic and natural waters. Geochim. Cosmochim. Acta 47, 67–79 (1983).
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).
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.
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).
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).
Heising, S. & Schink, B. Phototrophic oxidation of ferrous iron by a Rhodomicrobium vannielii strain. Microbiology 144, 2263–2269 (1998).
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).
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).
Straub, K. L., Benz, M. & Schink, B. Iron metabolism in anoxic environments at near neutral pH. FEMS Microbiol. Ecol. 34, 181–186 (2001).
Kappler, A. & Newman, D. K. Formation of Fe(III)-minerals by Fe(II)-oxidizing photoautotrophic bacteria. Geochim. Cosmochim. Acta 68, 1217–1226 (2004).
Ciania, A., Gossa, K.-U. & Schwarzenbach, R. P. Light penetration in soil and particulate minerals. Eur. J. Soil Sci. 53, 561–574 (2005).
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).
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).
Ratering, S. & Schnell, S. Nitrate-dependent iron(II) oxidation in paddy soil. Environ. Microbiol. 3, 100–109 (2001).
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).
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).
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.
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).
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).
Coates, J. D. & Achenbach, L. A. Microbial perchlorate reduction: rocket-fuelled metabolism. Nature Rev. Microbiol. 2, 569–580 (2004).
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).
Gold, T. The deep, hot biosphere. Proc. Natl Acad. Sci. USA 89, 6045–6049 (1992).
Cairns-Smith, A. G. Precambrian solution photochemistry, inverse segregation, and banded iron formations. Nature 276, 807–808 (1978).
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.
Lovley, D. R. in Origins: Genesis, Evolution and Diversity of Life (ed. Seckbach, J.) 707 (Kluwer Dordrecht, Boston, 2004).
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.
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).
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).
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.
Kostka, J. E. & Nealson, K. H. Dissolution and reduction of magnetite by bacteria. Environ. Sci. Technol. 29, 2535–2540 (1995).
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).
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).
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).
Childers, S. E., Ciufo, S. & Lovley, D. R. Geobacter metallireducens accesses insoluble Fe(III) oxide by chemotaxis. Nature 416, 767–769 (2002).
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.
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).
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.
Newman, D. K. & Kolter, R. A role for excreted quinones in extracellular electron transfer. Nature 405, 94–97 (2000).
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).
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).
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).
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).
Hernandez, M. E. & Newman, D. K. Extracellular electron transfer. Cell. Mol. Life Sci. 58, 1562–1571 (2001).
Nevin, K. P. & Lovley, D. R. Mechanisms for Fe(III) oxide reduction in sedimentary environments. Geomicrobiol. J. 19, 141–159 (2002).
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).
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).
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).
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).
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).
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).
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).
Myers, C. R. & Nealson, K. H. Bacterial manganese reduction and growth with manganese oxide as the sole electron-acceptor. Science 240, 1319–1321 (1988).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
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).
Roberts, J. L. Reduction of ferric hydroxide by strains of Bacillus polymyxa. Soil Sci. 63, 135–140 (1947).
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).
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).
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).
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).
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).
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).
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).
Madigan, M. T., Martinko, J. M. & Parker, J. Brock Biology of Microorganisms (Pearson Education, New Jersey, 2002).
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).
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).
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).
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).
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).
Heidelberg, J. F. et al. Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nature Biotechnol. 20, 1118–1123 (2002).
Methe, B. A. et al. Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science 302, 1967–1969 (2003).
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).
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).
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).
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).
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).
Pitts, K. E. et al. Characterization of the Shewanella oneidensis MR-1 decaheme cytochrome MtrA. J. Biol. Chem. 278, 27758–27765 (2003).
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).
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).
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).
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).
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).
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).
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).
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).
Lovely, D. Cleaning up with genomics: applying molecular biology to bioremediation. Nature Rev. Microbiol. 1, 35–44 (2003).
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).
Cloud, P. E. Paleoecological significance of the banded iron-formation. Econ. Geol. 68, 1135–1143 (1973).
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).
Cloud, P. E. Significance of the Gunflint (Precambrian) microflora. Science 148, 27–35 (1965).
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.
Kohnauser, K. O. et al. Could bacteria have formed the Precambrian banded iron formations? Geology 20, 1079–1082 (2002).
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).
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).
Towe, K. M. Early Precambrian oxygen: a case against photosynthesis. Nature 274, 657–661 (1978).
Canfield, D. E. & Teske, A. Late Proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies. Nature 382, 127–132 (1996).
Yung, Y. L. & McElroy, M. B. Fixation of nitrogen in the prebiotic atmosphere. Science 203, 1002–1004 (1979).
Mancinelli, R. L. & McKay, C. P. The evolution of nitrogen cycle. Orig. Life Evol. Biosph. 18, 311–325 (1988).
Walker, J. C. G. Suboxic diagenesis in banded iron formations. Nature 309, 340–342 (1984).
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).
Kim, H. J. et al. A mediator-less microbial fuel cell using a metal reducing bacterium. Enzyme Microbiol. Technol. 30, 145–152 (2002).
Bond, D., Holmes, D., Tender, L. & Lovely, D.R. Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295, 483–485 (2002).
Tender, L. et al. Harnessing microbially generated power on the seafloor. Nature Biotechnol. 20, 821–825 (2002).
Bond, D. & Lovley, D. Electricity production by Geobacter sulfurreducens attached to electrodes. Appl. Environ. Microbiol. 69, 1548–1555 (2003).
Bond, D. & Lovley, D. Evidence for involvement of an electron shuttle in electricity generation by Geothrix fermentans. Appl. Envir. Microbiol. 71, 2186–2189 (2005).
Lovley, D. et al. Oxidation of aromatic contaminants coupled to microbial iron reduction. Nature 339, 297–299 (1989).
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).
Coates, J., Anderson, R. & Lovley, D. Oxidation of polycyclic aromatic hydrocarbons under sulfate-reducing conditions. Appl. Environ. Microbiol. 62, 1099–1101 (1996).
Anderson, R. T. & Lovley, D. Naphthalene and benzene degradation under Fe(III)-reducing conditions in petroleum-contaminated aquifers. Bioremediation J. 3, 121–135 (1999).
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.
Lovley, D. R. & Coates, J. D. Novel forms of anaerobic respiration of environmental relevance. Curr. Opin. Microbiol. 3, 252–256 (2000).
Langmuir, D. Aqueous Environmental Geochemistry (Prentice-Hall, New Jersey, 1997).
Thamdrup, B. in Advanced Microbial Ecology (ed. Schink, B.) 41–84 (Kluwer Academic/Plenum Publishers, New York, 2000).
Dutton, P. L. & Prince, R. C. in The Photosynthetic Bacteria (eds Clayton, R. A. & Sistrom, W. R.) 525–570 (Plenum, New York, 1978).
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.
The authors declare no competing financial interests.
Entrez Genome Project
A lithotrophic organism uses an inorganic substrate (usually of mineral origin) to obtain energy for growth.
A heterotrophic organism requires organic compounds as a carbon source.
An environment with a partial pressure of oxygen that is substantially lower than the atmospheric oxygen content.
An environment lacking oxygen.
- Neoteric environments
- Electron sink
A compound that receives electrons as an endpoint of an oxidative reaction.
The disturbance of sediment layers by biological activity.
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.
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).
An organism that grows optimally in a cold environment (<15°C).
An organism that grows optimally in a moderate environment (∼25–45°C).
An organism that grows optimally in hot environments (>80°C).
An autotrophic organism uses inorganic carbon (carbon dioxide) as a carbon source.
An organism that obtains energy from inorganic compounds and carbon from carbon dioxide.
A mixotrophic organism uses an inorganic chemical energy source and organic compounds as a carbon source.
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.
An organism that grows optimally at temperatures ranging from 45–80°C.
An organism that grows in an acid environment (<pH 6).
An organism that grows in an alkaline environment (pH 9–pH 11).
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
Verticillium dahliae CFEM proteins manipulate host immunity and differentially contribute to virulence
BMC Biology (2022)
Microbial iron cycling during palsa hillslope collapse promotes greenhouse gas emissions before complete permafrost thaw
Communications Earth & Environment (2022)
The ISME Journal (2022)
Genetic and phylogenetic analysis of dissimilatory iodate-reducing bacteria identifies potential niches across the world’s oceans
The ISME Journal (2022)