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An evolving view on biogeochemical cycling of iron


Biogeochemical cycling of iron is crucial to many environmental processes, such as ocean productivity, carbon storage, greenhouse gas emissions and the fate of nutrients, toxic metals and metalloids. Knowledge of the underlying processes involved in iron cycling has accelerated in recent years along with appreciation of the complex network of biotic and abiotic reactions dictating the speciation, mobility and reactivity of iron in the environment. Recent studies have provided insights into novel processes in the biogeochemical iron cycle such as microbial ammonium oxidation and methane oxidation coupled to Fe(iii) reduction. They have also revealed that processes in the biogeochemical iron cycle spatially overlap and may compete with each other, and that oxidation and reduction of iron occur cyclically or simultaneously in many environments. This Review discusses these advances with particular focus on their environmental consequences, including the formation of greenhouse gases and the fate of nutrients and contaminants.

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Fig. 1: The biogeochemical iron cycle.
Fig. 2: Redox potentials of diverse Fe(ii)–Fe(iii) redox couples.
Fig. 3: Electron transfer mechanisms from microorganisms to Fe(iii) minerals.
Fig. 4: Overview of processes that can overlap and lead to cryptic iron cycling.


  1. 1.

    Ehrenberg, C. Vorläufige Mitteilungen über das wirkliche Vorkommen fossiler Infusorien und ihre große Verbreitung. Poggendorff Ann. 38, 213–227 (1836).

    Google Scholar 

  2. 2.

    Chan, C. S. et al. The architecture of iron microbial mats reflects the adaptation of chemolithotrophic iron oxidation in freshwater and marine environments. Front. Microbiol. (2016). Microscopic analysis indicates how the morphology of iron-oxidizing bacteria in microbial mats responds to environmental conditions.

    Article  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Melton, E. D., Swanner, E. D., Behrens, S., Schmidt, C. & Kappler, A. The interplay of microbially mediated and abiotic reactions in the biogeochemical Fe cycle. Nat. Rev. Microbiol. 12, 797–808 (2014).

    CAS  PubMed  Google Scholar 

  4. 4.

    Ehrlich, H. L., Newman, D. K. & Kappler, A. Ehrlich’s Geomicrobiology. (CRC Press, 2015).

  5. 5.

    Byrne, J. M. et al. Redox cycling of Fe(II) and Fe(III) in magnetite by Fe-metabolizing bacteria. Science 347, 1473–1476 (2015). First article to demonstrate magnetite could support complete microbial iron cycling; that is, Fe(ii) in magnetite can be used as an electron source by Fe(ii) oxidizers and Fe(iii) can be used by Fe(iii) reducers as an electron acceptor in a cycling fashion.

    CAS  PubMed  Google Scholar 

  6. 6.

    Berg, J. S. et al. Intensive cryptic microbial iron cycling in the low iron water column of the meromictic Lake Cadagno. Environ. Microbiol. 18, 5288–5302 (2016).

    CAS  PubMed  Google Scholar 

  7. 7.

    Kappler, A. & Bryce, C. Cryptic biogeochemical cycles: unravelling hidden redox reactions. Environ. Microbiol. 19, 842–846 (2017).

    PubMed  Google Scholar 

  8. 8.

    Wang, M., Hu, R., Zhao, J., Kuzyakov, Y. & Liu, S. Iron oxidation affects nitrous oxide emissions via donating electrons to denitrification in paddy soils. Geoderma 271, 173–180 (2016).

    CAS  Google Scholar 

  9. 9.

    Beal, E. J., House, C. H. & Orphan, V. J. Manganese- and iron-dependent marine methane oxidation. Science 325, 184–187 (2009). First demonstration that methane oxidation can be coupled to reduction of iron(iii) oxides and manganese(iv) oxides.

    CAS  PubMed  Google Scholar 

  10. 10.

    Orihel, D. M. et al. The “nutrient pump:” iron-poor sediments fuel low nitrogen-to-phosphorus ratios and cyanobacterial blooms in polymictic lakes. Limnol. Oceanogr. 60, 856–871 (2015).

    Google Scholar 

  11. 11.

    Lalonde, K., Mucci, A., Ouellet, A. & Gélinas, Y. Preservation of organic matter in sediments promoted by iron. Nature 483, 198–200 (2012).

    CAS  PubMed  Google Scholar 

  12. 12.

    Muehe, E. M. et al. Fate of Cd during microbial Fe(III) mineral reduction by a novel and Cd-tolerant Geobacter species. Environ. Sci. Technol. 47, 14099–14109 (2013).

    CAS  PubMed  Google Scholar 

  13. 13.

    Glodowska, M. et al. Role of in situ natural organic matter in mobilizing As during microbial reduction of FeIII-mineral-bearing aquifer sediments from Hanoi (Vietnam). Environ. Sci. Technol. 54, 4149–4159 (2020).

    CAS  PubMed  Google Scholar 

  14. 14.

    Cutting, R. S., Coker, V. S., Fellowes, J. W., Lloyd, J. R. & Vaughan, D. J. Mineralogical and morphological constraints on the reduction of Fe(III) minerals by Geobacter sulfurreducens. Geochim. Cosmochim. Acta 73, 4004–4022 (2009).

    CAS  Google Scholar 

  15. 15.

    Wu, T. et al. Interactions between Fe(III)-oxides and Fe(III)-phyllosilicates during microbial reduction 2: natural subsurface sediments. Geomicrobiol. J. 34, 231–241 (2017).

    CAS  Google Scholar 

  16. 16.

    Jaisi, D. P., Dong, H. & Liu, C. Influence of biogenic Fe(II) on the extent of microbial reduction of Fe(III) in clay minerals nontronite, illite, and chlorite. Geochim. Cosmochim. Acta 71, 1145–1158 (2007).

    CAS  Google Scholar 

  17. 17.

    Bosch, J., Heister, K., Hofmann, T. & Meckenstock, R. U. Nanosized iron oxide colloids strongly enhance microbial iron reduction. Appl. Environ. Microbiol. 76, 184–189 (2010).

    CAS  PubMed  Google Scholar 

  18. 18.

    Aeppli, M. et al. Decreases in iron oxide reducibility during microbial reductive dissolution and transformation of ferrihydrite. Environ. Sci. Technol. 53, 8736–8746 (2019).

    CAS  PubMed  Google Scholar 

  19. 19.

    Levar, C. E., Hoffman, C. L., Dunshee, A. J., Toner, B. M. & Bond, D. R. Redox potential as a master variable controlling pathways of metal reduction by Geobacter sulfurreducens. ISME J. 11, 741–752 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Wang, Z. et al. Kinetics of reduction of Fe(III) complexes by outer membrane cytochromes MtrC and OmcA of Shewanella oneidensis MR-1. Appl. Environ. Microbiol. 74, 6746–6755 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Kügler, S. et al. Iron-organic matter complexes accelerate microbial iron cycling in an iron-rich Fen. Sci. Total. Environ. 646, 972–988 (2019).

    PubMed  Google Scholar 

  22. 22.

    Daugherty, E. E., Gilbert, B., Nico, P. S. & Borch, T. Complexation and redox buffering of iron(II) by dissolved organic matter. Environ. Sci. Technol. 51, 11096–11104 (2017).

    CAS  PubMed  Google Scholar 

  23. 23.

    von der Heyden, B., Roychoudhury, A. & Myneni, S. Iron-rich nanoparticles in natural aquatic environments. Minerals 9, 287 (2019). Thorough review of the nature and impact of iron nanoparticles in the environment.

    Google Scholar 

  24. 24.

    Hassellöv, M. & von der Kammer, F. Iron oxides as geochemical nanovectors for metal transport in soil-river systems. Elements 4, 401–406 (2008).

    Google Scholar 

  25. 25.

    Liu, J. et al. Particle size effect and the mechanism of hematite reduction by the outer membrane cytochrome OmcA of Shewanella oneidensis MR-1. Geochim. Cosmochim. Acta 193, 160–175 (2016).

    CAS  Google Scholar 

  26. 26.

    Druschel, G. K., Emerson, D., Sutka, R., Suchecki, P. & Luther, G. W. Low-oxygen and chemical kinetic constraints on the geochemical niche of neutrophilic iron(II) oxidizing microorganisms. Geochim. Cosmochim. Acta 72, 3358–3370 (2008). Landmark study using voltammetric electrodes to elucidate the optimum geochemical conditions of microaerophilic Fe(ii) oxidizers.

    CAS  Google Scholar 

  27. 27.

    Barnes, A., Sapsford, D. J., Dey, M. & Williams, K. P. Heterogeneous Fe(II) oxidation and zeta potential. J. Geochem. Explor. 100, 192–198 (2009).

    CAS  Google Scholar 

  28. 28.

    González-Davila, M., Santana-Casiano, J. M. & Millero, F. J. Oxidation of iron (II) nanomolar with H2O2 in seawater. Geochim. Cosmochim. Acta 69, 83–93 (2005).

    Google Scholar 

  29. 29.

    Kanzaki, Y. & Murakami, T. Rate law of Fe(II) oxidation under low O2 conditions. Geochim. Cosmochim. Acta 123, 338–350 (2013).

    CAS  Google Scholar 

  30. 30.

    King, D. W., Lounsbury, H. A. & Millero, F. J. Rates and mechanism of Fe(II) oxidation at nanomolar total iron concentrations. Environ. Sci. Technol. 29, 818–824 (1995).

    CAS  PubMed  Google Scholar 

  31. 31.

    Emerson, D., Fleming, E. J. & McBeth, J. M. Iron-oxidizing bacteria: an environmental and genomic perspective. Annu. Rev. Microbiol. 64, 561–583 (2010).

    CAS  PubMed  Google Scholar 

  32. 32.

    Chan, C. S., Emerson, D. & Luther, G. W. III The role of microaerophilic Fe-oxidizing micro-organisms in producing banded iron formations. Geobiology 14, 509–528 (2016).

    CAS  PubMed  Google Scholar 

  33. 33.

    Mori, J. F. et al. Physiological and ecological implications of an iron- or hydrogen-oxidizing member of the Zetaproteobacteria, Ghiorsea bivora, gen. nov., sp. nov. ISME J. 11, 2624–2636 (2017).

    PubMed  PubMed Central  Google Scholar 

  34. 34.

    Emerson, D. & De Vet, W. The role of FeOB in engineered water ecosystems: a review. J. AWWA 107, E47–E57 (2015).

    Google Scholar 

  35. 35.

    MacDonald, D. J. et al. Using in situ voltammetry as a tool to identify and characterize habitats of iron-oxidizing bacteria: from fresh water wetlands to hydrothermal vent sites. Environ. Sci. Process. Impacts 16, 2117–2126 (2014).

    PubMed  Google Scholar 

  36. 36.

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Laufer, K. et al. Microaerophilic Fe(II)-oxidizing Zetaproteobacteria isolated from low-Fe marine coastal sediments: physiology and composition of their twisted stalks. Appl. Environ. Microbiol. 83, e03118–03116 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Orcutt, B. N. et al. Colonization of subsurface microbial observatories deployed in young ocean crust. ISME J. 5, 692–703 (2011).

    CAS  PubMed  Google Scholar 

  39. 39.

    Field, E. K. et al. Planktonic marine iron oxidizers drive iron mineralization under low-oxygen conditions. Geobiology 14, 499–508 (2016).

    CAS  PubMed  Google Scholar 

  40. 40.

    Maisch, M. et al. Contribution of microaerophilic iron(II)-oxidizers to iron(III) mineral formation. Environ. Sci. Technol. 53, 8197–8204 (2019).

    CAS  PubMed  Google Scholar 

  41. 41.

    Chiu, B. K., Kato, S., McAllister, S. M., Field, E. K. & Chan, C. S. Novel pelagic iron-oxidizing Zetaproteobacteria from the Chesapeake Bay oxic–anoxic transition zone. Front. Microbiol. 8, 1280 (2017).

    PubMed  PubMed Central  Google Scholar 

  42. 42.

    McAllister, S. M. et al. The Fe(II)-oxidizing Zetaproteobacteria: historical, ecological and genomic perspectives. FEMS Microbiol. Ecol. (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Barco, R. A. et al. New insight into microbial iron oxidation as revealed by the proteomic profile of an obligate iron-oxidizing chemolithoautotroph. Appl. Environ. Microbiol. 81, 5927–5937 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. 44.

    McAllister, S. M. et al. Validating the Cyc2 neutrophilic iron oxidation pathway using meta-omics of Zetaproteobacteria iron mats at marine hydrothermal vents. mSystems 5, e00553–00519 (2020). Support for Cyc2 as the iron oxidase in microaerophilic Fe(ii) oxidizers.

    PubMed  PubMed Central  Google Scholar 

  45. 45.

    Jeans, C. et al. Cytochrome 572 is a conspicuous membrane protein with iron oxidation activity purified directly from a natural acidophilic microbial community. ISME J. 2, 542–550 (2008).

    CAS  PubMed  Google Scholar 

  46. 46.

    Edwards, B. A. & Ferris, F. G. Influence of water flow on in situ rates of bacterial Fe(II) oxidation. Geomicrobiol. J. 37, 67–75 (2020).

    CAS  Google Scholar 

  47. 47.

    Liu, J. et al. Identification and characterization of MtoA: a decaheme c-type cytochrome of the neutrophilic Fe(II)-oxidizing bacterium Sideroxydans lithotrophicus ES-1. Front. Microbiol. 3, 37 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Chan, C. S., McAllister, S. M., Garber, A., Hallahan, B. J. & Rozovsky, S. Fe oxidation by a fused cytochrome-porin common to diverse Fe-oxidizing bacteria. bioRxiv (2018).

    Article  Google Scholar 

  49. 49.

    Byrne, J. M., Schmidt, M., Gauger, T., Bryce, C. & Kappler, A. Imaging organic–mineral aggregates formed by Fe(II)-oxidizing bacteria using helium ion microscopy. Environ. Sci. Technol. Lett. 5, 209–213 (2018).

    CAS  Google Scholar 

  50. 50.

    Krepski, S. T., Emerson, D., Hredzak-Showalter, P. L., Luther, G. W. III & Chan, C. S. Morphology of biogenic iron oxides records microbial physiology and environmental conditions: toward interpreting iron microfossils. Geobiology 11, 457–471 (2013).

    CAS  PubMed  Google Scholar 

  51. 51.

    Sowers, T. D., Holden, K. L., Coward, E. K. & Sparks, D. L. Dissolved organic matter sorption and molecular fractionation by naturally occurring bacteriogenic iron (oxyhydr)oxides. Environ. Sci. Technol. 53, 4295–4304 (2019).

    CAS  PubMed  Google Scholar 

  52. 52.

    Lueder, U., Druschel, G., Emerson, D., Kappler, A. & Schmidt, C. Quantitative analysis of O2 and Fe2+ profiles in gradient tubes for cultivation of microaerophilic iron(II)-oxidizing bacteria. FEMS Microbiol. Ecol. (2017).

    Article  Google Scholar 

  53. 53.

    van der Grift, B., Rozemeijer, J. C., Griffioen, J. & van der Velde, Y. Iron oxidation kinetics and phosphate immobilization along the flow-path from groundwater into surface water. Hydrol. Earth Syst. Sci. 18, 4687–4702 (2014).

    Google Scholar 

  54. 54.

    Enright, A. M. L. & Ferris, F. G. Bacterial Fe(II) oxidation distinguished by long-range correlation in redox potential. J. Geophys. Res. Biogeosci. 121, 1249–1257 (2016).

    CAS  Google Scholar 

  55. 55.

    Lueder, U., Jørgensen, B. B., Kappler, A. & Schmidt, C. Photochemistry of iron in aquatic environments. Environ. Sci. Process. Impacts 22, 12–24 (2020).

    CAS  PubMed  Google Scholar 

  56. 56.

    Widdel, F. et al. Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362, 834–836 (1993).

    CAS  Google Scholar 

  57. 57.

    Hartman, H. The Evolution of Photosynthesis and Microbial Mats: A Speculation on the Banded Iron Formations. (Alan R. Liss, Inc., 1984).

  58. 58.

    Ozaki, K., Tajika, E., Hong, P. K., Nakagawa, Y. & Reinhard, C. T. Effects of primitive photosynthesis on Earth’s early climate system. Nat. Geosci. 11, 55–59 (2018).

    CAS  Google Scholar 

  59. 59.

    Croal, L. R., Jiao, Y. & Newman, D. K. The fox operon from Rhodobacter strain SW2 promotes phototrophic Fe(II) oxidation in Rhodobacter capsulatus SB1003. J. Bacteriol. 189, 1774–1782 (2007).

    CAS  PubMed  Google Scholar 

  60. 60.

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. 61.

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. 62.

    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. Evol. Microbiol. 49, 729–735 (1999).

    CAS  Google Scholar 

  63. 63.

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

    CAS  PubMed  Google Scholar 

  64. 64.

    Llirós, M. et al. Pelagic photoferrotrophy and iron cycling in a modern ferruginous basin. Sci. Rep. 5, 13803 (2015).

    PubMed  PubMed Central  Google Scholar 

  65. 65.

    Laufer, K. et al. Physiological characterization of a halotolerant anoxygenic phototrophic Fe(II)-oxidizing green-sulfur bacterium isolated from a marine sediment. FEMS Microbiol. Ecol. (2017).

    Article  PubMed  Google Scholar 

  66. 66.

    Jiao, Y. & Newman, D. K. The pio operon is essential for phototrophic Fe(II) oxidation in Rhodopseudomonas palustris TIE-1. J. Bacteriol. 189, 1765–1773 (2007).

    CAS  PubMed  Google Scholar 

  67. 67.

    Gupta, D. et al. Photoferrotrophs produce a PioAB electron conduit for extracellular electron uptake. mBio 10, e02668–02619 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. 68.

    Gledhill, M. & Buck, K. The organic complexation of iron in the marine environment: A review. Front. Microbiol. 3, 69 (2012).

    PubMed  PubMed Central  Google Scholar 

  69. 69.

    Saraiva, I. H., Newman, D. K. & Louro, R. O. Functional characterization of the FoxE iron oxidoreductase from the photoferrotroph Rhodobacter ferrooxidans SW2. J. Biol. Chem. 287, 25541–25548 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. 70.

    Crowe, S. A. et al. Draft genome sequence of the pelagic photoferrotroph Chlorobium phaeoferrooxidans. Genome Announc. 5, e01584–01516 (2017).

    PubMed  PubMed Central  Google Scholar 

  71. 71.

    Bryce, C., Blackwell, N., Straub, D., Kleindienst, S. & Kappler, A. Draft genome sequence of Chlorobium sp. strain N1, a marine Fe(II)-oxidizing green sulfur bacterium. Microbiol. Resour. Announc. 8, e00080–00019 (2019).

    PubMed  PubMed Central  Google Scholar 

  72. 72.

    Miot, J. et al. Iron biomineralization by anaerobic neutrophilic iron-oxidizing bacteria. Geochim. Cosmochim. Acta 73, 696–711 (2009).

    CAS  Google Scholar 

  73. 73.

    Schaedler, S. et al. Formation of cell-iron-mineral aggregates by phototrophic and nitrate-reducing anaerobic Fe(II)-oxidizing bacteria. Geomicrobiol. J. 26, 93–103 (2009).

    CAS  Google Scholar 

  74. 74.

    Hegler, F., Schmidt, C., Schwarz, H. & Kappler, A. Does a low-pH microenvironment around phototrophic FeII-oxidizing bacteria prevent cell encrustation by FeIII minerals? FEMS Microbiol. Ecol. 74, 592–600 (2010).

    CAS  PubMed  Google Scholar 

  75. 75.

    Swanner, E. D. et al. Fractionation of Fe isotopes during Fe(II) oxidation by a marine photoferrotroph is controlled by the formation of organic Fe-complexes and colloidal Fe fractions. Geochim. Cosmochim. Acta 165, 44–61 (2015).

    CAS  Google Scholar 

  76. 76.

    Boyd, P. W. & Ellwood, M. J. The biogeochemical cycle of iron in the ocean. Nat. Geosci. 3, 675–682 (2010). A comprehensive review of the many dynamic processes which influence iron cycling in the oceans.

    CAS  Google Scholar 

  77. 77.

    Faust, B. C. & Zepp, R. G. Photochemistry of aqueous iron(III)-polycarboxylate complexes: roles in the chemistry of atmospheric and surface waters. Environ. Sci. Technol. 27, 2517–2522 (1993).

    CAS  Google Scholar 

  78. 78.

    Rose, A. L. & Waite, T. D. Reduction of organically complexed ferric iron by superoxide in a simulated natural water. Environ. Sci. Technol. 39, 2645–2650 (2005).

    CAS  PubMed  Google Scholar 

  79. 79.

    Voelker, B. M., Morel, F. M. M. & Sulzberger, B. Iron redox cycling in surface waters:  Effects of humic substances and light. Environ. Sci. Technol. 31, 1004–1011 (1997).

    CAS  Google Scholar 

  80. 80.

    Barbeau, K., Zhang, G., Live, D. H. & Butler, A. Petrobactin, a photoreactive siderophore produced by the oil-degrading marine bacterium Marinobacter hydrocarbonoclasticus. J. Am. Chem. Soc. 124, 378–379 (2002).

    CAS  PubMed  Google Scholar 

  81. 81.

    Waite, T. D. & Morel, F. M. M. Photoreductive dissolution of colloidal iron oxides in natural waters. Environ. Sci. Technol. 18, 860–868 (1984).

    CAS  PubMed  Google Scholar 

  82. 82.

    Sulzberger, B. Light-induced redox cycling of iron: roles for CO2 uptake and release by aquatic ecosystems. Aquat. Geochem. 21, 65–80 (2015).

    CAS  Google Scholar 

  83. 83.

    Garg, S., Rose, A. L. & Waite, T. D. Photochemical production of superoxide and hydrogen peroxide from natural organic matter. Geochim. Cosmochim. Acta 75, 4310–4320 (2011).

    CAS  Google Scholar 

  84. 84.

    Xing, G., Garg, S. & Waite, T. D. Is superoxide-mediated Fe(III) reduction important in sunlit surface waters? Environ. Sci. Technol. 53, 13179–13190 (2019).

    CAS  PubMed  Google Scholar 

  85. 85.

    Sutherland, K. M., Wankel, S. D. & Hansel, C. M. Dark biological superoxide production as a significant flux and sink of marine dissolved oxygen. Proc. Natl. Acad. Sci. USA 117, 3433–3439 (2020).

    CAS  PubMed  Google Scholar 

  86. 86.

    Diaz, J. M. et al. Widespread production of extracellular superoxide by heterotrophic bacteria. Science 340, 1223–1226 (2013).

    CAS  PubMed  Google Scholar 

  87. 87.

    Lis, H., Kranzler, C., Keren, N. & Shaked, Y. A comparative study of iron uptake rates and mechanisms amongst marine and fresh water cyanobacteria: prevalence of reductive iron uptake. Life 5, 841–860 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. 88.

    Swanner, E. D., Maisch, M., Wu, W. & Kappler, A. Oxic Fe(III) reduction could have generated Fe(II) in the photic zone of Precambrian seawater. Sci. Rep. 8, 4238 (2018).

    PubMed  PubMed Central  Google Scholar 

  89. 89.

    Emmenegger, L., Schönenberger, R., Sigg, L. & Sulzberger, B. Light-induced redox cycling of iron in circumneutral lakes. Limnol. Oceanogr. 46, 49–61 (2001).

    CAS  Google Scholar 

  90. 90.

    Lueder, U., Jørgensen, B. B., Kappler, A. & Schmidt, C. Fe(III) photoreduction producing Feaq2+ in oxic freshwater sediment. Environ. Sci. Technol. 54, 862–869 (2020).

    CAS  PubMed  Google Scholar 

  91. 91.

    Lueder, U. et al. Influence of physical perturbation on Fe(II) supply in coastal marine sediments. Environ. Sci. Technol. 54, 3209–3218 (2020).

    CAS  PubMed  Google Scholar 

  92. 92.

    Peng, C., Bryce, C., Sundman, A. & Kappler, A. Cryptic cycling of complexes containing Fe(III) and organic matter by phototrophic Fe(II)-oxidizing bacteria. Appl. Environ. Microbiol. 85, e02826–02818 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. 93.

    Schmidt, C., Behrens, S. & Kappler, A. Ecosystem functioning from a geomicrobiological perspective a conceptual framework for biogeochemical iron cycling. Environ. Chem. 7, 399–405 (2010).

    CAS  Google Scholar 

  94. 94.

    Raven, J. A., Kübler, J. E. & Beardall, J. Put out the light, and then put out the light. J. Mar. Biol. Assoc. U.K. 80, 1–25 (2000).

    CAS  Google Scholar 

  95. 95.

    Camacho, A., Walter, X. A., Picazo, A. & Zopfi, J. Photoferrotrophy: Remains of an ancient photosynthesis in modern environments. Front. Microbiol. 8 (2017). A review on the physiology of anoxygenic phototrophic Fe(ii) oxidizers and their role in modern and ancient redox-stratified systems.

  96. 96.

    Crowe, S. A. et al. Deep-water anoxygenic photosythesis in a ferruginous chemocline. Geobiology 12, 322–339 (2014).

    CAS  PubMed  Google Scholar 

  97. 97.

    Straub, K. L., Benz, M., Schink, B. & Widdel, F. Anaerobic, nitrate-dependent microbial oxidation of ferrous iron. Appl. Environ. Microbiol. 62, 1458–1460 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. 98.

    Bryce, C. et al. Microbial anaerobic Fe(II) oxidation – Ecology, mechanisms and environmental implications. Environ. Microbiol. 20, 3462–3483 (2018).

    CAS  PubMed  Google Scholar 

  99. 99.

    Blöthe, M. & Roden, E. E. Composition and activity of an autotrophic Fe(II)-oxidizing, nitrate-reducing enrichment culture. Appl. Environ. Microbiol. 75, 6937–6940 (2009). Article describing the composition of the only confirmed autotrophic nitrate-dependent, Fe(ii)-oxidizing enrichment culture.

    PubMed  PubMed Central  Google Scholar 

  100. 100.

    Laufer, K., Røy, H., Jørgensen, B. B. & Kappler, A. Evidence for the existence of autotrophic nitrate-reducing Fe(II)-oxidizing bacteria in marine coastal sediment. Appl. Environ. Microbiol. 82, 6120–6131 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. 101.

    Liu, T., Chen, D., Luo, X., Li, X. & Li, F. Microbially mediated nitrate-reducing Fe(II) oxidation: quantification of chemodenitrification and biological reactions. Geochim. Cosmochim. Acta 256, 97–115 (2019).

    CAS  Google Scholar 

  102. 102.

    Otte, J. M. et al. N2O formation by nitrite-induced (chemo)denitrification in coastal marine sediment. Sci. Rep. 9, 10691 (2019).

    PubMed  PubMed Central  Google Scholar 

  103. 103.

    Wang, M., Hu, R., Ruser, R., Schmidt, C. & Kappler, A. Role of chemodenitrification for N2O emissions from nitrate reduction in rice paddy soils. ACS Earth Space Chem. 4, 122–132 (2020).

    CAS  Google Scholar 

  104. 104.

    He, S., Tominski, C., Kappler, A., Behrens, S. & Roden, E. E. Metagenomic analyses of the autotrophic Fe(II)-oxidizing, nitrate-reducing enrichment culture KS. Appl. Environ. Microbiol. 82, 2656–2668 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  105. 105.

    Buchwald, C., Grabb, K., Hansel, C. M. & Wankel, S. D. Constraining the role of iron in environmental nitrogen transformations: Dual stable isotope systematics of abiotic NO2 reduction by Fe(II) and its production of N2O. Geochim. Cosmochim. Acta 186, 1–12 (2016).

    CAS  Google Scholar 

  106. 106.

    Haaijer, S. C. M., Lamers, L. P. M., Smolders, A. J. P., Jetten, M. S. M. & Op den Camp, H. J. M. Iron sulfide and pyrite as potential electron donors for microbial nitrate reduction in freshwater wetlands. Geomicrobiol. J. 24, 391–401 (2007).

    CAS  Google Scholar 

  107. 107.

    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).

    CAS  PubMed  PubMed Central  Google Scholar 

  108. 108.

    Yan, R. et al. Effect of reduced sulfur species on chemolithoautotrophic pyrite oxidation with nitrate. Geomicrobiol. J. 36, 19–29 (2019).

    CAS  Google Scholar 

  109. 109.

    Holmes, P. R. & Crundwell, F. K. The kinetics of the oxidation of pyrite by ferric ions and dissolved oxygen: an electrochemical study. Geochim. Cosmochim. Acta 64, 263–274 (2000).

    CAS  Google Scholar 

  110. 110.

    Zhao, L., Dong, H., Edelmann, R. E., Zeng, Q. & Agrawal, A. Coupling of Fe(II) oxidation in illite with nitrate reduction and its role in clay mineral transformation. Geochim. Cosmochim. Acta 200, 353–366 (2017).

    CAS  Google Scholar 

  111. 111.

    Zhang, L., Dong, H., Kukkadapu, R. K., Jin, Q. & Kovarik, L. Electron transfer between sorbed Fe(II) and structural Fe(III) in smectites and its effect on nitrate-dependent iron oxidation by Pseudogulbenkiania sp. strain 2002. Geochim. Cosmochim. Acta 265, 132–147 (2019).

    CAS  Google Scholar 

  112. 112.

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

    CAS  Google Scholar 

  113. 113.

    Larese-Casanova, P., Haderlein, S. B. & Kappler, A. Biomineralization of lepidocrocite and goethite by nitrate-reducing Fe(II)-oxidizing bacteria: effect of pH, bicarbonate, phosphate, and humic acids. Geochim. Cosmochim. Acta 74, 3721–3734 (2010).

    CAS  Google Scholar 

  114. 114.

    Pantke, C. et al. Green rust formation during Fe(II) oxidation by the nitrate-reducing Acidovorax sp. strain BoFeN1. Environ. Sci. Technol. 46, 1439–1446 (2012).

    CAS  PubMed  Google Scholar 

  115. 115.

    Nordhoff, M. et al. Insights into nitrate-reducing Fe(II) oxidation mechanisms through analysis of cell-mineral associations, cell encrustation, and mineralogy in the chemolithoautotrophic enrichment culture KS. Appl. Environ. Microbiol. 83, e00752–00717 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  116. 116.

    Smith, R. L., Kent, D. B., Repert, D. A. & Böhlke, J. K. Anoxic nitrate reduction coupled with iron oxidation and attenuation of dissolved arsenic and phosphate in a sand and gravel aquifer. Geochim. Cosmochim. Acta 196, 102–120 (2017).

    CAS  Google Scholar 

  117. 117.

    Madison, A. S., Tebo, B. M., Mucci, A., Sundby, B. & Luther, G. W. Abundant porewater Mn(III) is a major component of the sedimentary redox system. Science 341, 875–878 (2013).

    CAS  PubMed  Google Scholar 

  118. 118.

    Gillispie, E. C., Taylor, S. E., Qafoku, N. P. & Hochella, M. F. Jr. Impact of iron and manganese nano-metal-oxides on contaminant interaction and fortification potential in agricultural systems – a review. Environ. Chem. 16, 377–390 (2019).

    CAS  Google Scholar 

  119. 119.

    Siebecker, M., Madison, A. S. & Luther, G. W. Reduction kinetics of polymeric (soluble) manganese (IV) oxide (MnO2) by ferrous iron (Fe2+). Aquat. Geochem. 21, 143–158 (2015).

    CAS  Google Scholar 

  120. 120.

    Herndon, E. M., Havig, J. R., Singer, D. M., McCormick, M. L. & Kump, L. R. Manganese and iron geochemistry in sediments underlying the redox-stratified Fayetteville Green Lake. Geochim. Cosmochim. Acta 231, 50–63 (2018).

    CAS  Google Scholar 

  121. 121.

    Maguffin, S. C. et al. Influence of manganese abundances on iron and arsenic solubility in rice paddy soils. Geochim. Cosmochim. Acta 276, 50–69 (2020).

    CAS  Google Scholar 

  122. 122.

    Lovley, D. R. & Phillips, E. J. P. Novel mode of microbial energy metabolism: Organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl. Environ. Microbiol. 54, 1472–1480 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  123. 123.

    Myers, C. R. & Nealson, K. H. Respiration-linked proton translocation coupled to anaerobic reduction of manganese(IV) and iron(III) in Shewanella putrefaciens MR-1. J. Bacteriol. 172, 6232–6238 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  124. 124.

    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).

    CAS  Google Scholar 

  125. 125.

    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. Evol. Microbiol. 49, 1615–1622 (1999).

    CAS  Google Scholar 

  126. 126.

    Tor, J. M. & Lovley, D. R. Anaerobic degradation of aromatic compounds coupled to Fe(III) reduction by Ferroglobus placidus. Environ. Microbiol. 3, 281–287 (2001).

    CAS  PubMed  Google Scholar 

  127. 127.

    Hansel, C. M., Benner, S. G. & Fendorf, S. Competing Fe(II)-induced mineralization pathways of ferrihydrite. Environ. Sci. Technol. 39, 7147–7153 (2005).

    CAS  PubMed  Google Scholar 

  128. 128.

    Shi, L. et al. The roles of outer membrane cytochromes of Shewanella and Geobacter in extracellular electron transfer. Environ. Microbiol. Rep. 1, 220–227 (2009).

    CAS  PubMed  Google Scholar 

  129. 129.

    Shi, L., Squier, T. C., Zachara, J. M. & Fredrickson, J. K. Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes. Mol. Microbiol. 65, 12–20 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  130. 130.

    Butler, J. E., Young, N. D. & Lovley, D. R. Evolution of electron transfer out of the cell: comparative genomics of six Geobacter genomes. BMC Genomics 11, 40 (2010).

    PubMed  PubMed Central  Google Scholar 

  131. 131.

    Reguera, G. et al. Biofilm and nanowire production leads to increased current in Geobacter sulfurreducens fuel cells. Appl. Environ. Microbiol. 72, 7345–7348 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  132. 132.

    Lovley, D. R. & Holmes, D. E. Protein nanowires: the electrification of the microbial world and maybe our own. J. Bacteriol. 202, e00331–00320 (2020). A comprehensive and recent review on extracellular electron transfer by bacteria.

    CAS  PubMed  PubMed Central  Google Scholar 

  133. 133.

    Reguera, G. et al. Extracellular electron transfer via microbial nanowires. Nature 435, 1098–1101 (2005).

    CAS  PubMed  Google Scholar 

  134. 134.

    Cologgi, D. L., Lampa-Pastirk, S., Speers, A. M., Kelly, S. D. & Reguera, G. Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism. Proc. Natl. Acad. Sci. USA 108, 15248–15252 (2011).

    CAS  PubMed  Google Scholar 

  135. 135.

    Ueki, T. et al. Decorating the outer surface of microbially produced protein nanowires with peptides. ACS Synth. Biol. 8, 1809–1817 (2019).

    CAS  PubMed  Google Scholar 

  136. 136.

    Smith, J. A., Lovley, D. R. & Tremblay, P.-L. Outer cell surface components essential for Fe(III) oxide reduction by Geobacter metallireducens. Appl. Environ. Microbiol. 79, 901–907 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  137. 137.

    Pirbadian, S. et al. Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. Proc. Natl. Acad. Sci. USA 111, 12883–12888 (2014).

    CAS  PubMed  Google Scholar 

  138. 138.

    El-Naggar, M. Y. et al. Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. Proc. Natl. Acad. Sci. USA 107, 18127–18131 (2010).

    CAS  PubMed  Google Scholar 

  139. 139.

    Roden, E. E. et al. Extracellular electron transfer through microbial reduction of solid-phase humic substances. Nat. Geosci. 3, 417–421 (2010).

    CAS  Google Scholar 

  140. 140.

    Lohmayer, R., Kappler, A., Lösekann-Behrens, T. & Planer-Friedrich, B. Sulfur species as redox partners and electron shuttles for ferrihydrite reduction by Sulfurospirillum deleyianum. Appl. Environ. Microbiol. 80, 3141–3149 (2014).

    PubMed  PubMed Central  Google Scholar 

  141. 141.

    Kappler, A., Benz, M., Schink, B. & Brune, A. Electron shuttling via humic acids in microbial iron(III) reduction in a freshwater sediment. FEMS Microbiol. Ecol. 47, 85–92 (2004).

    CAS  PubMed  Google Scholar 

  142. 142.

    Cervantes, F. J. et al. Reduction of humic substances by halorespiring, sulphate-reducing and methanogenic microorganisms. Environ. Microbiol. 4, 51–57 (2002).

    CAS  PubMed  Google Scholar 

  143. 143.

    Coates, J. D. et al. Recovery of humic-reducing bacteria from a diversity of environments. Appl. Environ. Microbiol. 64, 1504–1509 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  144. 144.

    Piepenbrock, A., Behrens, S. & Kappler, A. Comparison of humic substance- and Fe(III)-reducing microbial communities in anoxic aquifers. Geomicrobiol. J. 31, 917–928 (2014).

    CAS  Google Scholar 

  145. 145.

    Canfield, D. E. Reactive iron in marine sediments. Geochim. Cosmochim. Acta 53, 619–632 (1989).

    CAS  PubMed  Google Scholar 

  146. 146.

    Marsili, E. et al. Shewanella secretes flavins that mediate extracellular electron transfer. Proc. Natl. Acad. Sci. USA 105, 3968–3973 (2008).

    CAS  PubMed  Google Scholar 

  147. 147.

    von Canstein, H., Ogawa, J., Shimizu, S. & Lloyd, J. R. Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Appl. Environ. Microbiol. 74, 615–623 (2008).

    Google Scholar 

  148. 148.

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

    CAS  Google Scholar 

  149. 149.

    Markelova, E. et al. Deconstructing the redox cascade: what role do microbial exudates (flavins) play? Environ. Chem. 14, 515–524 (2017).

    CAS  Google Scholar 

  150. 150.

    Bai, Y. et al. AQDS and redox-active NOM enables microbial Fe(III)-mineral reduction at cm-scales. Environ. Sci. Technol. 54, 4131–4139 (2020). The first article to demonstrate that microorganisms can transfer electrons to Fe(iii) over centimetre distances by electron shuttling.

    CAS  PubMed  Google Scholar 

  151. 151.

    Bai, Y., Sun, T., Angenent, L. T., Haderlein, S. B. & Kappler, A. Electron hopping enables rapid electron transfer between quinone-/hydroquinone-containing organic molecules in microbial iron(III) mineral reduction. Environ. Sci. Technol. 54, 10646–10653 (2020).

    CAS  PubMed  Google Scholar 

  152. 152.

    Liu, F. et al. Magnetite compensates for the lack of a pilin-associated c-type cytochrome in extracellular electron exchange. Environ. Microbiol. 17, 648–655 (2015).

    CAS  PubMed  Google Scholar 

  153. 153.

    Taillefert, M. et al. Shewanella putrefaciens produces an Fe(III)-solubilizing organic ligand during anaerobic respiration on insoluble Fe(III) oxides. J. Inorg. Biochem. 101, 1760–1767 (2007).

    CAS  PubMed  Google Scholar 

  154. 154.

    in ‘t Zandt, M. H., de Jong, A. E., Slomp, C. P. & Jetten, M. S. The hunt for the most-wanted chemolithoautotrophic spookmicrobes. FEMS Microbiol. Ecol. (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  155. 155.

    Sivan, O. et al. Geochemical evidence for iron-mediated anaerobic oxidation of methane. Limnol. Oceanogr. 56, 1536–1544 (2011).

    CAS  Google Scholar 

  156. 156.

    Miura, Y., Watanabe, A., Murase, J. & Kimura, M. Methane production and its fate in paddy fields. Soil Sci. Plant Nutr. 38, 673–679 (1992).

    CAS  Google Scholar 

  157. 157.

    Crowe, S. A. et al. The methane cycle in ferruginous Lake Matano. Geobiology 9, 61–78 (2011).

    CAS  PubMed  Google Scholar 

  158. 158.

    Amos, R. T. et al. Evidence for iron-mediated anaerobic methane oxidation in a crude oil-contaminated aquifer. Geobiology 10, 506–517 (2012).

    CAS  PubMed  Google Scholar 

  159. 159.

    Glodowska, M. et al. Arsenic mobilization by anaerobic iron-dependent methane oxidation. Commun. Earth Environ. 1, 42 (2020). First study providing evidence that anaerobic oxidation of methane coupled to reduction of arsenic-bearing Fe(iii) minerals can lead to arsenic mobilization in groundwater.

    Google Scholar 

  160. 160.

    Scheller, S., Yu, H., Chadwick, G. L., McGlynn, S. E. & Orphan, V. J. Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction. Science 351, 703–707 (2016).

    CAS  PubMed  Google Scholar 

  161. 161.

    Wegener, G., Krukenberg, V., Riedel, D., Tegetmeyer, H. E. & Boetius, A. Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria. Nature 526, 587–590 (2015).

    CAS  PubMed  Google Scholar 

  162. 162.

    Ettwig, K. F. et al. Archaea catalyze iron-dependent anaerobic oxidation of methane. Proc. Natl. Acad. Sci. USA 113, 12792–12796 (2016).

    CAS  PubMed  Google Scholar 

  163. 163.

    Cai, C. et al. A methanotrophic archaeon couples anaerobic oxidation of methane to Fe(III) reduction. ISME J. 12, 1929–1939 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  164. 164.

    Clément, J.-C., Shrestha, J., Ehrenfeld, J. G. & Jaffé, P. R. Ammonium oxidation coupled to dissimilatory reduction of iron under anaerobic conditions in wetland soils. Soil. Biol. Biochem. 37, 2323–2328 (2005).

    Google Scholar 

  165. 165.

    Huang, S. & Jaffé, P. R. Characterization of incubation experiments and development of an enrichment culture capable of ammonium oxidation under iron-reducing conditions. Biogeosciences 12, 769–779 (2015).

    Google Scholar 

  166. 166.

    Li, X. et al. Evidence of nitrogen loss from anaerobic ammonium oxidation coupled with ferric iron reduction in an intertidal wetland. Environ. Sci. Technol. 49, 11560–11568 (2015).

    CAS  PubMed  Google Scholar 

  167. 167.

    Zhou, G.-W. et al. Electron shuttles enhance anaerobic ammonium oxidation coupled to iron(III) reduction. Environ. Sci. Technol. 50, 9298–9307 (2016).

    CAS  PubMed  Google Scholar 

  168. 168.

    Yang, W. H., Weber, K. A. & Silver, W. L. Nitrogen loss from soil through anaerobic ammonium oxidation coupled to iron reduction. Nat. Geosci. 5, 538–541 (2012).

    CAS  Google Scholar 

  169. 169.

    Li, X. et al. Simultaneous Fe(III) reduction and ammonia oxidation process in Anammox sludge. J. Environ. Sci. 64, 42–50 (2018).

    Google Scholar 

  170. 170.

    Huang, S. & Jaffé, P. R. Isolation and characterization of an ammonium-oxidizing iron reducer: Acidimicrobiaceae sp. A6. PLoS ONE 13, e0194007 (2018).

    PubMed  PubMed Central  Google Scholar 

  171. 171.

    Sawayama, S. Possibility of anoxic ferric ammonium oxidation. J. Biosci. Bioeng. 101, 70–72 (2006).

    CAS  PubMed  Google Scholar 

  172. 172.

    Zhu, X., Burger, M., Doane, T. A. & Horwath, W. R. Ammonia oxidation pathways and nitrifier denitrification are significant sources of N2O and NO under low oxygen availability. Proc. Natl. Acad. Sci. USA 110, 6328–6333 (2013).

    CAS  PubMed  Google Scholar 

  173. 173.

    Ginn, B., Meile, C., Wilmoth, J., Tang, Y. & Thompson, A. Rapid iron reduction rates are stimulated by high-amplitude redox fluctuations in a tropical forest soil. Environ. Sci. Technol. 51, 3250–3259 (2017). A good example of the dynamic nature of iron cycling in the environment and its impact on the reducibility of minerals.

    CAS  PubMed  Google Scholar 

  174. 174.

    Mejia, J., Roden, E. E. & Ginder-Vogel, M. Influence of oxygen and nitrate on Fe (hydr)oxide mineral transformation and soil microbial communities during redox cycling. Environ. Sci. Technol. 50, 3580–3588 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  175. 175.

    Laufer, K. et al. Coexistence of microaerophilic, nitrate-reducing, and phototrophic Fe(II) oxidizers and Fe(III) reducers in coastal marine sediment. Appl. Environ. Microbiol. 82, 1433–1447 (2016).

    CAS  PubMed Central  Google Scholar 

  176. 176.

    Hansel, C. M., Ferdelman, T. G. & Tebo, B. M. Cryptic cross-linkages among biogeochemical cycles: novel insights from reactive intermediates. Elements 11, 409–414 (2015). A review on cryptic element cycling in the environment, including cryptic iron cycling.

    CAS  Google Scholar 

  177. 177.

    Klueglein, N. & Kappler, A. Abiotic oxidation of Fe(II) by reactive nitrogen species in cultures of the nitrate-reducing Fe(II) oxidizer Acidovorax sp. BoFeN1 – questioning the existence of enzymatic Fe(II) oxidation. Geobiology 11, 180–190 (2013).

    CAS  PubMed  Google Scholar 

  178. 178.

    Matus, F. et al. Ferrous wheel hypothesis: Abiotic nitrate incorporation into dissolved organic matter. Geochim. Cosmochim. Acta 245, 514–524 (2019). Demonstration of the ‘ferrous wheel hypothesis’ with insights for the role of coupled iron and nitrogen cycling in the environment.

    CAS  Google Scholar 

  179. 179.

    Chen, C., Hall, S. J., Coward, E. & Thompson, A. Iron-mediated organic matter decomposition in humid soils can counteract protection. Nat. Commun. 11, 2255 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  180. 180.

    Patzner, M. S. et al. Iron mineral dissolution releases iron and associated organic carbon during permafrost thaw. Nat. Commun. 11, 6329 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  181. 181.

    Beckwith, C. R. et al. Characterization of MtoD from Sideroxydans lithotrophicus: a cytochrome c electron shuttle used in lithoautotrophic growth. Front. Microbiol. 6, 332 (2015).

    PubMed  PubMed Central  Google Scholar 

  182. 182.

    Bird, L. J., Bonnefoy, V. & Newman, D. K. Bioenergetic challenges of microbial iron metabolisms. Trends Microbiol. 19, 330–340 (2011).

    CAS  PubMed  Google Scholar 

  183. 183.

    Field, S. J. et al. Purification and magneto-optical spectroscopic characterization of cytoplasmic membrane and outer membrane multiheme c-type cytochromes from Shewanella frigidimarina NCIMB400. J. Biol. Chem. 275, 8515–8522 (2000).

    CAS  PubMed  Google Scholar 

  184. 184.

    Giffaut, E. et al. Andra thermodynamic database for performance assessment: ThermoChimie. Appl. Geochem. 49, 225–236 (2014).

    CAS  Google Scholar 

  185. 185.

    Salmon, T. P., Rose, A. L., Neilan, B. A. & Waite, T. D. The FeL model of iron acquisition: nondissociative reduction of ferric complexes in the marine environment. Limnol. Oceanogr. 51, 1744–1754 (2006).

    CAS  Google Scholar 

  186. 186.

    Navrotsky, A., Mazeina, L. & Majzlan, J. Size-driven structural and thermodynamic complexity in iron oxides. Science 319, 1635–1638 (2008).

    CAS  PubMed  Google Scholar 

  187. 187.

    Gorski, C. A., Edwards, R., Sander, M., Hofstetter, T. B. & Stewart, S. M. Thermodynamic characterization of iron oxide–aqueous Fe2+ redox couples. Environ. Sci. Technol. 50, 8538–8547 (2016). One of the first examples of using electrochemical methods to better understand the range of redox potentials present in different iron phases.

    CAS  PubMed  Google Scholar 

  188. 188.

    Robie, R. A. & Heminway, B. S. Thermodynamic properties of minerals and related substances at 298.15 K and 1 bar (105 pascals) pressure and at higher temperatures. (United States Printing Office, 1995).

  189. 189.

    Navrotsky, A., Ma, C., Lilova, K. & Birkner, N. Nanophase transition metal oxides show large thermodynamically driven shifts in oxidation-reduction equilibria. Science 330, 199–201 (2010).

    CAS  PubMed  Google Scholar 

  190. 190.

    Robie, R. A. & Bethke, P. Molar Volumes and Densities of Minerals. Report TEI-822 (United States Department of the Interior Geological Survey, 1962).

  191. 191.

    Gorski, C. A., Nurmi, J. T., Tratnyek, P. G., Hofstetter, T. B. & Scherer, M. M. Redox behavior of magnetite: implications for contaminant reduction. Environ. Sci. Technol. 44, 55–60 (2010).

    CAS  PubMed  Google Scholar 

  192. 192.

    Gorski, C. A., Klüpfel, L. E., Voegelin, A., Sander, M. & Hofstetter, T. B. Redox properties of structural Fe in clay minerals: 3. Relationships between smectite redox and structural properties. Environ. Sci. Technol. 47, 13477–13485 (2013).

    CAS  PubMed  Google Scholar 

  193. 193.

    Oswald, K. et al. Aerobic gammaproteobacterial methanotrophs mitigate methane emissions from oxic and anoxic lake waters. Limnol. Oceanogr. 61, S101–S118 (2016).

    Google Scholar 

  194. 194.

    Braunschweig, J., Bosch, J. & Meckenstock, R. U. Iron oxide nanoparticles in geomicrobiology: from biogeochemistry to bioremediation. N. Biotechnol. 30, 793–802 (2013).

    CAS  PubMed  Google Scholar 

  195. 195.

    Villa, R. D., Trovó, A. G. & Nogueira, R. F. P. Environmental implications of soil remediation using the Fenton process. Chemosphere 71, 43–50 (2008).

    CAS  PubMed  Google Scholar 

  196. 196.

    Wagai, R. & Mayer, L. M. Sorptive stabilization of organic matter in soils by hydrous iron oxides. Geochim. Cosmochim. Acta 71, 25–35 (2007).

    CAS  Google Scholar 

  197. 197.

    Nitzsche, K. S. et al. Arsenic removal from drinking water by a household sand filter in Vietnam — effect of filter usage practices on arsenic removal efficiency and microbiological water quality. Sci. Total. Environ. 502, 526–536 (2015).

    CAS  PubMed  Google Scholar 

  198. 198.

    Sipos, P., Németh, T., Kis, V. K. & Mohai, I. Sorption of copper, zinc and lead on soil mineral phases. Chemosphere 73, 461–469 (2008).

    CAS  PubMed  Google Scholar 

  199. 199.

    Poulton, S. W. & Canfield, D. E. Development of a sequential extraction procedure for iron: implications for iron partitioning in continentally derived particulates. Chem. Geol. 214, 209–221 (2005).

    CAS  Google Scholar 

  200. 200.

    Schaedler, F., Kappler, A. & Schmidt, C. A revised iron extraction protocol for environmental samples rich in nitrite and carbonate. Geomicrobiol. J. 35, 23–30 (2018).

    CAS  Google Scholar 

  201. 201.

    Porsch, K. & Kappler, A. FeII oxidation by molecular O2 during HCl extraction. Environ. Chem. 8, 190–197 (2011).

    CAS  Google Scholar 

  202. 202.

    Roden, E. E. & Zachara, J. M. Microbial reduction of crystalline iron(III) oxides:  Influence of oxide surface area and potential for cell growth. Environ. Sci. Technol. 30, 1618–1628 (1996).

    CAS  Google Scholar 

  203. 203.

    Tessier, A., Campbell, P. G. C. & Bisson, M. Sequential extraction procedure for the speciation of particulate trace metals. Anal. Chem. 51, 844–851 (1979).

    CAS  Google Scholar 

  204. 204.

    Stookey, L. L. Ferrozine - a new spectrophotometric reagent for iron. Anal. Chem. 42, 779–781 (1970).

    CAS  Google Scholar 

  205. 205.

    Clark, L. J. Iron(II) determination in the presence of iron(III) using 4,7-diphenyl-1,10-phenanthroline. Anal. Chem. 34, 348–352 (1962).

    CAS  Google Scholar 

  206. 206.

    Viollier, E., Inglett, P. W., Hunter, K., Roychoudhury, A. N. & Van Cappellen, P. The ferrozine method revisited: Fe(II)/Fe(III) determination in natural waters. Appl. Geochem. 15, 785–790 (2000).

    CAS  Google Scholar 

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The authors acknowledge funding for several research grants from the German Research Foundation (DFG), in particular the Collaborative Research Center CAMPOS (DFG grant agreement SFB 1253/1) and the priority programme EarthShape.

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A.K. and C.B. initiated the manuscript, designed the content, wrote the manuscript, created some of the figures, and compiled and revised all content. E.D.S., M.M., U.L. and J.M.B. wrote the manuscript and created some of the figures.

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Correspondence to Andreas Kappler.

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Microorganisms that oxidize Fe(ii) at O2 concentrations in the tens of micromoles per litre range are microaerophilic Fe(ii) oxidizers.


Describes the oxidation state and the identity of the coordinating ligands (for example, organic matter, chloride or sulfide).

Redox potentials

Redox potential (in millivolts) indicates the thermodynamic driving force for reduction or oxidation, for example, of an Fe(iii)–Fe(ii) pair.


A poorly crystalline (short-range-ordered) iron(iii) oxyhydroxide mineral with a primary particle diameter in the low nanometre range (less than 6 nm), and a resulting large surface area and high reactivity.

Natural organic matter

(NOM). Mixture of organic compounds resulting in nature from the degradation of biopolymers (proteins, lipids, lignin, polysaccharides and so on) stemming from plants, microorganisms and animals.


Particles smaller than 100 nm in at least one dimension.


Particles smaller than 1,000 nm in at least one dimension that are dispersed in a substance of another physical state (for example, mineral particles in a liquid).


Particles larger than 1,000 nm in all dimensions.

Transmission electron microscopy

(TEM). An imaging technique using a beam of electrons transmitted through a thin specimen to obtain an image of the specimen down to atomic resolution, applied in physical, chemical and biological sciences. Can be used, for example, to characterize nanoparticles formed by iron-metabolizing microorganisms.

Scanning electron microscopy

(SEM). An imaging technique using a beam of electrons to scan the surface of a specimen to obtain information about the morphology, topography and surface structure. Applied, for example, to characterize cell–mineral structures of iron-metabolizing microorganisms.

Homogeneous Fe(ii) oxidation

The oxidation of reduced iron (Fe(ii)) by an oxidant that is in the same physical state (for example, oxidation of dissolved Fe2+ by dissolved O2).

Reactive oxygen species

(ROS). Very reactive compounds with unpaired electrons formed from molecular O2.


A ferric iron oxyhydroxide polymorph (γ-FeOOH) with a yellow to reddish brown colour.


A ferric iron oxyhydroxide polymorph (α-FeOOH) known for its use as a paint pigment and named after the poet Johann Wolfgang von Goethe.


A chloride-containing ferric iron oxyhydroxide polymorph (β-FeOOH) that typically forms in marine environments.

Heterogeneous Fe(ii) oxidation

The oxidation of iron (Fe(ii)) by an oxidant that is in a different physical state (for example, oxidation of sorbed Fe(ii) by dissolved O2).

Voltammetric microelectrodes

Electrodes with tip diameters in the micrometre range (the potential at the working electrode is varied and the resulting current is recorded). Such electrodes can be used to identify and quantify iron redox species with high spatial resolution (for example, in sediments).

c-type cytochrome

A protein that contains haem as a prosthetic group and is involved in oxidation and reduction reactions inside and outside the microbial cell.

Extracellular polymeric substances

Organic molecules consisting of polysaccharides and proteins, but also DNA and lipids, purposefully released by microorganisms into the environment (for example, during biofilm formation).

Humic substances

Stable organic molecules that are redox active and thought to form by humification; that is, the transformation of biomolecules (including lignin, proteins and polysaccharides). This formation theory has been questioned and is being gradually replaced by a soil continuum model.


Organic compounds produced and released by microorganisms in order to make otherwise poorly soluble Fe(iii) ions bioavailable for the cells and to facilitate their uptake.


Describes microorganisms that use energy from a chemical reaction of inorganic compounds (for example, oxidation of Fe(ii)) to fix carbon from CO2 into biomass.


Microorganisms using an inorganic electron source (for example Fe(ii)) in addition to an organic compound for their metabolism are termed mixotrophs, i.e. mixotrophic microorganisms.

Fe(iii) reducers

Microorganisms that specialize in gaining energy by coupling Fe(iii) reduction with the oxidation of an electron donor (for example, an organic compound).

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Kappler, A., Bryce, C., Mansor, M. et al. An evolving view on biogeochemical cycling of iron. Nat Rev Microbiol 19, 360–374 (2021).

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