Skip to main content
Log in

Neutrophilic lithotrophic iron-oxidizing prokaryotes and their role in the biogeochemical processes of the iron cycle

  • Reviews
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

Biology of lithotrophic neutrophilic iron-oxidizing prokaryotes and their role in the processes of the biogeochemical cycle of iron are discussed. This group of microorganisms is phylogenetically, taxonomically, and physiologically heterogeneous, comprising three metabolically different groups: aerobes, nitratedependent anaerobes, and phototrophs; the latter two groups have been revealed relatively recently. Their taxonomy and metabolism are described. Materials on the structure and functioning of the electron transport chain in the course of Fe(II) oxidation by members of various physiological groups are discussed. Occurrence of iron oxidizers in freshwater and marine ecosystems, thermal springs, areas of hydrothermal activity, and underwater volcanic areas are considered. Molecular genetic techniques were used to determine the structure of iron-oxidizing microbial communities in various natural ecosystems. Analysis of stable isotope fractionation of 56/54Fe in pure cultures and model experiments revealed a predominance of biological oxidation over abiotic ones in shallow aquatic habitats and mineral springs, which was especially pronounced under microaerobic conditions at the redox zone boundary. Discovery of anaerobic bacterial Fe(II) oxidation resulted in development of new hypotheses concerning the possible role of microorganisms and the mechanisms of formation of the major iron ore deposits during Precambrian era until the early Proterozoic epoch. Paleobiological data are presented on the microfossils and specific biomarkers retrieved from ancient ore samples and confirming involvement of anaerobic biogenic processes in their formation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Hedrich, S., Schlömann, M., and Johnson, D.B., The iron-oxidizing proteobacteria, Microbiology (UK), 2011, vol. 157, pp. 1551–1564.

    Article  CAS  Google Scholar 

  2. Ehrenberg, C.G., Vorlaufige Mitteilungen uber das wirkliche Vorkommen fossiler Infusorien and ihre grosse Verbreitung, Poggendorts Ann., 1836, vol. 38, pp. 213–227.

    Google Scholar 

  3. Winogradsky, S.N., Über Eisenbakterien, Botan. Zeit, 1888, vol. 46, pp. 262–270.

    Google Scholar 

  4. Halbeck, L. and Pedersen, K., Autotrophic and mixotrophic growth of Gallionella ferruginea, Gen. Microbiol., 1991, vol. 137, pp. 2657–2661.

    Article  Google Scholar 

  5. Hallbeck, L. and Pedersen, K., Phylogeny and phenotypic characterization of the stalk-forming and ironoxidizing bacterium Gallionella ferruginea, Gen. Microbiol., 1993, vol. 139, pp. 1531–1535.

    Article  CAS  Google Scholar 

  6. Emerson, D. and Moyer, C., Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH, Appl. Environ. Microbiol., 1997, vol. 63, pp. 4784–4792.

    CAS  PubMed Central  PubMed  Google Scholar 

  7. Emerson, D., Field, E.K., Chertkov, O., Davenport, K.W., Goodwin, L., Munk, C., Nolan, M., and Woyke, T., Comparative genomics of freshwater Fe-oxidizing bacteria: implications for physiology, ecology, and systematic, Front. in Microbiol., 2013, vol. 4, article 254.

    Google Scholar 

  8. Sobolev, D. and Roden, E., Characterization of a neutrophilic, chemolithoautotrophic Fe(II)-oxidizing Betaproteobacterium from freshwater wetland sediments, Geomicrobiol. J., 2004, vol. 21, pp. 1–10.

    Article  CAS  Google Scholar 

  9. Weiss, J.V., Rentz, J.A., Plaia, T., Neubauer, S.C., Merrill-Floyd, M., Lilburn, T., Bradburne, C., Megonigal, J.P., and Emerson, D., Characterization of neutrophilic Fe(II)-oxidizing bacteria isolated from the rhizosphere of wetland plants and description of Ferritrophicum radicicola gen. nov., sp. nov., and Sideroxydans paludicola sp. nov, Geomicrobiol. J., 2007, vol. 24, pp. 559–570.

    Article  CAS  Google Scholar 

  10. Emerson, D., Rentz, J.A., Lilburn, T.G., Davis, R.E., Aldrich, H., Chan, C., and Moyer, C.L., A novel lineage of Proteobacteria involved in formation of marine Fe-oxidizing microbial mat communities, PLoS ONE, 2: e667. doi: 10.1371/journal.pone.0000667

  11. McBeth, J.M., Little, B.J., Ray, R.I., Farrar, K.M., and Emerson, D., Neutrophilic iron-oxidizing “Zetaproteobacteria” and mild steel corrosion in near shore marine environments, Appl. Environ. Microbiol., 2011, vol. 77, pp. 1405–1412.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Krepski, S.T., Hanson, T.E., and Chan, C.S., Isolation and characterization of novel biomineral stalk-forming iron-oxidizing bacterium from a circumneutral groundwater seep, Environ. Microbiol., 2012, vol. 14, pp. 1671–1680.

    Article  CAS  PubMed  Google Scholar 

  13. Edwards, K.J., Rogers, D.R., Wirsen, C.O., and McCollom, T.M., Isolation and characterization of novel psychrophilic, neutrophilic, Fe-oxidizing, chemolithoautotrophic α and γProteobacteria from the deep sea, Appl. Environ. Microbiol., 2003, vol. 69, pp. 2906–2913.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Lovley, D.R., Giovannoni, S.J., White, D.C., Champine, J.E., Phillips, E.J.P., Gorby, Y.A., and Goodwin, S., 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., 1993, vol. 159, pp. 336–344.

    Article  CAS  PubMed  Google Scholar 

  15. Senko, J. and Stolz, J., Evidence for iron-dependent nitrate respiration in the dissimilatory iron-reducing bacterium Geobacter metallireducens, Appl. Environ. Microbiol., 2001, vol. 67, pp. 3750–3752.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Finneran, K., Anderson, R., Nevin, K., and Lovley, D.R., Potential for bioremediation of uraniumcontaminated aquifers with microbial U(VI) reduction, Soil Sediment. Contam., 2002, vol. 11, pp. 339–357.

    Article  CAS  Google Scholar 

  17. Hafenbrandl, D., Keller, M., Dirmeier, R., Rachel, R., Rossnagel, P., Burggraf, S., Huber, H., and Stetter, K.O., Ferroglobus placidus gen. nov., sp. nov., a novel hyperthermophilic archaeum that oxidizes Fe2+ at neutral pH under anoxic conditions, Arch. Microbiol., 1996, vol. 166, pp. 308–314.

    Article  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  19. Jørgensen, C.J., Jacobsen, O.S., Elberling, B., and Aamand, J., Microbial oxidation of pyrite coupled to nitrate reduction in anoxic groundwater sediment, Environ. Sci. Technol., 2009, vol. 43, pp. 4851–4857.

    Article  PubMed  Google Scholar 

  20. Benz, M., Brune, A., and Shinck, B., Anaerobic and aerobic oxidation of ferrous iron at neutral pH by chemoheterotrophic nitrate-reducing bacteria, Arch. Microbiol., 1998, vol. 169, pp. 159–165.

    Article  CAS  PubMed  Google Scholar 

  21. Chaudhuri, S.K., Lack, J.G., and Coates, J.D., Biogenic magnetite formation through anaerobic biooxidation of Fe(II), Appl. Environ. Microbiol., 2001, vol. 67, pp. 2844–2848.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Coates, J.D., Chakraborty, R., Lack, J.G., O’Connor, S.M., Cole, K.A., Bender, K.S., and Achenbach, L.A., Anaerobic benzene oxidation coupled to nitrate reduction in pure culture by two strains of Dechloromonas, Nature, 2001, vol. 411, pp. 1039–1043.

    Article  CAS  PubMed  Google Scholar 

  23. Straub, K.L., Schönhuber, W.A., Buchholz-Cleven, B.E., and Schink, B., Diversity of ferrous ironoxidizing, nitrate-reducing bacteria and their involvement in oxygen-independent iron cycling, Geomicrobiol. J., 2004, vol. 21, pp. 371–378.

    Article  CAS  Google Scholar 

  24. Kappler, U., Pasquero, C., Konhauser, K.O., and Newman, D.K., Deposition of banded iron formations by anoxygenic phototrophic Fe(II)-oxidizing bacteria, Geology, 2005, vol. 33, pp. 865–868.

    Article  CAS  Google Scholar 

  25. Kumaraswamy, R., Sjollema, K., Kuenen, G., van Loosdrecht, M., and Muyzer, G., Nitrate-dependent [Fe(II)EDTA]2-oxidation by Paracoccus ferrooxidans sp. nov., isolated from a denitrifying bioreactor, Syst. Appl. Microbiol., 2006, vol. 29, pp. 276–286.

    Article  CAS  PubMed  Google Scholar 

  26. Muehe, E.M., Gerhardt, S., Schink, B., and Kappler, A., Ecophysiology and the energetic benefit of mixotrophic Fe(II) oxidation by various strains of nitrate-reducing bacteria, FEMS Microbiol. Ecol., 2009, vol. 70, pp. 335–343.

    Article  CAS  PubMed  Google Scholar 

  27. Weber, K.A., Achenbach, L.A., and Coates, J.D., Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction, Nat. Rev. Microbiol., 2006, vol. 4, pp. 752–764.

    Article  CAS  PubMed  Google Scholar 

  28. Byrne-Bailey, K.G., Weber, K.A., Chair, A.H., Bose, S., Knox, T., Spanbauer, T.L., Chertkov, O., and Coates, J.D., Completed genome sequence of the anaerobic iron-oxidizing bacterium Acidovorax ebreus strain TPSY, J. Bacteriol., 2010, vol. 192, pp. 1475–1476.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Chakraborty, S. and Newton, A.C., Climate change, plant diseases and food security: an overview, Plant Pathol., 2011, vol. 60, pp. 2–14.

    Article  Google Scholar 

  30. Picardal, F.W., Zaybak, Z., Chakraborty, A., Schieber, J., and Szewzyk, U., Microaerophilic, Fe(II)-dependent growth and Fe(II) oxidation by a Dechlorospirillum species, FEMS Microbiol. Lett., 2011, vol. 319, pp. 51–57.

    Article  CAS  PubMed  Google Scholar 

  31. Sorokina, A.Yu., Chernousova, E.Yu., and Dubinina, G.A., Hoeflea siderophila sp. nov. a new neutrophilic iron-oxidizing bacterium, Microbiology (Moscow), 2012, vol. 81, pp. 59–66.

    Article  CAS  Google Scholar 

  32. Sorokina, A.Y., Chernousova, E.Y., and Dubinina, G.A., Ferrovibrio denitrificans gen. nov., sp. nov., a novel neutrophilic facultative anaerobic Fe(II)-oxidizing bacterium, FEMS Microbiol. Lett., 2012, vol. 335, pp. 19–25.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  35. Widdel, F., Schnell, S., Heising, S., Ehrenreich, A., Assmus, B., and Schink, B., Ferrous iron oxidation by anoxygenic phototrophic bacteria, Nature, 1993, vol. 362, pp. 834–836.

    Article  CAS  Google Scholar 

  36. Ehrenreich, A. and Widdel, F., Anaerobic oxidation of ferrous iron by purple bacteria, a new type of phototrophic metabolism, Appl. Environ. Microbiol., 1994, vol. 60, pp. 4517–4526.

    CAS  PubMed Central  PubMed  Google Scholar 

  37. Heising, S. and Schink, B., Phototrophic oxidation of ferrous iron by a Rhodomicrobium vannielii strain, Microbiology (UK), 1998, vol. 144, pp. 2263–2269.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  39. Heising, S., Richter, L., Ludwig, W., and Schink, B., Chlorobium ferrooxidans sp. nov., a phototrophic green sulfur bacterium that oxidizes ferrous iron in coculture with a “Geospirillum” sp. strain, Arch. Microbiol., 1999, vol. 172, pp. 116–124.

    Article  CAS  PubMed  Google Scholar 

  40. Croal, L.R., Johnson, C.M., Beard, B.L., and Newman, D.K., Iron isotope fractionation by Fe(II)-oxidizing photoautotrophic bacteria, Geochim. Cosmochim. Acta, 2004, vol. 68, pp. 1227–1242.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. Poulain, A.J. and Newman, D.K., Rhodobacter capsulatus catalyzes light-dependent Fe(II) oxidation under anaerobic conditions as a potential detoxification mechanism, Appl. Environ. Microbiol., 2009, vol. 75, pp. 6639–6646.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Roden, E.E., Sobolev, D., Glazer, B., and Luther, G.W., Potential for microscale bacterial Fe redox cycling at the aerobic-anaerobic interface, Geomicrobiol. J., 2004, vol. 21, pp. 379–391.

    Article  CAS  Google Scholar 

  46. Neubauer, S.C., Emerson, D., and Megonigal, J.P., Life at the energetic edge: kinetics of circumneutral iron oxidation by lithotrophic iron-oxidizing bacteria isolated from the wetland-plant rhizosphere, Appl. Environ. Microbiol., 2002, vol. 68, pp. 3988–3995.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Drussel, G.K., Emerson, D., and Satka, R., Low-oxygen and chemical constraints on the geochemical niche of neutrophilic iron(II) oxidizing microorganisms, Geochim. Cosmochim. Acta, 2008, vol. 72, pp. 3358–3370.

    Article  Google Scholar 

  48. Dubinina, G.A., Sorokina, A.Yu., Gapeeva, M.V., and Dolotov, A.V., Communities of neutrophilic iron-oxidizing microorganisms of ferruginous springs of various types and their involvement in fractionation of stable iron isotopes, Microbiology, 2012, vol. 81, pp. 90–97.

    Article  CAS  Google Scholar 

  49. Rentz, J.A., Turner, I.P., and Ullman, J.L., Removal of phosphorus from solution using biogenic iron oxides, Water Res., 2009, vol. 43, pp. 2029–2035.

    Article  CAS  PubMed  Google Scholar 

  50. Sobolev, D. and Roden, E.E., Suboxic deposition of ferric iron by bacteria in opposing gradients of Fe(II) and oxygen, Appl. Environ. Microbiol., 2001, vol. 67, pp. 1328–1334.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. Miot, J., Benzerara, K., Morin, G., Kappler, A., Bernard, S., Obst, M., Férardm C., Skouri-Panet, F., Guigner, J.M., Posth, N., Galvez, M., Brown, G.E., Jr., and Guyot, F., Iron biomineralization by anaerobic neutrophilic iron-oxidizing bacteria, Geochim. Cosmochim. Acta, 2009, vol. 73, pp. 696–711.

    Article  CAS  Google Scholar 

  52. Schaedler, S., Burkhardt, C., Hegler, F., Straub, K.L., Miot, J., Benzerara, K., and Kappler, A., Formation of cell-iron-mineral aggregates by phototrophic and nitrate-reducing anaerobic Fe(II)-oxidizing bacteria, Geomicrobiol. J., 2009, vol. 26, pp. 93–103.

    Article  CAS  Google Scholar 

  53. Liu, J., Wang, Z., Belchik, S.M., Edwards, M.J., Liu, C., and Kennedy, D.W., Identification and characterization of MtoA: a decaheme c-type cytochrome of the neutrophilic Fe(II)-oxidizing bacterium Sideroxydans lithotrophicus ES-1, Front. Microbiol., 2012, 3:37. doi: 10.3389/fmicb.2012.00037

    CAS  PubMed Central  PubMed  Google Scholar 

  54. Ilbert, M. and Bonnefoy, V., Insight into the evolution of the iron oxidation pathways, Biochim. Biophys. Acta, 2013, vol. 1827, pp. 161–175.

    Article  CAS  PubMed  Google Scholar 

  55. Singer, E., Emerson, D., Webb, E.A., Barco, R.A., Kuenen, J.G., Nelson, W.C., Chan, C.S., Comolli, L.R., Ferriera, S., Johnson, J., Heidelberg, J.F., and Edwards, K.J., Mariprofundus ferrooxydans PV-1 the first genome of a marine Fe(II) oxidizing Zetaproteobacterium, PLoS ONE, 6(9): e25386. doi: 10.1371/journal.pone.0025386

  56. Bonnefoy, V. and Holmes, D.S., Genomic insights into microbial iron oxidation and iron uptake strategies in extremely acidic environments, Environ. Microbiol., 2011, vol. 14, pp. 1597–1611.

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  59. Pantke, C., Obst, M., Benzerara, K., Morin, G., Ona-Nguema, G., Dippon, U., and Kappler, A., Green rust formation during Fe(II) oxidation by the nitrate-reducing Acidovorax sp. strain BoFeN1, Environ. Sci. Technol., 2012, vol. 46, pp. 1439–1446.

    Article  CAS  PubMed  Google Scholar 

  60. Carlson, H.K., Clark, I.C., Melnyk, R.A., and Coates, J.D., Toward a mechanistic understanding of anaerobic nitrate-dependent iron oxidation: balancing electron uptake and detoxification, Front. Microbiol., 2012, 3:57. doi: 10.3389/fmicb.2012.00057

    PubMed Central  PubMed  Google Scholar 

  61. Picardal, F., Abiotic and microbial interactions during anaerobic transformations of Fe(II) and NO x , Front. Microbiol., 2012, 3:112. doi: 10.3389/fmicb.2012.00112

    PubMed Central  PubMed  Google Scholar 

  62. Emerson, D., Weiss, J.V., and Megonigal, J.P., Ironoxidizing bacteria are associated with ferric hydroxide precipitates (Fe-plaque) on the roots of wetland plants, Appl. Environ. Microbiol., 1999, vol. 65, pp. 2758–2761.

    CAS  PubMed Central  PubMed  Google Scholar 

  63. Gorshkov, A.I., Drits, V.A., Dubinina, G.A., and Bogdanova, O.Yu., Crystal chemical nature, mineralogy, and genesis of the Franklin seamount hydrothermal field ferruginous and iron-manganese formations, Litol. Polezn. Iskop., 1992, vol. 4, pp. 3–14.

    Google Scholar 

  64. Gorshkov, A.I., Drits, V.A., Dubinina, G.A., Bogdanova, O.A., and Sivtsov, A.V., Role of bacterial activity in formation of hydrothermal iron-manganese formations in the northern part of the Lau Basin (southwestern Pacific), Izv. Akad. Nauk SSSR, Ser. Geol., 1992, vol. 5, pp. 84–93.

    Google Scholar 

  65. Bogdanov, Y.A., Lisitzin, A.P., Binns, R.A., Gorshkov, A.I., Gurvich, E.G., and Dubinina, G.A., Low-temperature hydrothermal deposits of Franklin Seamount, Woodlark Basin, Papua New Guinea, Mar. Geol., 1997, vol. 142, pp. 99–117.

    Article  CAS  Google Scholar 

  66. Kennedy, C.B., Martinez, R.E., Scott, S.D., and Ferris, F.G., Surface chemistry and reactivity of bacteriogenic iron oxides from Axial Volcano, Juan de Fuca Ridge, Geobiology, 2003, vol. 1, pp. 59–69.

    Article  CAS  Google Scholar 

  67. Kato, S., Yanagawa, K., Sunamura, M., Takano, Y., and Ishibashi, J.I., Abundance of Zetaproteobacteria within crustal fluids in back-arc hydrothermal fields of the Southern Mariana Trough, Env. Microbiol., 2009, vol. 11, pp. 3210–3222.

    Article  CAS  Google Scholar 

  68. Blothe, M. and Roden, E.E., Microbial iron redox cycling in a circumneutral-pH groundwater seep, Appl. Environ. Microbiol., 2009, vol. 75, pp. 468–473.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  69. Bruun, A.M., Finster, K., Gunnlaugsson, H., Nornberg, P., and Friedrich, M.W., A comprehensive investigation on iron cycling in a freshwater seep including microscopy, cultivation and molecular community analysis, Geomicrobiol. J., 2010, vol. 27, pp. 15–34.

    Article  CAS  Google Scholar 

  70. Yu, R., Gan, P., MacKay, A.A., Zhang, S., and Smets, B.S., Presence, distribution, and diversity of iron-oxidizing bacteria at a landfill leachate-impacted groundwater surface water interface, FEMS Microbiol. Ecol., 2010, vol. 71, pp. 260–271.

    Article  CAS  PubMed  Google Scholar 

  71. Straub, K.L. and Buchholz-Cleven, B.E., Enumeration and detection of anaerobic ferrous iron-oxidizing, nitrate-reducing bacteria from diverse European sediments, Appl. Environ. Microbiol., 1998, vol. 64, pp. 4846–4856.

    CAS  PubMed Central  PubMed  Google Scholar 

  72. Cárdenas, J.P., Valdés, J., Quatrini, R., Duarte, F., and Holmes, D.S., Lessons from the genomes of extremely acidophilic bacteria and archaea with special emphasis on bioleaching microorganisms, Appl. Microbiol. Biotechnol., 2010, vol. 88, pp. 605–620.

    Article  PubMed  Google Scholar 

  73. Weber, K.A., Urrutia, M.M., Churchill, P.F., Kukkadapu, P.F., and Roden, E.E., Anaerobic redox cycling of iron by freshwater sediment microorganisms, Environ. Microbiol., 2006, vol. 8, pp. 100–113.

    Article  CAS  PubMed  Google Scholar 

  74. Kasama, T. and Murakami, T., The effect of microorganisms on Fe precipitation rates at neutral pH, Chem. Geol., 2001, vol. 180, pp. 117–128.

    Article  CAS  Google Scholar 

  75. James, R.E. and Ferris, F.G., Evidence for microbialmediated iron oxidation at a neutrophilic groundwater spring, Chem. Geol., 2004, vol. 212, pp. 301–311.

    Article  CAS  Google Scholar 

  76. Rentz, J.A., Kraiya, C., Luther, G.W., and Emerson, D., Control of ferrous iron oxidation within circumneutral microbial iron mats by cellular activity and autocatalysis, Environ. Sci. Technol., 2007, vol. 41, pp. 6084–6089.

    Article  CAS  PubMed  Google Scholar 

  77. Mancinelli, R.L. and McKay, C.P., The evolution of nitrogen cycle, Orig. Life Evol. Biosph., 1988, vol. 18, pp. 311–325.

    Article  CAS  PubMed  Google Scholar 

  78. Lovley, D.R., In Origins: Genesis, Evolution and Diversity of Life, Seckbach, J., Ed., Dordrecht: Kluwer, 2004.

  79. Little, C.T.S., Glynn, S.E.J., and Mills, R.A., Fourhundred-and-ninety-million-year record of bacteriogenic iron oxide precipitation at sea-floor hydrothermal vents, Geomicrobiol. J., 2004, vol. 21, pp. 415–429.

    Article  CAS  Google Scholar 

  80. Boyce, A.J., Little, C.T.S., and Russel, M.J., A new fossil vent biota in the Ballynoe barite deposit, Silvermines, Ireland: evidence for intracratonic sea-floor hydrothermal activity about 352 Ma, Econ. Geol., 2003, vol. 98, pp. 649–656.

    CAS  Google Scholar 

  81. Anbar, A.D., Oceans. Elements and evolution, Science, 2008, vol. 322, pp. 1481–1483.

    Article  CAS  PubMed  Google Scholar 

  82. Planavsky, N.J., McGoldrik, P., and Lyons, T.W., Widespread iron-rich conditions in the mid-Proterozoic ocean, Nature, 2011, vol. 477, pp. 448–451.

    Article  CAS  PubMed  Google Scholar 

  83. Rashby, S.E., Sessions, A.L., Summons, R.E., and Newman, D.K., Biosynthesis of 2-methylbacteriohopanepolyols by an anoxygenic phototroph, Proc. Nat. Acad. Sci. USA, 2007, vol. 104, pp. 15099–15104.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  84. Härtner, T., Straub, K.L., and Kannenberg, E., Occurrence of hopanoid lipids in anaerobic Geobacter species, FEMS Microbiol. Lett., 2005, vol. 243, pp. 59–64.

    Article  PubMed  Google Scholar 

  85. Runnegar, B., Precambrian oxygen levels estimated from the biochemistry and physiology of early eukaryotes, Palaeogeograph., Palaeoclimatol., Palaeoecol., 1991, vol. 71, pp. 97–111.

    Article  Google Scholar 

  86. Waldbauer, J.R., Newman, D.K., and Summons, R.E., Microaerobic steroid biosynthesis and the molecular fossil record of Archaean life, Proc. Nat. Acad. Sci. USA, 2011, vol. 108, pp. 13409–13414.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  87. Brock, J.J., Biomarker evidence for green and purple sulphur bacteria in a stratified Palaeoproterozoic sea, Nature, 2005, vol. 437, pp. 866–870.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to G. A. Dubinina.

Additional information

Original Russian Text © G.A. Dubinina, A.Yu. Sorokina, 2014, published in Mikrobiologiya, 2014, Vol. 83, No. 2, pp. 127–142.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dubinina, G.A., Sorokina, A.Y. Neutrophilic lithotrophic iron-oxidizing prokaryotes and their role in the biogeochemical processes of the iron cycle. Microbiology 83, 1–14 (2014). https://doi.org/10.1134/S0026261714020052

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261714020052

Keywords

Navigation