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Iron-oxidizing bacteria in marine environments: recent progresses and future directions

Abstract

Iron-oxidizing bacteria (FeOB) refers to a group of bacteria with the ability to exchange and accumulate divalent iron dissolved in water as trivalent iron inside and outside the bacterial cell. Most FeOB belong the largest bacterial phylum, Proteobacteria. Within this phylum, FeOB with varying physiology with regards to their response to oxygen (obligate aerobes, facultative and obligate anaerobes) and pH optimum for proliferation (neutrophiles, moderate and extreme acidophiles) can be found. Although FeOB have been reported from a wide variety of environments, most of them have not been isolated and their biochemical characteristics remain largely unknown. This is especially true for those living in the marine realm, where the properties of FeOB was not known until the isolation of the Zetaproteobacteria Mariprofundus ferrooxydans, first reported in 2007. Since the proposal of Zetaproteobacteria by Emerson et al., the detection and isolation of those microorganisms from the marine environment has greatly escalated. Furthermore, FeOB have also recently been reported from works on ocean drilling and metal corrosion. This review aims to summarize the current state of phylogenetic and physiological diversity in marine FeOB, the significance of their roles in their environments (on both global and local scales), as well as their growing importance and applications in the industry.

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Fig. 1

a and b are reproduces with permission from American Society for Microbiology: [Appl Environ Microbiol] (Makita et al. 2016). Panel d is reproduced with permission from Springer International Publishing AG: [Arch Microbiol] (Makita et al. 2017)

Fig. 2
Fig. 3

Panel a is reproduced with permission from PLOS: [PLoS One] (Singer et al. 2007), panels c and e are reproduced by permission from Frontiers Media S. A.: [Front Microbiol] (Chiu et al. 2017), panels b and d are reproduced by permission from Springer International Publishing AG.: [Arch Microbiol] (Makita et al. 2017), panel f is reproduced by permission from PLOS: [PLoS One] (Emerson et al. 2007), and panel g is reprinted by permission from Macmillan Publishers Ltd: [ISME Journal] (Mori et al. 2017)

Fig. 4

Panel a is reproduced with permission from Macmillan Publishers Ltd: [ISME Journal] (Chan et al. 2011), panel b is reproduced with permission from PLOS: [PLoS One] (Singer et al. 2007), panels c and d are reproduced with permission from Frontiers Media S. A.: [Front Microbiol] (Chiu et al. 2017), and panels e and f are reproduced with permission from Springer International Publishing AG.: [Arch Microbiol] (Makita et al. 2017)

References

  1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402

    PubMed  CAS  Article  Google Scholar 

  2. Bacelar-Nicolau P, Johnson DB (1999) Leaching of pyrite by acidophilic heterotrophic iron-oxidizing bacteria in pure and mixed cultures. Appl Environ Microbiol 65:585–590

    PubMed  PubMed Central  CAS  Google Scholar 

  3. Bach W, Edwards KJ (2003) Iron and sulfide oxidation within the basaltic ocean crust: Implications for chemolithoautotrophic microbial biomass production. Geochim Cosmochim Acta 67:3871–3887

    CAS  Article  Google Scholar 

  4. Baker BJ, Banfield JF (2003) Microbial communities in acid mine drainage. FEMS Microbiol Ecol 44:139–152

    PubMed  CAS  Article  Google Scholar 

  5. Benson DA, Boguski MS, Lipman DJ, Ostell J, Ouellette BF (1998) GenBank Nucl Acids Res 26:1–7

    PubMed  CAS  Article  Google Scholar 

  6. Cao H, Wang Y, Lee OO, Zeng X, Shao Z, Qian P-Y (2014) Microbial sulfur cycle in two hydrothermal chimneys on the Southwest Indian Ridge. mBio 5(1):e00980-13. https://doi.org/10.1128/mBio.00980-13

    Article  Google Scholar 

  7. Chan CS, Fakra SC, Edwards DC, Emerson D, Banfield JF (2009) Iron oxyhydroxide mineralization on microbial extracellular polysaccharides. Geochim Cosmochim Acta 73:3807–3818

    CAS  Article  Google Scholar 

  8. Chan CS, Fakra SC, Emerson D, Fleming EJ, Edwards KJ (2011) Lithotrophic iron-oxidizing bacteria produce organic stalks to control mineral growth: implications for biosignature formation. ISME J 5:717–727. https://doi.org/10.1038/ismej.2010.173

    PubMed  CAS  Article  Google Scholar 

  9. Chiu BK, Kato S, McAllister SM, Field EK, Chan CS (2017) Novel pelagic iron-oxidizing Zetaproteobacteria from the Chesapeake bay oxic-anoxic transition zone. Front Microbiol 18(8):1280. https://doi.org/10.3389/fmicb.2017.01280

    Article  Google Scholar 

  10. Dang H, Chen R, Wang L, Shao S, Dai L, Ye Y, Guo L, Huang G, Klotz MG (2011) Molecular characterization of putative biocorroding microbiota with a novel niche detection of Epsilon- and Zetaproteobacteria in Pacific Ocean coastal seawaters. Environ Microbiol 13:3059–3074. https://doi.org/10.1111/j.1462-2920.2011.02583.x

    PubMed  CAS  Article  Google Scholar 

  11. Davis RE, Stakes DS, Wheat CG, Moyer CL (2009) Bacterial variability within an iron-silica-manganese-rich hydrothermal mound located off-axis at the Cleft Segment, Juan de Fuca Ridge. Geomicrobiol J 26:570–580

    CAS  Article  Google Scholar 

  12. Davis RE, Moyer C, McAllister S, Rassa A, Tebo B (2010) Spatial and temporal variability of microbial communities from pre- and post-eruption microbial mats collected from Loihi Seamount, Hawaii. Abstr. In: 13th International Symposium on Microbial Ecology, abstr. PS.01.015

  13. Dhillon A, Teske A, Dillon J, Stahl DA, Sogin ML (2003) Molecular characterization of sulfate-reducing bacteria in the Guaymas Basin. Appl Environ Microbiol 69:2765–2772. https://doi.org/10.1128/AEM.69.5.2765-2772.2003

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  14. Dickinson I, Goodall-Copestake W, Thorne MA, Schlitt T, Ávila-Jiménez ML, Pearce DA (2016) Extremophiles in an Antarctic marine ecosystem. Microorganisms 4:8. https://doi.org/10.3390/microorganisms4010008

    PubMed Central  CAS  Article  Google Scholar 

  15. Dyer A, Pillinger M, Harjulab R, Aminc S (2000) Sorption characteristics of radionuclides on synthetic birnessite-type layered manganese oxides. J Mater Chem 10:1867–1874. https://doi.org/10.1039/B002435J

    CAS  Article  Google Scholar 

  16. Eder W, Jahnke LL, Schmidt M, Huber R (2001) Microbial diversity of the brine-seawater interface of the Kebrit Deep, Red Sea, studied via 16S rRNA gene sequences and cultivation methods. Appl Environ Microbiol 67:3077–3085. https://doi.org/10.1128/AEM.67.7.3077-3085.2001

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  17. Edwards KJ, Bond PL, Gihring TM, Banfield JF (2000) An archaeal iron-oxidizing extreme acidophile important in acid mine drainage. Science 287:1796–1799

    PubMed  CAS  Article  Google Scholar 

  18. Edwards KJ, Rogers DR, Wirsen CO, McCollom TM (2003) Isolation and characterization of novel psychrophilic, neutrophilic, Fe-oxidizing, chemolithoautotrophic α- and γ-Proteobacteria from the deep sea. Appl Environ Microbiol 69:2906–2913

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  19. Edwards KJ, Bach W, McCollom TM, Rogers DR (2004) Neutrophilic iron-oxidizing bacteria in the ocean: their habitats, diversity, and roles in mineral deposition rock alteration, and biomass production in the deep-sea. Geomicrobiol J 21:393–404

    CAS  Article  Google Scholar 

  20. Edwards KJ, Glazer BT, Rouxel OJ, Bach W, Emerson D, Davis RE, Toner BM, Chan CS, Tebo BM, Staudigel H, Moyer CL (2011) Ultra-diffuse hydrothermal venting supports Fe-oxidizing bacteria and massive umber deposition at 5000 m off Hawaii. ISME J. https://doi.org/10.1038/ismej.2011.48

    PubMed Central  Article  PubMed  Google Scholar 

  21. Ehrenberg CG (1836) Vorläufige mitteilungen über das wirkliche vorkommen fossiler infusorien und ihre große verbreitung. Poggendorff’s Ann Phys Chem 38:213–227

    Article  Google Scholar 

  22. Emerson D, Ghiorse WC (1993) Ultrastructure and chemical composition of the sheath of Leptothrix discophora SP-6. J Bacteriol 175(24):7808–7818

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  23. Emerson D, Moyer CL (1997) Isolation and characterization of novel iron-oxidizingbacteria that grow at circumneutral pH. Appl Environ Microbiol 63:4784–4792

    PubMed  PubMed Central  CAS  Google Scholar 

  24. Emerson D, Moyer CL (2002) Neutrophilic Fe-oxidizing bacteria are abundant at the Loihi Seamount hydrothermal vents and play a major role in Fe oxide deposition. Appl Environ Microbiol 68:3085–3093

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  25. Emerson D, Floyd MM (2005) Enrichment and isolation of iron-oxidizing bacteria at neutral pH. In: Methods in enzymology, vol. 397. Academic Press, Cambridge MA, pp 112–123

  26. Emerson D, Moyer CL (2010) Microbiology of seamounts: common patterns observed in community structure. Oceanography 23:148–163

    Article  Google Scholar 

  27. Emerson D, Rentz JA, Lilburn TG, Davis RE, Aldrich H, Chan C, Moyer CL (2007) A novel lineage of Proteobacteria involved in formation of marine Fe-oxidizing microbial mat communities. PLoS ONE 2:e667. https://doi.org/10.1371/journal.pone.0000667

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  28. Field EK, Kato S, Findlay AJ, MacDonald DJ, Chiu BK, Luther GW, Chan CS (2016) Planktonic marine iron oxidizers drive iron mineralization under low-oxygen conditions. Geobiology 14:499–508. https://doi.org/10.1111/gbi.12189

    PubMed  CAS  Article  Google Scholar 

  29. Fleming EJ, Davis RE, McAllister SM, Chan CS, Moyer CL, Tebo BM, Emerson D (2013) Hidden in plain sight: discovery of sheath-forming, iron-oxidizing Zetaproteobacteria at Loihi Seamount, Hawaii, USA. FEMS Microbiol Ecol 85:116–127. https://doi.org/10.1111/1574-6941.12104

    PubMed  Article  Google Scholar 

  30. Forget NL, Murdock SA, Juniper SK (2010) Bacterial diversity in Fe-rich hydrothermal sediments at two South Tonga Arc submarine volcanoes. Geobiology 8:417–432. https://doi.org/10.1111/j.1472-4669.2010.00247.x

    PubMed  CAS  Article  Google Scholar 

  31. Fullerton H, Hager KW, McAllister SM, Moyer CL (2017) Hidden diversity revealed by genome-resolved metagenomics of iron-oxidizing microbial mats from Lō’ihi Seamount, Hawai’i. ISME J 11(8):1900–1914. https://doi.org/10.1038/ismej.2017.40

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  32. Ghiorse WC (1984) Biology of iron- and manganese-depositing bacteria. Annu Rev Microbiol 38:515–550

    PubMed  CAS  Article  Google Scholar 

  33. Glazer BT, Rouxel OJ (2009) Redox speciation and distribution within diverse iron-dominated microbial habitats at Loihi Seamount. Geomicrobiol J 26:606–622

    CAS  Article  Google Scholar 

  34. Halbach M, Koschinsky A, Halbach P (2001) Report of the discovery of Gallionella ferruginea from an active hydrothermal field in the deep sea. InterRidge News 10:18–20

    Google Scholar 

  35. Hallbeck L, Pedersen K (1990) Culture parameters regulating stalk formation and growth rate of Gallionella ferruginea. J Gen Microbiol 136:1675–1680

    Article  Google Scholar 

  36. Hallbeck L, Pedersen K (1991) Autotrophic and mixotrophic growth of Gallionella ferruginea. J Gen Microbiol 137:2657–2661

    CAS  Article  Google Scholar 

  37. Hallbeck L, Ståhl F, Pedersen K (1993) Phylogeny and phenotypic characterization of the stalk-forming and iron-oxidizing bacterium Gallionella ferruginea. Microbiology 139(7):1531–1535

    CAS  Google Scholar 

  38. Hallberg R, Ferris FG (2004) Biomineralization by Gallionella. Geomicrobiol J 21:325–330

    CAS  Article  Google Scholar 

  39. Handley KM, Boothman C, Mills RA, Pancost RD, Lloyd JR (2010) Functional diversity of bacteria in a ferruginous hydrothermal sediment. ISME J 4:1193–1205. https://doi.org/10.1038/ismej.2010.38

    PubMed  CAS  Article  Google Scholar 

  40. Hanert HH (2006) The genus Gallionella. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH (eds) The prokaryotes, vol 7. Springer, New York, pp 990–995

    Chapter  Google Scholar 

  41. Hashimoto H, Kobayashi G, Sakuma R, Fujii T, Hayashi N, Suzuki T, Kanno R, Takano M, Takada J (2014) Bacterial nanometric amorphous Fe-based oxide: a potential lithium-ion battery anode material. ACS Appl Mater Interfaces 2014 6:5374–5378

    PubMed  CAS  Article  Google Scholar 

  42. Hegler F, Lösekann-Behrens T, Hanselmann K, Behrens S, Kappler A (2012) Influence of seasonal and geochemical changes on the geomicrobiology of an iron carbonate mineral water spring. Appl Environ Microbiol 78(20):7185–7196

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  43. Hodges TW, Olson JB (2009) Molecular comparison of bacterial communities within iron-containing flocculent mats associated with submarine volcanoes along the Kermadec Arc. Appl Environ Microbiol 75:1650–1657

    PubMed  CAS  Article  Google Scholar 

  44. Iino T, Ito K, Wakai S, Tsurumaru H, Ohkuma M, Harayama S (2014) Iron corrosion induced by nonhydrogenotrophic nitrate-reducing Prolixibacter sp. strain MIC1-1. Appl Environ Microbiol 81(5):1839–1846. https://doi.org/10.1128/AEM.03741-14

    PubMed  Article  Google Scholar 

  45. Iino T, Sakamoto M, Ohkuma M (2015) Prolixibacter denitrificans sp. nov., an iron-corroding, facultatively aerobic, nitrate-reducing bacterium isolated from crude oil, and emended descriptions of the genus Prolixibacter and Prolixibacter bellariivorans. Int J Syst Evol Microbiol 65(9):2865–2869. https://doi.org/10.1099/ijs.0.000343

    PubMed  CAS  Article  Google Scholar 

  46. Javaherdashti R (2008) Microbiologically influenced corrosion: an engineering insight. Springer, New York

    Google Scholar 

  47. Juniper SK, Fouquet Y (1988) Filamentous iron-silica deposits from modern and ancient hydrothermal sites. Can Miner 26:859–869

    CAS  Google Scholar 

  48. Kato S, Kobayashi C, Kakegawa T, Yamagishi A (2009a) Microbial communities in iron-silica-rich microbial mats at deep-sea hydrothermal fields of the Southern Mariana Trough. Environ Microbiol 11:2094–2111

    PubMed  CAS  Article  Google Scholar 

  49. Kato S, Yanagawa K, Sunamura M, Takano Y, Ishibashi J, Kakegawa T, Utsumi M, Yamanaka T, Toki T, Noguchi T, Kobayashi K, Moroi A, Kimura H, Kawarabayasi Y, Marumo K, Urabe T, Yamagishi A (2009b) Abundance of Zetaproteobacteria within crustal fluids in back-arc hydrothermal fields of the Southern Mariana Trough. Environ Microbiol 11:210–3222

    Google Scholar 

  50. Kato S, Ohkuma M, Powell DH, Krepski ST, Oshima K, Hattori M, Shapiro N, Woyke T, Chan CS (2015) Comparative genomic insights into ecophysiology of neutrophilic, microaerophilic iron oxidizing bacteria. Front Microbiol 6:1265. https://doi.org/10.3389/fmicb.2015.01265

    PubMed  PubMed Central  Article  Google Scholar 

  51. Katsoyiannis IA, Zouboulis AI (2006) Use of iron- and manganese-oxidizing bacteria for the combined removal of iron, manganese and arsenic from contaminated groundwater. Water Qual Res J Can 41(2):117–129

    CAS  Article  Google Scholar 

  52. Kennedy CB, Scott SD, Ferris FG (2003a) Characterization of bacteriogenic iron oxide deposits from Axial Volcano, Juan de Fuca Ridge, Northeast Pacific Ocean. Geomicrobiol J 20:199–214

    CAS  Article  Google Scholar 

  53. Kennedy CB, Martinez RE, Scott SD, Ferris FG (2003b) Surface chemistry and reactivity of bacteriogenic iron oxides from Axial Volcano, Juan de Fuca Ridge, north-east Pacific Ocean. Geobiology 1:59–69

    CAS  Article  Google Scholar 

  54. Kennedy CB, Scott SD, Ferris FG (2003c) Ultrastructure and potential sub- seafloor evidence of bacteriogenic iron oxides from Axial Volcano, Juan de Fuca Ridge, north-east Pacific Ocean. FEMS Microbiol Ecol 43:247–254

    PubMed  CAS  Article  Google Scholar 

  55. Kikuchi S, Makita H, Mitsunobu S, Terada Y, Yamaguchi N, Takai K, Takahashi Y (2011) Application of synchrotron based µ-XRF-XAFS to the speciation of Fe on single stalk in bacteriogenic iron oxides (BIOS). Chem Lett 40:680–681

    CAS  Article  Google Scholar 

  56. Kikuchi S, Makita H, Takai K, Yamaguchi N, Takahashi Y (2014) Characterization of biogenic iron oxides collected by the newly designed liquid culture method using diffusion chambers. Geobiology. https://doi.org/10.1111/gbi.12073

    PubMed  Article  Google Scholar 

  57. Klueglein N, Kappler A (2013) 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(2):180–190. https://doi.org/10.1111/gbi.12019

    PubMed  CAS  Article  Google Scholar 

  58. Kucera S, Wolfe RS (1957) A selective enrichment method for Gallionella ferruginea. J Bacteriol 74:344–349

    PubMed  PubMed Central  CAS  Google Scholar 

  59. Kumeria T, Maher S, Wang Y, Kaur G, Wang L, Erkelens M, Forward P, Lambert MF, Evdokiou A, Losic D (2016) Naturally derived iron oxide nanowires from bacteria for magnetically triggered drug release and cancer hyperthermia in 2D and 3D culture environments: bacteria bio film to potent cancer therapeutic. Biomacromolecules 17(8):2726–2736. https://doi.org/10.1021/acs.biomac.6b00786

    PubMed  CAS  Article  Google Scholar 

  60. Kurane R, Hatamochi K, Kakuno T, Kiyohara M, Kawaguchi K, Mizuno Y, Hirano M, Taniguchi Y (1994) Purification and characterization of lipid bioflocculant produced by Rhodococcus erythropolis. Biosci Biotechnol Biochem 58:1977–1982. https://doi.org/10.1271/bbb.58.1977

    CAS  Article  Google Scholar 

  61. Langley S, Gault AG, Ibrahim A, Takahashi Y, Renaud R, Fortin D, Clark ID, Ferris FG (2009) Sorption of strontium onto bacteriogenic iron oxides. Environ Sci Technol 43:1008–1014. https://doi.org/10.1021/es802027f

    PubMed  CAS  Article  Google Scholar 

  62. Laufer K, Nordhoff M, Halama M, Martinez RE, Obst M, Nowak M, Stryhanyuk H, Richnow HH, Kappler A (2017) Microaerophilic Fe(II)-oxidizing Zetaproteobacteria isolated from low-Fe marine coastal sediments: physiology and composition of their twisted stalks. Appl Environ Microbiol 83(8):e03118–e03116. https://doi.org/10.1128/AEM.03118-16

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  63. Makita H, Nakahara Y, Fukui H, Miyanoiri Y, Katahira M. Takeda M, Koizumi J (2006) Identification of 2-(Cysteinyl)amido-2-deoxy-D-galacturonic acid residue from the sheath of Leptothrix cholodnii. Biosci Biotechnol Biochem 70:1265–1268. https://doi.org/10.1271/bbb.70.1265

    PubMed  CAS  Article  Google Scholar 

  64. Makita H, Kikuchi S, Mitsunobu S, Takaki Y, Yamanaka T, Toki T, Noguchi T, Nakamura K, Abe M, Hirai M, Yamamoto M, Uematsu K, Miyazaki J, Nunoura T, Takahashi Y, Takai K (2016) Comparative analysis of microbial communities in iron-dominated flocculent mats in deep sea hydrothermal environments. Appl Environ Microbiol 82(19):5741–5755. https://doi.org/10.1128/AEM.01151-16

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  65. Makita H, Tanaka E, Mitsunobu S, Miyazaki M, Nunoura T, Uematsu K, Takaki Y, Nishi S, Shimamura S, Takai K (2017) Mariprofundus micogutta sp. nov., a novel iron-oxidizing zetaproteobacterium isolated from a deep-sea hydrothermal field at the Bayonnaise knoll of the Izu-Ogasawara arc, and a description of Mariprofundales ord. nov. and Zetaproteobacteria classis nov. Arch Microbiol 199(2):335–346. https://doi.org/10.1007/s00203-016-1307-4

    PubMed  CAS  Article  Google Scholar 

  66. Makita H, Nishi S, Takaki Y, Tanaka E, Nunoura T, Mitsunobu S, Takai K (2018) Draft genome sequence of Mariprofundus micogutta strain ET2. Genome Announ. 6(20):e00342-18

    Article  Google Scholar 

  67. McAllister SM, Davis RE, McBeth JM, Tebo BM, Emerson D, Moyer CL (2011) Biodiversity and emerging biogeography of the neutrophilic iron-oxidizing Zetaproteobacteria. Appl Environ Microbiol 77(15):5445–5457. https://doi.org/10.1128/AEM.00533-11

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  68. McAllister SM, Barnett JM, Heiss JW, Findlay AJ, MacDonald DJ, Dow CL, Luther GW, Michael HM, Chan CS (2015) Dynamic hydrologic and biogeochemical processes drive microbially enhanced iron and sulfur cycling within the intertidal mixing zone of a beach aquifer. Limnol Oceanogr 60:329–345. https://doi.org/10.1111/lno.10029

    CAS  Article  Google Scholar 

  69. McBeth JM, Little BJ, Ray RI, Farrar KM, Emerson D (2011) Neutrophilic iron-oxidizing “Zetaproteobacteria” and mild steel corrosion in nearshore marine environments. Appl Environ Microbiol 77:1405–1412

    PubMed  CAS  Article  Google Scholar 

  70. Mitsunobu S, Shiraishi F, Makita H, Orchtt B, Kikuchi S, Jorgensen B, Takahashi Y (2012) Bacteriogenic Fe(III)(oxyhydr)oxides characterized by synchrotron microprobe coupled with spatially-resolved phylogenetic analysis. Environ Sci Technol 46:3304–3311

    PubMed  CAS  Article  Google Scholar 

  71. Mogi T, Ishii T, Hashimoto K, Nakamura R (2013) Low-voltage electrochemical CO2 reduction by bacterial voltage-multiplier circuits. Chem Commun 49:3967–3969

    CAS  Article  Google Scholar 

  72. Mori JF, Scott JJ, Hager KW, Moyer CL, Küsel K, Emerson D (2017) Physiological and ecological implications of an iron- or hydrogen-oxidizing member of the Zetaproteobacteria, Ghiorsea bivora, gen. nov., sp. nov. ISME J 11(11):2624–2636. https://doi.org/10.1038/ismej.2017.132

    PubMed  PubMed Central  Article  Google Scholar 

  73. Moyer CL, Dobbs FC, Karl DM (1994) Estimation of diversity and community structure through restriction fragment length polymorphism distribution analysis of bacterial 16S rRNA genes from a microbial mat at an active, hydrothermal vent system, Loihi Seamount, Hawaii. Appl Environ Microbiol 60:871–879

    PubMed  PubMed Central  CAS  Google Scholar 

  74. Moyer CL, Dobbs FC. Karl DM (1995) Phylogenetic diversity of the bacterial community from a microbial mat at an active, hydrothermal vent system, Loihi Seamount, Hawaii. Appl Environ Microbiol 61:1555–1562

    PubMed  PubMed Central  CAS  Google Scholar 

  75. Mumford AC, Adaktylou IJ, Emerson D (2016) Peeking under the iron curtain: development of a microcosm for imaging the colonization of steel surfaces by Mariprofundus sp. strain DIS-1, an oxygen-tolerant Fe-oxidizing bacterium. Appl Environ Microbiol 82(22):6799–6807

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  76. Orcutt BN, Bach W, Becker K, Fisher AT, Hentscher M, Toner BM, Wheat CG, Edwards KJ (2011) Colonization of subsurface microbial observatories deployed in young ocean crust. ISME J 5:692–703. https://doi.org/10.1038/ismej.2010.157

    PubMed  CAS  Article  Google Scholar 

  77. Peng X, Ta K, Chen S, Zhang L, Xu H (2015) Coexistence of Fe(II)- and Mn(II)-oxidizing bacteria govern the formation of deep sea umber deposits. Geochim Cosmochim Acta 169:200–216. https://doi.org/10.1016/j.gca.2015.09.011

    CAS  Article  Google Scholar 

  78. Pokhrel D, Viraraghavan T (2009) Biological filtration for removal of arsenic from drinking water. J Environ Manag 90(5):1956–1961. https://doi.org/10.1016/j.jenvman.2009.01.004

    CAS  Article  Google Scholar 

  79. Pringsheim EG (1949) Iron bacteria. Biol Rev Camb Philos Soc 24:200–245

    PubMed  CAS  Article  Google Scholar 

  80. Rassa AC, McAllister SM, Safran SA, Moyer CL (2009) Zeta-Proteobacteria dominate the colonization and formation of microbial mats in low-temperature hydrothermal vents at Loihi Seamount, Hawaii. Geomicrobiol J 26:623–638

    CAS  Article  Google Scholar 

  81. Rawlings DE, Johnson DB (2007) The microbiology of biomining: development and optimization of mineral-oxidizing microbial consortia. Microbiology 153:315–324

    PubMed  CAS  Article  Google Scholar 

  82. Reyes C, Dellwig O, Dähnke K, Gehre M, Noriega-Ortega B, Böttcher ME, Meister P, Friedrich MW (2016) Bacterial communities potentially involved in iron-cycling in Baltic Sea and North Sea sediments revealed by pyrosequencing. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fiw054

    PubMed  Article  Google Scholar 

  83. Rohwerder T, Gehrke T, Kinzler K, Sand W (2003) Bioleaching review part A: Progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation. Appl Microbiol Biotechnol 63:239–248

    PubMed  CAS  Article  Google Scholar 

  84. Rubin-Blum M, Antler G, Tsadok R, Shemesh E, Austin JA Jr, Coleman DF, Goodman-Tchernov BN, Ben-Avraham Z, Tchernov D (2014) First evidence for the presence of iron-oxidizing Zetaproteobacteria at the Levantine continental margins. PLoS ONE 9:e91456. https://doi.org/10.1371/journal.pone.0091456

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  85. Sahabi DM, Takeda M, Suzuki I, Koizumi J (2010) Comparison of arsenate, lead, and cadmium adsorption onto aged biofilter media. J Environ Eng 136(5):493–500

    CAS  Article  Google Scholar 

  86. Schwertmann U, Cornell RM (2000) The iron oxides in the laboratory: preparation and characterization. Wiley-VCH, New York

    Book  Google Scholar 

  87. Singer E, Emerson D, Webb EA, Barco RA, Kuenen JG, Nelson WC, Chan CS, Comolli LR, Ferriera S, Johnson J, Heidelberg JF, Edwards KJ (2011) Mariprofundus ferrooxydans PV-1 the first genome of a marine Fe(II) oxidizing Zetaproteobacterium. PLoS ONE 6(9):e25386. https://doi.org/10.1371/journal.pone.0025386

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  88. Staudigel H, Hart SR, Pile A, Bailey BE, Baker ET, Brooke S, Connelly DP, Haucke L, German CR, Hudson I, Jones D, Koppers AA, Konter J, Lee R, Pietsch TW, Tebo BM, Templeton AS, Zierenberg R, Young CM (2006) Vailulu’u Seamount, Samoa: life and death on an active submarine volcano. Proc Natl Acad Sci USA 103(17):6448–6453. https://doi.org/10.1073/pnas.0600830103

    PubMed  CAS  Article  Google Scholar 

  89. Stauffert M, Cravo-Laureau C, Jezequel R, Barantal S, Cuny P, Gilbert F, Cagnon C, Militon C, Amouroux D, Mahdaoui F, Bouyssiere B, Stora G, Merlin F-X, Duran R (2013) Impact of oil on bacterial community structure in bioturbated sediments. PLoS ONE 8:e65347. https://doi.org/10.1371/journal.pone.0065347

    PubMed  PubMed Central  CAS  Article  Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

  91. Sudek LA, Templeton AS, Tebo BM, Staudigel H (2009) Microbial ecology of Fe (hydr)oxide mats and basaltic rock from Vailulu’u Seamount, American Samoa. Geomicrobiol J 26:581–596

    CAS  Article  Google Scholar 

  92. Summers ZM, Gralnick JA, Bond DR (2013) Cultivation of an obligate Fe(II)-oxidizing lithoautotrophic bacterium using electrodes. MBio 4(1):e00420–e00412. https://doi.org/10.1128/mBio.00420-12

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  93. Suzuki I (2012) Seibutsu-Kogaku Kaishi. Soc Biosci Bioeng 90(4):170–173

    CAS  Google Scholar 

  94. Sylvan JB, Pyenson BC, Rouxel O, German CR, Edwards KJ (2012) Time-series analysis of two hydrothermal plumes at 9°50′N East Pacific Rise reveals distinct, heterogeneous bacterial populations. Geobiology 10:178–192. https://doi.org/10.1111/j.1472-4669.2011.00315.x

    PubMed  CAS  Article  Google Scholar 

  95. Takeda M, Makita H, Ohno K, Nakahara Y, Koizumi J (2005) Structural analysis of the sheath of a sheathed bacterium, Leptothrix cholodnii. Int J Biol Macromol 37:92–98

    PubMed  CAS  Article  Google Scholar 

  96. Tamura T, Tsunai K, Ishimaru Y, Nakata A (1999) Iron and manganese removal by iron bacteria in ground water. Suidou-Kyokai-Zasshi 68(6):2–13 (1999)

    Google Scholar 

  97. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  98. Thapa Chhetri R, Suzuki I, Fujita T, Takeda M, Koizumi J, Fujikawa Y, Minami A, Hamasaki T, Sugahara M (2013) Bacterial diversity in biological filtration system for the simultaneous removal of arsenic, iron and manganese from groundwater. J Water Environ Technol 12(2):135–149. https://doi.org/10.2965/jwet.2014.135

    Article  Google Scholar 

  99. Toner MB, Santelli CM, Marcus MA, Wirth R, Chan CS, McCollom T, Bach W, Edwards KJ (2009) Biogenic iron oxyhydroxide formation at mid-ocean ridge hydrothermal vents: Juan de Fuca Ridge. Geochim Cosmochim Acta 73:388–403

    CAS  Article  Google Scholar 

  100. Toner MB, Berquo T, Michel FM, Sorensen JV, Templeton AS, Edwards KJ (2012) Mineralogy of iron microbial mats from Loihi Seamount. Front Microbiol 3:118. https://doi.org/10.3389/fmicb.2012.00118

    PubMed  PubMed Central  Article  Google Scholar 

  101. Wang L, Kumeria T, Santos A, Forward P, Lambert MF, Losic D (2016) Iron oxide nanowires from bacteria biofilm as an efficient visible-light magnetic photocatalyst. ACS Appl Mater Interfaces 8(31):20110–20119. https://doi.org/10.1021/acsami.6b06486

    PubMed  CAS  Article  Google Scholar 

  102. Wedepohl HK (1995) The composition of the continental crust. Geochimicaet Cosmochimica Acta 59(7):1217–1232

    CAS  Article  Google Scholar 

  103. Winogradsky S (1888) Ueber Eisenbacterien. Bot Zeit 17:262–269

    Google Scholar 

  104. Wu W, Swanner ED, Hao L, Zeitvogel F, Obst M, Pan Y, Kappler A (2014) Characterization of the physiology and cell-mieneral interactions of the marine anoxygenic phototrophic Fe(II) oxidizer Rhodovulum iodosum-implications for Precambrian Fe(II) oxidation. FEMS Microbiol Ecol 88:503–515

    PubMed  CAS  Article  Google Scholar 

  105. Yayam M (2014) Upward biological contact filtration. In: Nakamoto N, Graham N, Collins R, Gimbel R (eds) Progress in slow sand and alternative biofiltration processes, Chap. 66. London: IWA Publishing

    Google Scholar 

  106. Zhang X, Fang J, Bach W, Edwards KJ, Orcutt BN, Wang F (2016) Nitrogen stimulates the growth of subsurface basalt-associated microorganisms at the Western flank of the mid-Atlantic Ridge. Front Microbiol 3(7):633. https://doi.org/10.3389/fmicb.2016.00633

    Article  Google Scholar 

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Acknowledgements

Dr. Chong Chen and Dr. Donald Pan (JAMSTEC) are gratefully acknowledged for their help in improving an earlier version of the manuscript. This research was partially supported by KAKENHI JP26820389 and JP18K04595 to HM.

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Correspondence to Hiroko Makita.

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Makita, H. Iron-oxidizing bacteria in marine environments: recent progresses and future directions. World J Microbiol Biotechnol 34, 110 (2018). https://doi.org/10.1007/s11274-018-2491-y

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Keywords

  • Biodiversity
  • Biogeography
  • FeOB
  • Iron-oxidizing bacteria
  • Marine environments
  • Microbial ecology
  • Zetaproteobacteria