Skip to main content
Log in

Biomineralization of a poorly crystalline Fe(III) oxide, akaganeite, by an anaerobic Fe(III)-reducing bacterium (Shewanella alga) isolated from marine environment

  • Published:
Geosciences Journal Aims and scope Submit manuscript

Abstract

Formation of Fe(II)-containing mineral through microbial processes may play an important role in iron and carbon geochemistry in subsurface environments. Fe(III)-reducing bacteria form Fe(II)-containing minerals such as siderite, magnetive, vivianite, and green rust using iron oxides. A psychrotolerant Fe(III)-reducing bacterium,Shewanella alga (PV-4), was used to examine the reduction and biomineralization of a poorly crystalline iron oxide, akaganeite (β-FeOOH), in the absence of a soluble electron shuttle, anthraquinone disulphonate (AQDS), under different atmospheric compositions as well as in HCO 3 buffered medium (30 to 210 mM). Iron biomineralization was also examined under different growth conditions such as incubation time, electron donors, and electron acceptors. The Fe(III)-reducing bacterium, PV-4, reduced akaganeite, Fe(III)-citrate, and Co(III)-EDTA using lactate or H2 as an electron donor. The iron biomineralization of Fe(III) oxide, akaganeite—as it undergos reduction by an iron reducing bacterium—is a complex process influenced by biogeochemical factors including microorganisms, bicarbonate buffer concentration, atmospheric composition, electron donors/acceptors, incubation time, and Eh/pH. From this research we found that microorganisms do participate in the formation of diverse iron minerals and that microbial iron biomineralization may affect Fe and C biogeochemistry in subsurface environments.

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

  • Cairins-Smith, A.G., Hall, A.J. and Russell, M.J., 1992, Mineral theories of the origin of life and an iron sulfide example. Origins of Life Evolution, Biosph, 22, 161–180.

    Article  Google Scholar 

  • Chapelle, F.J., 1994, Groundwater microbiology and geochemistry. New York: John Wiley & Sons, Inc.

    Google Scholar 

  • Childs, C.W., 1992, Ferrihydrite: A review of structure, properties, and occurrence in relation to soils. Z Pfanzenernbhr Bndenk, 155, 441–448.

    Article  Google Scholar 

  • Dong, H., Fredriokson, J.K., Kennedy, D.W., Zachara, J.M., Kukkadapu, R.K. and Onstott, T.C., 2000, Mineral transformations associated with the microbial reduction of magnetite. Chemical Geology, 169, 299–318.

    Article  Google Scholar 

  • Emerson, S., 1976, Early diagenesis in anaerobic lake sediments: chemical equilibria in interstitial waters. Geochimica et Cosmochimica Acta, 40, 925–934.

    Article  Google Scholar 

  • Fredrickson, J.K., Zachara, L.N., Kennedy, D.W., Dong, H., Onstott, T.C., Hinman, N.W. and Li, S., 1998, Biogenic iron mineralization accompanying the dissimilatory reduction of hydrous ferric oxide by a groundwater bacterium. Geochimica et Cosmochimica Acta, 62, 3239–3257.

    Article  Google Scholar 

  • Fredrickson, J.K., Zachara, J.M., Kukkadau, R.K., Gorby, Y.A., Smith, S.C. and Brown, C.F. 2001, Biotransformation of Ni-substituted hydrous ferric oxide by an Fe(III)-reducing bacterium. Environmental Science & Technology, 35, 703–712.

    Article  Google Scholar 

  • Jenne, E.A., 1977, Trace element sorption by sediments and soil-sites and processes. In: Chappel, K.P. (ed.), Symposium on molybdenum in the environment. Marcel Dekker, New York, p. 425–553.

    Google Scholar 

  • Karlin, R. and Levi, S., 1983, Diagenesis of magnetic minerals in recent hemipelagic sediments. Nature, 303, 327–330.

    Article  Google Scholar 

  • Kirchman, D., Sigda, J., Kapuscinski, R. and Mitchell, R., 1982, Statistical analysis of the direct count method for enumeration bacteria. Applied Environmental Microbiology, 44, 376–382.

    Google Scholar 

  • Kukkadapu, R.K., Zachara, J.M., Smith, S.C., Fredrickson, J.K. and Liu, C.X., 2001, Dissimilatory bacterial reduction of Al-substituted goethite in subsurface sediments. Geochimica et Cosmochimica Acta, 65, 2913–2924.

    Article  Google Scholar 

  • Liu, S., Zhou, J., Zhang, C.L., Cole, D.R., Gajdarziska-Josifovska, M. and Phelps, T.J., 1997, Thermophilic Fe(III)-reducing bacteria from the deep subsurface: The evolutionary implications. Science, 277, 1106–1109.

    Article  Google Scholar 

  • Liu, C.X., Kota, S., Zachara, J.M., Fredrickson, K.K. and Brinkman, C.K., 2001, Kinetic analysis of the bacteria reduction of goethite. Environmental Science & Technology, 35, 2482–2490.

    Article  Google Scholar 

  • Lovley, D.R., 1991, dissimilatory Fe(III) and Mn(IV) reduction. Microbialogical Review, 55, 259–287.

    Google Scholar 

  • Lovley, D.R., 1993, Dissimilatory metal reduction. Annual Reviews of Microbiology, 47, 263–290.

    Article  Google Scholar 

  • Lovley, D.R., 1995, Bioremediation of organic and metal contaminants with dissimilatory metal reduction. Journal of Industrial Microbiology, 14, 85–93.

    Article  Google Scholar 

  • Mckay, D.S., Gibson, E.K., Thomas-Keprta, K.L., Vai, H., Romanek, C.S., Clemett, S.J., Maechling, C.R. and Zare, R.N., 1996, Search for past life on Mars: Possible relic biogenic activity in Martian meteorite ALH84001. Science, 273, 924–930.

    Article  Google Scholar 

  • Morita, R.Y., 1975, Psychrophilic bacteria. Bacteriology Review, 39, 144–167.

    Google Scholar 

  • Mortimer, R.J.G. and Coleman, M.L., 1997, Microbial influence on the oxygen isotopic composition of diagenetic siderite. Geochimica et Cosmochimica Acta, 6, 1705–1711.

    Article  Google Scholar 

  • Mortimer, R.J.G., Coleman, M.L. and Rae, J.E., 1997, Effect of bacteria on the elemental composition of early diagenetic siderite: implications for paleoenvironmental interpretations. Sedimentology, 44, 759–765.

    Article  Google Scholar 

  • Nealson, K.H. and Myers, C.R., 1990, Iron reduction by bacteria: A potential role in the genesis of banded iron formation. American Journal of Science, 290A, 35–45.

    Google Scholar 

  • Pedersen, K., 2000, Exploration of deep intraterrestrial microbial life: current perspectives. FEMS Microbiology Letters, 185, 9–16.

    Article  Google Scholar 

  • Phelps, T.J., Raione, E.G., White, D.C. and Fliermans, C.B., 1989, Microbial activity in deep subsurface environments. Geomicrobiology Journal, 7, 79–91.

    Google Scholar 

  • Rajan, S., Mackenzie, F.T. and Glenn, C.R., 1996, A thermodynamic model for water column precipitation of siderite in the Plio-Pleistocene Black Sea. American Journal of Science, 296, 506–548.

    Google Scholar 

  • Roden, E.E. and Zachara, J.M., 1996, Microbial reduction of crystalline Fe(III) oxides: Influence of oxide surface area and potential for cell growth. Environmental Science and Technology, 30, 1618–1628.

    Article  Google Scholar 

  • Roh, Y., Lauf, R.J., McMillan, A.D., Zhang, C., Rawn, C.J., Bai, J. and Phelps, T.J., 2001, Microbial synthesis and the characterization of some metal-doped magnetite. Solid State Communications, 118, 529–534.

    Article  Google Scholar 

  • Roh, Y. and Moon, H.S., 2001, Iron reduction by a psychrotolerant Fe(III)-reducing bacterium isolated from ocean sediment. Geosciences Journal, 5, 183–190.

    Article  Google Scholar 

  • Roh, Y., Liu, S.V., Li, G., Huang, H., Phelps, T.J. and Zhou, J., 2002, Isolation and characterization of Metal-reducingThermoanaerobacter strains from deep subsurface environments of the Piceance Basin, Colorado. Applied and Environmental Microbiology, 68, 6013–6020.

    Article  Google Scholar 

  • Rosselló-Mora, R.A., Caccavo, F. Jr., Osterlehner, K., Springer, N., Springer, N., Spring, S., Schüler, D., Ludwig, W., Amann, R., Vanncanneyt, M. and Schleifer, K.H., 1994. Isolation and taxonomic characterization of a halotolerant, facultatively iron-reducting bacterium. Systematic and Applied Microbiology, 17, 569–573.

    Google Scholar 

  • Rye, K., Dickson, A.D., Schiavon, N., Coleman, M.L. and Cox, M., 1990, Formation of siderite-Mg-calcite-iron sulfide concretions in intertidal marsh and sandflat sediments, north Norfolk, England. Sedimentology, 37, 325–343.

    Article  Google Scholar 

  • Stookey, L.L., 1970, Ferrozine-a new spectrophotometric reagent for iron. Analytical Chemistry, 42, 779–781.

    Article  Google Scholar 

  • Suess, E., 1979, Mineral phases formed in anoxic sediments by microbial decomposition of organic matter. Geochimica et Cosmochimica Acta, 43, 339–352.

    Article  Google Scholar 

  • Stapleton, R.D.Jr., Sabree, Z.L., Palumbo, A.V., Moyer, C., Devol, A., Roh, Y. and Jhou, J., 2003, Metabolic capabilities and distribution ofShewanella isolates from diverse marine environments. Aquatic and Microbial Ecology (in review)

  • Urrutia, M.M., Roden, E.E., Fredrickson, J.M. and Zachara, J.M., 1998, Microbial and surface chemistry controls on reduction of synthetic Fe(III) oxide minerals by the dissimilatory iron-reducing bacteriumShewanella alga. Geomicrobiology Journal, 15, 269–291.

    Google Scholar 

  • Walker, J.C.G., 1984, Suboxic diagenesis in banded iron formation. Nature, 309, 340–342.

    Article  Google Scholar 

  • Zachara, J.M., Fredrickson, J.K., Smith, S.C. and Gassman, P.L., 2001, Solubilization of Fe(III) oxide-bound trace metals by a dissimilatory Fe(III) reducing bacterium. Geochimica et Cosmochimica Acta, 65, 65–73.

    Article  Google Scholar 

  • Zachara, J.M., Kukkadapu, R.K., Fredrickson, J.K., Gorby, Y.A. and Smith, S.C., 2002, Biomineralization of poorly crystalline Fe(III) oxides by dissimilatory metal reducing bacteria (DMRB). Geomicrobiology Journal, 19, 179–207.

    Article  Google Scholar 

  • Zhang, C., Liu, S., Logan, J., Mazumer, R. and Phelps, T.J., 1996, Enhancement of Fe(III), Co(III), and Cr(VI) reduction at elevated temperatures and by a thermophilic bacterium. Applied Biochemistry and Biotechnology, 57/58, 923–932.

    Google Scholar 

  • Zhang, C., Liu, S., Phelps, T.J., Cole, D.R., Horita, J., Fortier, S.M., Elless, M. and Valley, J.W., 1997, Physiochemical, mineralogical, and isotopic characterization of magnetite-rich iron oxides formed by thermophilic iron-reducing bacteria. Geochimica et Cosmochimica Acta, 61, 4621–4632.

    Article  Google Scholar 

  • Zhang, C., Vali, H., Romanek, C.S., Phelps, T.J. and Liu, S., 1988, Formation of single-domain magnetite by a thermophilic bacterium. American Mineralogist, 83, 1409–1418.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Insung Lee.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lee, S.H., Lee, I. & Roh, Y. Biomineralization of a poorly crystalline Fe(III) oxide, akaganeite, by an anaerobic Fe(III)-reducing bacterium (Shewanella alga) isolated from marine environment. Geosci J 7, 217–226 (2003). https://doi.org/10.1007/BF02910288

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02910288

Key words

Navigation