Biogeochemical and Environmental Factors in Fe Biomineralization: Magnetite and Siderite Formation | Clays and Clay Minerals | Cambridge Core (original) (raw)

Abstract

The formation of siderite and magnetite by Fe(III)-reducing bacteria may play an important role in C and Fe geochemistry in subsurface and ocean sediments. The objective of this study was to identify environmental factors that control the formation of siderite (FeCO3) and magnetite (Fe3O4) by Fe(III)-reducing bacteria. Psychrotolerant (<20°C), mesophilic (20–35°C) and thermophilic (>45°C) Fe(III)-reducing bacteria were used to examine the reduction of a poorly crystalline iron oxide, akaganeite (β-FeOOH), without a soluble electron shuttle, anthraquinone disulfuonate (AQDS), in the presence of N2, N2-CO2(80:20, V:V), H2 and H2-CO2 (80:20, V:V) headspace gases as well as in -buffered medium (30–210 mM) under a N2 atmosphere. Iron biomineralization was also examined under different growth conditions such as salinity, pH, incubation time, incubation temperature and electron donors. Magnetite formation was dominant under a N2 and a H2 atmosphere. Siderite formation was dominant under a H2-CO2 atmosphere. A mixture of magnetite and siderite was formed in the presence of a N2-CO2 headspace. Akaganeite was reduced and transformed to siderite and magnetite in a -buffered medium (>120 mM) with lactate as an electron donor in the presence of a N2 atmosphere. Biogeochemical and environmental factors controlling the phases of the secondary mineral suite include medium pH, salinity, electron donors, atmospheric composition and incubation time. These results indicate that microbial Fe(III) reduction may play an important role in Fe and C biogeochemistry as well as C sequestration in natural environments.

References

Bazylinski, D.A. Frankel, R.B. and Jannasch, H.W., (1988) Anaerobic magnetite production by a marine, magnetotatic bacterium Nature 334 518–519 10.1038/334518a0.CrossRefGoogle Scholar

Bell, P.E. Mills, A.L. and Herman, J.S., (1987) Biogeochemical conditions favoring magnetite formation during anaerobic iron reduction Applied and Environmental Microbiology 53 2610 2616.CrossRefGoogle ScholarPubMed

Blakemore, R.P., (1982) Magnetotactic bacteria Annual Review of Microbiology 36 217–238 10.1146/annurev.mi.36.100182.001245.CrossRefGoogle ScholarPubMed

Boone, D.R. Liu, Y. Zhao, Z. Balkwill, D.L. Drake, G.R. Stevens, T.O. and Aldrich, H.C., (1995) Bacillus infernus-sp. Nov.: an Fe(III) and Mn(IV) reducing anaerobe from the deep terrestrial subsurface. International Journal of Systematic Bacterialogy 45 441 448.Google Scholar

Dong, H. Fredrickson, 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 10.1016/S0009-2541(00)00210-2.10.1016/S0009-2541(00)00210-2CrossRefGoogle Scholar

Ferris, F.G. Wiese, R.G. and Fyfe, W.S., (1994) Precipitation of carbonate minerals by microorganisms: Implications for silicate weathering and the global carbon dioxide budget Geomicrobiology Journal 12 1–13 10.1080/01490459409377966.CrossRefGoogle Scholar

Fortin, D. Ferris, F.G. and Beveridge, T.J., (1997) Surface mediated mineral development by bacteria Geomicrobiology: Interactions between Microbes and Minerals Washington, D.C. Mineralogical Society of America 161–177 10.1515/9781501509247-007.10.1515/9781501509247-007CrossRefGoogle Scholar

Frankel, R.B. and Blakemore, R.P., (1990) Iron Biominerals New York Plenum Press 435 pp.Google Scholar

Fredrickson, J.K. Zachara, J.M. 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 10.1016/S0016-7037(98)00243-9.10.1016/S0016-7037(98)00243-9CrossRefGoogle 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 10.1021/es001500v.10.1021/es001500vCrossRefGoogle Scholar

Heijman, C.G. Holliger, C. Glaus, M.A. and Schwarzenbach, R.P., (1993) Abiotic reduction of 4-chlorobenzene to 4-chloroaniline in a dissimilatory iron-reducing enrichment culture Applied and Environmental Microbiology 59 4350 4353.CrossRefGoogle Scholar

Heijman, C.G. Grieder, E. Holliger, C. and Schwarzenbach, R.P., (1995) Reduction of nitroaromatic compounds coupled to microbial iron reduction in laboratory aquifer columns Environmental Science & Technology 29 775–783 10.1021/es00003a027.10.1021/es00003a027CrossRefGoogle ScholarPubMed

Juniper, S.K. Martineu, P. Sarrazin, J. and Gelinas, Y., (1995) Microbial-mineral floc associated with nascent hydrothermal activity on coaxial segment, Juan-De-Fuca Ridge Geophysical Research Letters 22 179–182 10.1029/94GL02436.CrossRefGoogle 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 10.1016/S0016-7037(01)00656-1.10.1016/S0016-7037(01)00656-1CrossRefGoogle 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 10.1021/es001956c.10.1021/es001956cCrossRefGoogle ScholarPubMed

Liu, S.V. Zhou, J. Zhang, C. Cole, D.R. Gajdarziska-Josifovska, P. and Phelps, T.J., (1997) Thermophilic Fe(III)-reducing bacteria from the deep subsurface: The evolutionary implications Science 277 1106–1109 10.1126/science.277.5329.1106.10.1126/science.277.5329.1106CrossRefGoogle Scholar

Lovley, D.R., Frankel, R.B. and Blakemore, R.P., (1990) Magnetite formation during microbial dissimilatory iron reduction Iron Biominerals New York Plenum Press 151 166.Google Scholar

Lovley, D.R., (1991) Dissimilatory Fe(III) and Mn(IV) reduction Microbiolgical Review 55 259 287.10.1128/mr.55.2.259-287.1991CrossRefGoogle ScholarPubMed

Lovley, D.R., (1993) Dissimilatory metal reduction Annual Review of Microbiology 47 263–290 10.1146/annurev.mi.47.100193.001403.10.1146/annurev.mi.47.100193.001403CrossRefGoogle ScholarPubMed

Lovely, D.R., (1995) Bioremediation of organic and metal contaminants with dissimilatory metal reduction Journal of Industrial Microbiology 14 85–93 10.1007/BF01569889.10.1007/BF01569889CrossRefGoogle Scholar

Lovley, D.R. and Phillips, E.J.P., (1988) Novel mode of microbial energy metabolism: organic carbon oxidation coupled with dissimilatory reduction of iron and manganese Applied and Environmental Microbiology 54 1472 1480.10.1128/aem.54.6.1472-1480.1988CrossRefGoogle Scholar

Lovley, D.R. Stolz, J.F. Nord, G.L. Jr. and Phillips, E.J.P., (1987) Anaerobic production of magnetite by a dissimilatory iron-reducing microorganism Nature 330 252–254 10.1038/330252a0.10.1038/330252a0CrossRefGoogle Scholar

Mann, S. Sparks, N.H.C. Wade, V.J., Frankel, R.B. and Blakemore, R.P., (1990) Crystallochemical control of iron oxide biomineralization Iron Biominerals New York Plenum Press 21 49.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 61 1705–1711 10.1016/S0016-7037(97)00027-6.10.1016/S0016-7037(97)00027-6CrossRefGoogle 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 10.1046/j.1365-3091.1997.d01-45.x.CrossRefGoogle 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

Nealson, K.H. and Saffarini, D., (1994) Iron and manganese in anaerobic respiration: Environmental significance, physiology, and regulation Annual Reviews of Microbiology 48 311–343 10.1146/annurev.mi.48.100194.001523.10.1146/annurev.mi.48.100194.001523CrossRefGoogle ScholarPubMed

Pedersen, K., (2000) Exploration of deep intraterrestrial microbial life: Current perspectives FEMS Microbiology Letters 185 9–16 10.1111/j.1574-6968.2000.tb09033.x.10.1111/j.1574-6968.2000.tb09033.xCrossRefGoogle ScholarPubMed

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 10.1080/01490458909377851.10.1080/01490458909377851CrossRefGoogle Scholar

Postma, D., (1981) Formation of siderite and vivianite and the pore-water composition of a recent bog sediment in Denmark Chemical Geology 31 225–244 10.1016/0009-2541(80)90088-1.10.1016/0009-2541(80)90088-1CrossRefGoogle Scholar

Pye, 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 10.1111/j.1365-3091.1990.tb00962.x.10.1111/j.1365-3091.1990.tb00962.xCrossRefGoogle 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 10.2475/ajs.296.5.506.10.2475/ajs.296.5.506CrossRefGoogle Scholar

Roden, E.E. and Zachara, J.M., (1996) Microbial reduction of crystalline iron (III) oxides: influence of oxide surfaces area and potential for cell growth Environmental Science & Technology 30 1618–1628 10.1021/es9506216.10.1021/es9506216CrossRefGoogle 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 10.1016/S0038-1098(01)00146-6.CrossRefGoogle Scholar

Rossellomora, R.A. Caccavo, F. Osterlehner, K. Springer, N. Spring, S. Schuler, D. Ludwig, W. Amann, R. Vanncanneyt, M. and Schleifer, K.H., (1994) Isolation and taxonomic characterization of a halotolerant facultatively iron-reducing bacterium Systematic and Applied Microbiology 17 569–573 10.1016/S0723-2020(11)80078-0.CrossRefGoogle Scholar

Schwertmann, U. and Cornell, R.M., (1991) Iron Oxides in the Laboratory New York VCH Publishers, Inc. 137 pp.Google Scholar

Schwertmann, U. Fitzpatrick, R.W., Skinner, H.C.W. and Fitzpatrick, R.W., (1992) Iron minerals in surface environments Biomineralization, Processes of Iron and Manganese Destedt, Germany Catena Verlag 7 30.Google Scholar

Sparks, N.C.H. Mann, S. Bazylinski, D.A. Lovley, D.R. Jannasch, H.W. and Frankel, R.B., (1990) Structure and morphology of magnetite anaerobically-produced by a marine magnetotactic bacterium and dissimilatory iron-reducing bacterium Earth and Planetary Science Letters 98 14–22 10.1016/0012-821X(90)90084-B.CrossRefGoogle Scholar

Stapleton, R.D. Jr., Sabree, J.L., Palumbo, A.V., Moyer, C., Devol, A., Roh, Y. and Zhou, J. (2002) Metabolic capabilities and distribution of Shewanella isolates from diverse marine environments. Limnology and Oceanography (in review).Google Scholar

Suess, E., (1979) Mineral phases formed in anoxic sediments by microbial decomposition of organic matter Geochimica et Cosmochimica Acta 43 339–352 10.1016/0016-7037(79)90199-6.10.1016/0016-7037(79)90199-6CrossRefGoogle Scholar

Walker, J.C.G., (1984) Subtoxic diagenesis in banded iron formation Nature 309 340–342 10.1038/309340a0.10.1038/309340a0CrossRefGoogle 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 10.1080/01490450252864271.10.1080/01490450252864271CrossRefGoogle 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 10.1007/BF02941773.10.1007/BF02941773CrossRefGoogle 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 bacteria Geochimica et Cosmochimica Acta 61 4621–4632 10.1016/S0016-7037(97)00257-3.10.1016/S0016-7037(97)00257-3CrossRefGoogle Scholar

Zhang, C. Vali, H. Romanek, C.S. Phelps, T.J. and Liu, S., (1998) Formation of single-domain magnetite by a thermophilic bacterium American Mineralogist 83 1409–1418 10.2138/am-1998-11-1230.10.2138/am-1998-11-1230CrossRefGoogle Scholar