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Microscopic Evidence for Microbial Dissolution of Smectite

Published online by Cambridge University Press:  01 January 2024

Hailiang Dong ,
Joel E. Kostka  and
Jinwook Kim
Hailiang Dong*
Affiliation:
Department of Geology, Miami University, Oxford, OH 45056, USA
Joel E. Kostka
Affiliation:
Oceanography Department, Florida State University, Tallahassee, FL 32306, USA
Jinwook Kim
Affiliation:
Naval Research Laboratory, CODE 7431, NASA Stennis Space Center, MS 39529, USA
*
*E-mail address of corresponding author: [email protected]
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Abstract

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This study was undertaken to investigate mechanisms of mineral transformations associated with microbial reduction of structural Fe(III) in smectite. Shewanella oneidensis strain MR-1 cells were inoculated with lactate as the electron donor and Fe(III) in smectite as the electron acceptor. The extent of Fe(III) reduction was observed to reach up to 26%. Reduction proceeded via association of live bacterial cells with smectite. At the end of incubation, a large fraction of starting smectite was transformed to euhedral flakes of biogenic smectite with different morphology, structure, and composition. Lattice-fringe images obtained from environmental cell transmission electron microscope displayed a decrease of layer spacing from 1.5±0.1 nm for the unreduced smectite to 1.1±0.1 nm for the reduced smectite. The biogenic smectite contained more abundant interlayer cations, apparently as a result of charge compensation for the reduced oxidation state of Fe in the octahedral site. To capture the dynamics of smectite reduction, a separate experiment was designed. The experiment consisted of several systems, where various combinations of carbon source (lactate) and different concentrations of AQDS, an electron shuttle, were used. Selected area electron diffraction patterns of smectite showed progressive change from single-crystal patterns for the control experiment (oxidized, unaltered smectite), to diffuse ring patterns for the no-carbon experiment (oxidized, but altered smectite), to well-ordered single crystal pattern for the experiment amended with 1 mM AQDS (well crystalline, biogenic smectite). Large crystals of vivianite and finegrained silica of biogenic origin were also detected in the bioreduced sample. These data collectively demonstrate that microbial reduction of Fe(III) in smectite was achieved via dissolution of smectite and formation of biogenic minerals. The microbially mediated mineral dissolution-precipitation mechanism has important implications for mineral reactions in natural environments, where the reaction rates may be substantially enhanced by the presence of bacteria.

Keywords

EC-TEMMicrobial Fe(III) ReductionMineral TransformationShewanella oneidensisSmectite
Type
Research Article
Information
Clays and Clay Minerals , Volume 51 , Issue 5 , October 2003 , pp. 502 - 512
Copyright
Copyright © 2003, The Clay Minerals Society

References

Childers, S.E. Ciufo, S. and Lovley, D.R., (2002) Geobacter metallireducens accesses insoluble Fe(III) oxide by chemotaxis Nature 416 767–769 10.1038/416767a.Google Scholar
Cooper, D.C. Picardal, F. Rivera, J. and Talbot, C., (2000) Zinc immobilization and magnetite formation via ferric oxide reduction by Shewanella putrefaciens 200 Environmental Science and Technology 34 100–106 10.1021/es990510x.CrossRefGoogle Scholar
Daulton, T.L. Little, B.J. Lowe, K. and Jones-Meehan, J., (2002) Electron energy loss spectroscopy techniques for the study of microbial chromium(VI) reduction Journal of Microbiological Methods 50 39–54 10.1016/S0167-7012(02)00013-1.Google Scholar
Dong, H. and Peacor, D.R., (1996) TEM observations of coherent stacking relations in smectite, I/S and illite of shales: evidence for MacEwan crystallites and dominance of 2M1 polytypism Clays and Clay Minerals 44 257–275 10.1346/CCMN.1996.0440211.CrossRefGoogle Scholar
Dong, H. Fredrickson, J.K. Kennedy, D.W. Zachara, J.M. Kukkadapu, R.K. and Onstott, T.C., (2000) Mineral transformation associated with the microbial reduction of magnetite Chemical Geology 169 299–318 10.1016/S0009-2541(00)00210-2.Google Scholar
Dong, H. Kukkadapu, R.K. Fredrickson, J.K. Zachara, J.M. Kennedy, D.W. and Kostandarithes, H.M., (2003) Microbial reduction of structural Fe(III) in illite and goethite by a groundwater bacterium Environmental Science and Technology 37 1268–1276 10.1021/es020919d.Google Scholar
Fredrickson, J.K. Zachara, J.M. Kennedy, D.W. Dong, H. Onstott, T.C. Hinman, N.W. and Li, S.M., (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.Google Scholar
Fredrickson, J.K. Kostandarithes, H.M. Li, S.W. Plymale, A.E. and Daly, M.J., (2000) Reduction of Fe(III), Cr(VI), U(VI), and Tc(VII) by Deinococcus radiodurans R 1 Applied and Environmental Microbiology 66 2006–2011 10.1128/AEM.66.5.2006-2011.2000.Google Scholar
Freed, R.L. and Peacor, D.R., (1992) Diagenesis and the formation of authigenic illite-rich I/S crystals in Gulf Coast shales: TEM study of clay separates Journal ofSedimentary Petrology 62 220 234.Google Scholar
Furrer, G. Zysset, M. and Schindler, P.W., (1993) Weathering kinetics of montmorillonite: investigations in batch and mixed-flow reactors Geochemistry of Clay-Pore Fluid Interactions 4 243 262.Google Scholar
Gates, W.P. Jaunet, A.M. Tessier, D. Cole, M.A. Wilkinson, H.T. and Stucki, J.W., (1998) Swelling and texture of iron-bearing smectites reduced by bacteria Clays and Clay Minerals 46 487–497 10.1346/CCMN.1998.0460502.Google Scholar
Hem, J.D., (1985) Study and interpretation of the chemical characteristics ofnatural water Washington, DC United States Government Printing Office.Google Scholar
Hobbie, J.E. Daley, R.J. and Jasper, S., (1977) Use of Nucleopore filters for counting bacteria by fluorescence microscopy Applied and Environmental Microbiology 33 1225 1228.Google Scholar
Kim, J.W. Furukawa, Y. Daulton, T. Lavoie, D. and Newell, S., (2003) Characterization of microbially Fe(III)-reduced nontronite: environmental cell transmission electron microscopy Clays and Clay Minerals 51 382–389 10.1346/CCMN.2003.0510403.Google Scholar
Kostka, J.E. and Nealson, K.H., (1995) Dissolution and reduction of magnetite by bacteria Environmental Science and Technology 29 2535–2540 10.1021/es00010a012.Google Scholar
Kostka, J.E. Nealson, K.H. and Burlage, R.S., (1998) Isolation, cultivation, and characterization of iron- and manganese-reducing bacteria Techniques in Microbial Ecology Oxford, UK Oxford University Press 58 78.Google Scholar
Kostka, J.E. Haefele, E. Viehweger, R. and Stucki, J.W., (1999) Respiration and dissolution of iron(III)-containing clay minerals by bacteria Environmental Science and Technology 33 3127–3133 10.1021/es990021x.Google Scholar
Kostka, J.E. Wu, J. Nealson, K.H. and Stucki, J.W., (1999) The impact of structural Fe(III) reduction by bacteria on the surface chemistry of smectite clay minerals Geochimica et Cosmochimica Acta 63 3705–3713 10.1016/S0016-7037(99)00199-4.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 10.1016/S0016-7037(01)00656-1.Google Scholar
Lear, P.R. and Stucki, J.W., (1989) Effects of iron oxidation state on the specific surface area of nontronite Clays and Clay Minerals 37 547–552 10.1346/CCMN.1989.0370607.Google Scholar
Liu, C. Kota, S. Zachara, J.M. Fredrickson, J.K. and Brinkman, C.K., (2001) Kinetic analysis of the bacterial reduction of goethite Environmental Science and Technology 35 2482–2490 10.1021/es001956c.Google Scholar
Lovley, D.R., (2000) Environmental Microbe-Metal Interactions Washington, D.C. ASM press 10.1128/9781555818098 408 pp.Google Scholar
Lovley, D.R. and Phillips, E.J.P., (1986) Availability of ferric iron for microbial reduction in bottom sediments of the fresh water tidal Potomac River Applied and Environmental Microbiology 52 751 757.Google Scholar
Lovley, D.R. Coates, J.D. Bluent-Harris, E.L. Philips, E.J.P. and Woodward, J.C., (1996) Humic substances as electron acceptors for microbial respiration Nature 382 445–448 10.1038/382445a0.Google Scholar
Lovley, D.R. Fraga, J.L. Blunt-Harris, E.L. Hayes, L.A. Philips, E.J.P. and Coates, J.D., (1998) Humic substances as a mediator for microbially catalyzed metal reduction Acta Hydrochimica et Hydrobiologica 26 152–157 10.1002/(SICI)1521-401X(199805)26:3<152::AID-AHEH152>3.0.CO;2-D.Google Scholar
Luther, G. Shellanbarger, P. and Brendel, P., (1996) Dissolved organic Fe(III) and Fe(II) complexes in salt marsh pore-waters Geochimica et Cosmochimica Acta 60 951–960 10.1016/0016-7037(95)00444-0.Google Scholar
Munch, J.C. and Ottow, J.C.G., (1983) Reductive transformation mechanism of ferric oxides in hydromorphic soils Environmental Biogeochemistry and Ecology Bulletin 35 383 394.Google Scholar
Nevin, K.P. and Lovley, D.R., (2002) Mechanisms for Fe(III) oxide reduction in sedimentary environments Geomicrobiological Journal 19 141–159 10.1080/01490450252864253.Google Scholar
Newman, D.K. and Kolter, R., (2000) A role for excreted quinones in extracellular electron transfer Nature 405 93 97.Google Scholar
Proctor, L.M. and Souza, A., (2001) Method for enumeration of 5-cyano-2,3-ditolyltetrazolium chloride (CTC)-active cells and cell-specific activity of benthic bacteria in riverine, estuarine, and coastal sediments Journal of Microbiological Methods 43 213–222 10.1016/S0167-7012(00)00218-9.Google Scholar
Roden, E.E. and Urrutia, M.M., (2002) Influence of biogenic Fe(II) on bacterial crystalline Fe(III) oxide reduction Geomicrobiological Journal 209 251.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 10.1021/es9506216.Google Scholar
Stucki, J.W. and Tessier, D., (1991) Effects of iron oxidation state on the texture and structural order of Na-nontronite gels Clays and Clay Minerals 39 137–143 10.1346/CCMN.1991.0390204.Google Scholar
Zachara, J.M. Fredrickson, J.K. Li, S.-M. Kennedy, D.W. Smith, S.C. and Gassman, P.L., (1998) Bacterial reduction of crystalline Fe3+ oxides in single phase suspensions and subsurface materials American Mineralogist 83 1426–1443 10.2138/am-1998-11-1232.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 75–93 10.1016/S0016-7037(00)00500-7.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) Geomicrobiological Journal 19 179–207 10.1080/01490450252864271.Google Scholar