Hostname: page-component-848d4c4894-xm8r8 Total loading time: 0 Render date: 2024-06-19T17:51:38.209Z Has data issue: false hasContentIssue false
  • English
  • Français

Bioavailability of Fe(III) In Loess Sediments: An Important Source of Electron Acceptors

Published online by Cambridge University Press:  01 January 2024

Michael E. Bishop ,
Deb P. Jaisi ,
Hailiang Dong ,
Ravi K. Kukkadapu  and
Junfeng Ji
Michael E. Bishop
Affiliation:
Department of Geology, Miami University, Oxford, OH 45056, USA
Deb P. Jaisi
Affiliation:
Department of Geology, Miami University, Oxford, OH 45056, USA Department of Geology and Geophysics, Yale University, PO Box 20820, New Haven, CT 06520, USA
Hailiang Dong*
Affiliation:
Department of Geology, Miami University, Oxford, OH 45056, USA Geomicrobiology Laboratory, State Key Laboratory of Geological Processes and Mineral Resources, China University of Geosciences, Beijing, 100083, China Key Laboratory of Biogeology and Environmental Geology of Ministry of Education, Faculty of Earth Sciences, China University of Geosciences — Wuhan, Wuhan, 430074, China
Ravi K. Kukkadapu
Affiliation:
Pacific Northwest National Laboratory, Richland, Washington 99352, USA
Junfeng Ji
Affiliation:
Department of Earth Sciences, Nanjing University, Nanjing China
*
* E-mail address of corresponding author: dongh@muohio.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Fe-reducing micro-organisms can change the oxidation state of structural Fe in clay minerals. The interactions with complex clays and clay minerals in natural materials remain poorly understood, however. The objective of this study was to determine if Fe(III) in loess was available as an electron acceptor and to study subsequent mineralogical changes. The loess samples were collected from St. Louis (Peoria), Missouri, USA, and Huanxia (HX) and Yanchang (YCH), in the Shanxi Province of China. The total Fe concentrations for the three samples was 1.69, 2.76, and 3.29 wt.%, respectively, and Fe(III) content was 0.48, 0.69, and 1.27 wt.%, respectively. All unreduced loess sediments contained Fe (oxyhydr)oxides and phyllosilicates. Bioreduction experiments were performed using Shewanella putrefaciens CN32 with lactate as the sole electron donor and Fe(III) in loess as the sole electron acceptor with and without anthraquinone-2, 6-disulfonate (AQDS) as an electron shuttle. Experiments were performed in non-growth (bicarbonate buffer) and growth (M1) media. The unreduced and bioreduced solids were analyzed by X-ray diffraction, Mössbauer spectroscopy, diffuse reflectance spectroscopy, and scanning electron microscopy/energy dispersive spectroscopy. Despite many similarities among the three loess samples, the extent and rate of Fe(III) reduction varied significantly. In the presence of AQDS the extent of reduction in the non-growth experiment was 25% of total Fe(III) in HX, 34% in Peoria, and 38% in YCH. The extent of reduction in the growth experiment was 72% in HX, 94% in Peoria, and 65% in YCH. The extent of bioreduction was less in the absence of AQDS. Overall, AQDS and the M1 growth medium significantly enhanced the rate and extent of bioreduction. Fe(III) in (oxyhydr)oxides and phyllosilicates was bioreduced. Siderite was absent in control samples, but was identified in bioreduced samples. The present research suggests that Fe(III) in loess sediments is an important potential source of electron acceptors that could support microbial activity under favorable conditions.

Keywords

BioreductionIronLoessMineral TransformationShewanella putrefaciens
Type
Article
Information
Clays and Clay Minerals , Volume 58 , Issue 4 , August 2010 , pp. 542 - 557
Copyright
Copyright © The Clay Minerals Society 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amonette, J.E. and Templeton, C., 1998 Improvements to the quantitative assay of nonrefractory minerals for Fe(II) and total Fe using 1, 10-Phenanthroline Clays and Clay Minerals 46 51–62 10.1346/CCMN.1998.0460106.CrossRefGoogle Scholar
Anastácio, A.S. Aouad, A. Sellin, P. Fabris, J.D. Bergaya, F. and Stucki, J.W., 2008 Characterization of a redox-modified clay mineral with respect to its suitability as a barrier in radioactive waste confinement Applied Clay Science 39 172–179 10.1016/j.clay.2007.05.007.CrossRefGoogle Scholar
Andrade, S. Hypolito, R. Ulbrich, H.H. and Silva, M.L., 2002 Technical note on iron (II) oxide determination in rocks and minerals Chemical Geology 182 85–89 10.1016/S0009-2541(01)00274-1.CrossRefGoogle Scholar
Balsam, W.L. and Ji, J.F. (1999) Mineralogic variations in the Chinese loess sequence determined by NUV/VIS/NIR reflectance spectra. GSA Abstracts with Programs, 31, A-54.Google Scholar
Bazylinski, D.A. and Frankel, R.B., 2004 Magnetosome formation in prokaryotes Nature Review Microbiology 2 217–230 10.1038/nrmicro842.CrossRefGoogle ScholarPubMed
Chanal, A. Chapon, V. Benzerara, K. Barakat, M. Christen, R. Achouak, W. Barras, F. and Heulin, T., 2006 The desert of Tataouine: an extreme environment that hosts a wide diversity of microorganisms and radiotolerant bacteria Environmental Microbiology 8 514–525 10.1111/j.1462-2920.2005.00921.x.CrossRefGoogle ScholarPubMed
Chen, T.H. Xu, H.F. Ji, J.F. Chen, J. and Chen, Y., 2003 Formation mechanism of ferromagnetic minerals in loess of China: TEM investigation Chinese Science Bulletin 48 2259–2266 10.1360/03wd0126.CrossRefGoogle Scholar
Chen, T. Xu, H. Xie, Q. Chen, J. Ji, J. and Lu, H., 2005 Characteristics and genesis of maghemite in Chinese loess and paleosols: Mechanism for magnetic susceptibility enhancement in paleosols Earth and Planetary Science Letters 240 790–802 10.1016/j.epsl.2005.09.026.CrossRefGoogle Scholar
Chinese Academy of Sciences, 1979 Comprehensive Survey of Qinghai Lake .Google Scholar
Curry, G.B. Theng, B.K.G. and Zheng, H.H., 1994 Amino acid distribution in a loess-paleosol sequence near Luochuan, Loess Playeau, China Organic Geochemistry 22 287–298 10.1016/0146-6380(94)90175-9.CrossRefGoogle Scholar
Dolgoff, A., 1998 Physical Geology Boston, Massachussets, USA Houghton Mifflin Company 499–504.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 Environmental Science & Technology 37 1268–1276 10.1021/es020919d.CrossRefGoogle Scholar
Dong, H. Kostka, J.E. and Kim, J., 2003 Microscopic evidence for microbial dissolution of smectite Clays and Clay Minerals 51 502–512 10.1346/CCMN.2003.0510504.CrossRefGoogle Scholar
Dong, H. Jaisi, D.P. Kim, J.W. and Zhang, G., 2009 Microbe-clay mineral interactions: a Review American Mineralogist 94 1505–1519 10.2138/am.2009.3246.CrossRefGoogle Scholar
Dorn, R.I. and Oberlander, T.M., 1981 Microbial origin of desert varnish Science 213 1245–1247 10.1126/science.213.4513.1245.CrossRefGoogle ScholarPubMed
Favre, F. Tessier, D. Abdelmoula, M. Genin, J.M. Gates, W.P. and Boivin, P., 2002 Iron reduction and changes in cation exchange capacity in intermittently waterlogged soil European Journal of Soil Science 53 175–183 10.1046/j.1365-2389.2002.00423.x.CrossRefGoogle Scholar
Favre, F. Stucki, J.W. and Boivin, P., 2006 Redox properties of structural Fe in ferruginous smectite. A discussion of the standard potential and its environmental implications Clays and Clay Minerals 54 466–472 10.1346/CCMN.2006.0540407.CrossRefGoogle 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 R1 Applied and Environmental Microbiology 66 2006–2011 10.1128/AEM.66.5.2006-2011.2000.CrossRefGoogle Scholar
Gallet, S. Jahn, B.M. and Torii, M., 1996 Geochemical characterization of the Luochuan loess-paleosol sequence, China, and paleoclimatic implications Chemical Geology 133 67–88 10.1016/S0009-2541(96)00070-8.CrossRefGoogle Scholar
Gates, W.P. Jaunet, A. 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.CrossRefGoogle Scholar
Grimley, D.A. Follmer, L.R. and McKay, E.D., 1998 Magnetic susceptibility and mineral zonations controlled by provenance in loess along the Illinois and central Mississippi River valleys Quaternary Research 49 24–36 10.1006/qres.1997.1947.CrossRefGoogle Scholar
Grimley, D.A., 2000 Glacial and nonglacial sediment contributions to Wisconsin Episode loess in the central United States Geological Society of America Bulletin 112 1475–1495 10.1130/0016-7606(2000)112<1475:GANSCT>2.0.CO;2.2.0.CO;2>CrossRefGoogle Scholar
Hu, X.F. Lu, H. Xu, Q. Dong, L.J. and Hu, X., 2004 Red ratings for loess-paleosol sequences on China’s loess plateau and their paleo-climatic implications Pedosphere 14 430–440.Google Scholar
Jahn, B.M. Gallet, S. and Han, J.M., 2001 Geochemistry of the Xining, Xifeng and Jixian sections, China: Eolian dust provenance and paleosol evolution during the last 140 ka Chemical Geology 178 71–94 10.1016/S0009-2541(00)00430-7.CrossRefGoogle Scholar
Jaisi, D.P. Kukkadapu, R.K. Eberl, D.D. and Dong, H., 2005 Control of Fe(III) site occupancy on the rate and extent of microbial reduction of Fe(III) in nontronite Geochimica et Cosmochimica Acta 69 5429–5440 10.1016/j.gca.2005.07.008.CrossRefGoogle Scholar
Jaisi, DP D H and Liu, C.X., 2007 Influence of biogenic Fe(II) on the extent of microbial reduction of Fe(III) in clay minerals nontronite, illite, and chlorite Geochimica et Cosmochimica Acta 71 1145–1158 10.1016/j.gca.2006.11.027.CrossRefGoogle Scholar
Ji, J.F. Balsam, W.L. Chen, J. and Liu, L.W., 2002 Rapid and precise measurement of hematite and goethite concentrations in the Chinese loess sequences by diffuse reflectance spectroscopy Clays and Clay Minerals 50 210–218 10.1346/000986002760832801.CrossRefGoogle Scholar
Ji, J., Chen, J., Jin, L., Zhang, W., Balsam, W., and Lu, H. (2004) Relating magnetic susceptibility (MS) to the simulated thematic mapper (TM)bands of the Chinese loess: Application of TM image for soil MS mapping on Loess Plateau. Journal of Geophysical Research, 109, B05102.CrossRefGoogle Scholar
Jia, R.F. Yan, B.Z. Li, R.S. Fan, G.C. and Lin, B.H., 1996 Characteristics of magnetotactic bacteria in Duanjiapo loess section, Shaanxi province and their environmental significance Science in China Series D — Earth Sciences 39 478–485.Google Scholar
Judd, D.B. and Wyszecki, G., 1975 Color in Business, Science, and Industry New York John Wiley & Sons.Google Scholar
Kim, J.W. Dong, H. Seabaugh, J. Newell, S.W. and Eberl, D.D., 2004 Role of microbes in the smectite-to-illite reaction Science 303 830–832 10.1126/science.1093245.CrossRefGoogle ScholarPubMed
Komlos, J. Kukkadapu, R.K. Zachara, J.M. and Jaffe, P.R., 2007 Biostimulation of iron reduction and subsequent oxidation of sediment containing Fe-silicates and Fe-oxides: Effect of redox cycling on Fe(III) bioreduction Water Research 41 2996–3004 10.1016/j.watres.2007.03.019.CrossRefGoogle Scholar
Komlos, J. Peacock, A. Kukkadapu, R.K. and Jaffe, P.R., 2008 Long-term dynamics of uranium reduction/reoxidation under low sulfate conditions Geochimica et Cosmochimica Acta 72 3603–3615 10.1016/j.gca.2008.05.040.CrossRefGoogle Scholar
Kostka, J.E. Haefele, E. Viehweger, R. and Stucki, J.W., 1999 Respiration and dissolution of Fe(III)-containing clay minerals by bacteria Environmental Science & Technology 33 3127–3133 10.1021/es990021x.CrossRefGoogle 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 clay minerals Geochimica et Cosmochimica Acta 63 3705–3713 10.1016/S0016-7037(99)00199-4.CrossRefGoogle Scholar
Kostka, J.E. Dalton, D.D. Skelton, H. Dollhopf, S. and Stucki, J.W., 2002 Growth of iron(III)-reducing bacteria on clay minerals as the sole electron acceptor and comparison of growth yields on a variety of oxidized iron forms Applied and Environmental Microbiology 68 6256–6262 10.1128/AEM.68.12.6256-6262.2002.CrossRefGoogle ScholarPubMed
Kukkadapu, R.K. Zachara, J.M. Fredrickson, J.K. and Kennedy, D.W., 2004 Biotransformation of two-line silica-ferrihydrite by a dissimilatory Fe(III)-reducing bacterium: formation of carbonate green rust in the presence of phosphate Geochimica et Cosmochimica Acta 68 2799–2814 10.1016/j.gca.2003.12.024.CrossRefGoogle Scholar
Kukkadapu, R.K. Zachara, J.M. Fredrickson, J.K. McKinley, J.P. Kennedy, D.W. Smith, S.C. and Dong, H.L., 2006 Reductive biotransformation of Fe in shale-limestone saporite containing Fe(III) oxides and Fe(II)/Fe(III) phyllo-silicates Geochimica et Cosmochimica Acta 70 3662–3676 10.1016/j.gca.2006.05.004.CrossRefGoogle Scholar
Leigh, D.S., 1994 Roxana silt of the Upper Mississippi Valley — lithology, source, and paleoenvironment Geological Society of America Bulletin 106 430–442 10.1130/0016-7606(1994)106<0430:RSOTUM>2.3.CO;2.2.3.CO;2>CrossRefGoogle Scholar
Li, Y.L. Zhang, C.L. Yang, J. Deng, B. and Vali, H., 2004 Dissolution of nontronite NAu-2 by a sulfate-reducing bacterium Geochimica et Cosmochimica Acta 68 3251–3260 10.1016/j.gca.2004.03.004.CrossRefGoogle Scholar
Lovley, D.R., 1991 Dissimilatory Fe(llI) and Mn(lV) reduction Microbiology Review 55 259–287.CrossRefGoogle Scholar
Maat, P.B. and Johnson, W.C., 1996 Thermoluminescence and new 14C age estimates for late Quaternary loesses in southwestern Nebraska Geomorphology 17 115–128 10.1016/0169-555X(95)00099-Q.CrossRefGoogle Scholar
Mohanty, S.R. Kollah, B. Hedrick, D.B. Peacock, A.D. Kukkadapu, R.K. and Roden, E.E., 2008 Biogeochemical processes in ethanol stimulated uranium contaminated subsurface sediments Environmental Science & Technology 42 4384–4390 10.1021/es703082v.CrossRefGoogle ScholarPubMed
Moore, D.M. and Reynolds, RC Jr., 1997 X-ray Diffraction and the Identification and Analysis of Clay Minerals New York Oxford University Press.Google Scholar
Muhs, D.R. and Bettis, EA III, 2000 Geochemical variations in Peoria Loess of western Iowa indicate paleowinds of midcontinental North America during the last glaciation Quaternary Research 53 49–61 10.1006/qres.1999.2090.CrossRefGoogle Scholar
Muhs, D.R. Zárate, M. and Markgraf, V., 2001 Eolian records of the Americas and their paleoclimatic significance Interhemispheric Climate Linkages San Diego Academic Press 183–216 10.1016/B978-012472670-3/50015-X.CrossRefGoogle Scholar
Myers, C.R. and Nealson, K.H., 1988 Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor Science 240 1319–1321 10.1126/science.240.4857.1319.CrossRefGoogle ScholarPubMed
Osman, S. Peeters, Z. La Duc, M.T. Mancinelli, R. Ehrenfreund, P. and Venkateswaran, K., 2008 Effect of shadowing on survival of bacteria under conditions simulating the Martian atmosphere and UV radiation Applied and Environmental Microbiology 74 959–970 10.1128/AEM.01973-07.CrossRefGoogle ScholarPubMed
Perry, R.S. Engel, M.H. Botta, O. and Staley, J.T., 2003 Amino acid analyses of desert varnish from the Sonoran and Mojave Deserts Geomicrobiology Journal 20 427–438 10.1080/713851132.CrossRefGoogle Scholar
Rancourt, D.G. and Ping, J.Y., 1991 Voigt-based methods for arbitrary-shape static hyperfine parameter distributions in Mössbauer spectroscopy Nuclear Instrument Methods in Physics research 58 85–97 10.1016/0168-583X(91)95681-3.CrossRefGoogle Scholar
Riberio, F.R. Fabris, J.D. Kostka, J.E. Komadel, P. and Stucki, J.W., 2009 Comparisons of structural iron reduction in smectites by bacteria and dithionite: II. A variable-temperature Mössbauer spectroscopic study of Garfield nontronite Pure and Applied Chemistry 81 1499–1509 10.1351/PAC-CON-08-11-16.CrossRefGoogle Scholar
Roberts, H.M. Muhs, D.R. Wintle, A.G. Duller, G.A.T. and Bettis, E III, 2003 Unprecedented last-glacial mass accumulation rates determined by luminescence dating of loess from western Nebraska Quaternary Research 59 411–419 10.1016/S0033-5894(03)00040-1.CrossRefGoogle Scholar
Shelobolina, E.S. Vanpraagh, C.G. and Lovley, D.R., 2003 Use of ferric and ferrous iron containing minerals for respiration by Desulfitobacterium frappieri Geomicrobiology Journal 20 143–156 10.1080/01490450303884.CrossRefGoogle Scholar
Shelobolina, E.S. Pickering, S.M. and Lovley, D.R., 2005 Fe-cycle bacteria from industrial clays mined in Georgia, USA Clays and Clay Minerals 53 580–586 10.1346/CCMN.2005.0530604.CrossRefGoogle Scholar
Shelobolina, E.E. Nevin, K.P. Blakeney-Hayward, J.D. Johnsen, C.V. Plaia, T.W. Krader, P. Woodard, T. Holmes, D.E. VanPraagh, C.G. and Lovley, D.R., 2007 Geobacter pickeringii sp nov., Geobacter argillaceus sp nov., and Pelosinus fermentans gen. nov., sp nov., isolated from subsurface kaolin lenses International Journal of Systematic and Evolutionary Microbiology 57 126–135 10.1099/ijs.0.64221-0.CrossRefGoogle ScholarPubMed
Smalley, I.J., 1975 Lithology and Genesis New York Dowden, Hutchinson, and Ross.Google Scholar
Smalley, I.J. Jefferson, I.F. Dijkstra, T.A. and Derbyshire, E., 2001 Some major events in the development of the scientific study of loess Earth-Science Reviews 54 5–18 10.1016/S0012-8252(01)00038-1.CrossRefGoogle Scholar
Stookey, L.L., 1970 Ferrozine — a new spectrophotometric reagent for iron Analytical Chemistry 42 779–781 10.1021/ac60289a016.CrossRefGoogle Scholar
Stucki, J.W., Bergaya, F. Lagaly, G. and Theng, B.G.K., 2006 Properties and behavior of iron in clay minerals Handbook of Clay Science 423–476 10.1016/S1572-4352(05)01013-5.CrossRefGoogle Scholar
Stucki, J.W. and Kostka, J.E., 2006 Microbial reduction of iron in smectite Comptes Rendus Geoscience 338 468–475 10.1016/j.crte.2006.04.010.CrossRefGoogle Scholar
Stucki, J.W. Lee, K. Zhang, L. and Larson, R.A., 2002 The effects of iron oxidation state on the surface and structural properties of smectites Pure and Applied Chemistry 74 2079–2092 10.1351/pac200274112145.CrossRefGoogle Scholar
Stucki, JW L K Goodman, B.A. and Kostka, J.E., 2007 Effects of in situ biostimulation on iron mineral speciation in a sub-surface soil Geochimica et Cosmochimica Acta 71 835–843 10.1016/j.gca.2006.11.023.CrossRefGoogle Scholar
Sun, J.M., 2002 Source Regions and formation of the loess sediments on the high mountain regions of northwest China Quaternary Research 3 341–351 10.1006/qres.2002.2381.CrossRefGoogle Scholar
Thorp, J. and Smith, H.T.U., 1952 Pleistocene eolian deposits of the United States, Alaska, and parts of Canada. National Research Council Committee for the Study of Eolian Deposits New York Geological Society of America.Google Scholar
Van Der Zee, C. Slomp, C.P. Rancourt, D.G. de Lange, G.J. and Raaphorst, W.V., 2005 A Mössbauer spectroscopic study of the iron redox transition in eastern Mediterranean sediments Geochimica et Cosmochimica Acta 69 441–453 10.1016/j.gca.2004.07.003.CrossRefGoogle Scholar
Wade, L. Agresti, D.G. Wdowiak, T.J. and Armendarez, L.P., 1999 A Mössbauer investigation of iron-rich terrestrial hydrothermal vent systems: lessons for Mars exploration Journal of Geophysical Research 104 8489–8507 10.1029/1998JE900049.CrossRefGoogle ScholarPubMed
Wang, F. Wang, P. Chen, M. and Xiao, X., 2004 Isolation of extremophiles with the detection and retrieval of Shewanella strains in deep-sea sediments from the west Pacific Extremophiles 8 165–168 10.1007/s00792-003-0365-0.CrossRefGoogle ScholarPubMed
Wang, H. Follmer, L.R. and Liu, J.C., 2000 Isotope evidence of El Nino — southern oscillation cycles in loess-paleosol record in the central United States Geology 28 771–774 10.1130/0091-7613(2000)28<771:IEOPNO>2.0.CO;2.2.0.CO;2>CrossRefGoogle Scholar
Wang, H. Hughes, R. Steele, J.D. Lepley, S.W. and Tian, J., 2003 Correlation of climate cycles in middle Mississippi Valley loess and Greenland ice Geology 31 179–182 10.1130/0091-7613(2003)031<0179:COCCIM>2.0.CO;2.2.0.CO;2>CrossRefGoogle Scholar
Xu, H.F. and Chen, T., 2008 Microbe-templated calcite nano-fibers in Chinese Loess Plateau: Potential carbon dioxide sinker Geochimica et Cosmochimica Acta 72 A1046 10.1016/j.gca.2008.04.019.Google Scholar
Xu, Y., 1993 Clay Mineralogy in Salt Lakes of China Beijing Science Publishing House.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 Fe(III) oxides in single phase suspensions and subsurface materials American Mineralogist 83 1426–1443 10.2138/am-1998-11-1232.CrossRefGoogle Scholar
Zavarzina, D.G. Alekseev, A.O. and Alekseeva, T.V., 2003 The role of iron-reducing bacteria in the formation of magnetic properties of steppe soils Eurasian Soil Science 36 1085–1094.Google Scholar