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Nontronite particle aggregation induced by microbial Fe(III) reduction and exopolysaccharide production

Published online by Cambridge University Press:  01 January 2024

Deb P. Jaisi ,
Hailiang Dong ,
Jinwook Kim ,
Ziqi He  and
John P. Morton
Deb P. Jaisi
Affiliation:
Department of Geology, Miami University, Oxford, OH 45056, USA
Hailiang Dong*
Affiliation:
Department of Geology, Miami University, Oxford, OH 45056, USA
Jinwook Kim
Affiliation:
Naval Research Laboratory, NASA Stennis Space Center, MS 39529, USA
Ziqi He
Affiliation:
Department of Civil & Environmental Engineering and Geodetic Science, The Ohio State University, Columbus, OH 43210, USA
John P. Morton
Affiliation:
Department of Geology, Miami University, Oxford, OH 45056, USA
*
*E-mail address of corresponding author: dongh@muohio.edu
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Abstract

Clay particle aggregation affects a number of environmental processes, such as contaminant sorption/desorption, particle movement/deposition, and sediment structure and stability, yet factors that control clay aggregation are not well understood. This study was designed to investigate how microbial reduction of Fe(III) in clay structure, a common process in soils and sediments, affects clay-particle aggregation. Microbial Fe(III) reduction experiments were conducted with Shewanella putrefaciens CN32 in bicarbonate buffer with structural Fe (III) in nontronite as the sole electron acceptor, lactate as the sole electron donor, and AQDS as an electron shuttle. Four size fractions of nontronite (D5–D95 of 0.12–0.22 µm, 0.41–0.69 µm, 0.73–0.96 µm and 1.42–1.78 µm) were used to evaluate size-dependent aggregation kinetics. The extent of Fe(III) bioreduction and the amount of exopolysaccharide (EPS), a major biopolymer secreted by CN32 cells during Fe(III) bioreduction, were measured with chemical methods. Nontronite particle aggregation was determined by photon correlation spectroscopy and scanning electron microscopy. The maximum extent of Fe(III) bioreduction reached 36% and 24% for the smallest and the largest size fractions, respectively. Within the same time duration, the effective diameter, measured at 95% percentile (D95), increased by a factor of 43.7 and 7.7 for these two fractions, respectively. Because there was production of EPS by CN32 cells during Fe(III) reduction, it was difficult to assess the relative role of Fe(III) bioreduction and EPS bridging in particle aggregation. Thus, additional experiments were performed. Reduction of Fe(III) by dithionite was designed to examine the effect of Fe(III) reduction, and pure EPS isolated from CN32 cells was used to examine the effect of EPS. The data showed that both Fe(III) reduction and EPS were important in promoting clay mineral aggregation. In natural environments, the relative importance of these two factors may be dependent on local conditions. These results have important implications for understanding factors in controlling clay particle aggregation in natural environments.

Keywords

AggregationElectrophoretic MobilityEPSFe(III) ReductionNontroniteSEMShewanella Putrefaciens
Type
Research Article
Information
Clays and Clay Minerals , Volume 55 , Issue 1 , February 2007 , pp. 96 - 107
Copyright
Copyright © 2007, The Clay Minerals Society

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References

Arias, M. Barral, T. and Diaz-Fierros, F., (1995) Effects of iron and aluminum oxides on the colloidal and surface properties of kaolin Clays and Clay Minerals 43 406–416 10.1346/CCMN.1995.0430403.CrossRefGoogle Scholar
Boily, J. and Fein, J.B., (1998) Adsorption of Pb(II) and benzenecarboxylates onto corundum Chemical Geology 148 157–175 10.1016/S0009-2541(98)00027-8.CrossRefGoogle Scholar
Bradford, M.M., (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding Analytical Biochemistry 1/2 248–254 10.1016/0003-2697(76)90527-3.CrossRefGoogle Scholar
Bura, R. Chung, M. Liao, B. Finlayson, J. Lee, B.C. Droppo, I.G. Lepard, G.G. and Liss, S.N., (1998) Composition of extracellular polymeric substances in the activated sludge matrix Water Science and Technology 37 325–333 10.2166/wst.1998.0657.CrossRefGoogle Scholar
Cervini-Silva, J. Wu, J. Stucki, J.W. and Larson, R.A., (2000) Adsorption kinetics of pentachloroethane in iron-bearing smectites Clays and Clay Minerals 48 132–138 10.1346/CCMN.2000.0480116.CrossRefGoogle Scholar
Chenu, C. Pons, C.H. and Robert, M., (1979) Interaction of kaolinite and montmorillonite with neutral polysaccharide Proceedings of International Clay Conference Denver, Colorado The Clay Minerals Society.Google Scholar
Dachs, J. and Bayona, J.M., (1997) Langmuir-derived model for diffusion- and reaction-limited adsorption of organic compounds on fractal aggregates Environmental Science and Technology 31 2754–2760 10.1021/es961021p.CrossRefGoogle Scholar
de Boodt, M.F. (1990) Application of Polymeric Substances as Physical Soil Conditioners. Soil Colloids and their Association in Aggregates (de Boodt, M.F., Hays, M.H., Herbillon, A., editors). Plenum Press, New York pp. 517–556.Google Scholar
Dong, H., (2002) Significance of electrophoretic mobility distribution to bacterial transport Journal of Microbiological Methods 51 83–93 10.1016/S0167-7012(02)00062-3.CrossRefGoogle ScholarPubMed
Dong, H. Kostka, J.E. and Kim, J.W., (2003) Microscopic evidence for microbial dissolution of smectite Clays and Clay Minerals 51 502–512 10.1346/CCMN.2003.0510504.CrossRefGoogle Scholar
Droppo, I.G. and Irvine, K.N., (2002) Flocculation/aggregation of cohesive sediments in the urban continuum: Implications for storm water management Environmental Technology 23 27–41 10.1080/09593332508618433.CrossRefGoogle Scholar
Dubois, M. Gilles, K.A. Hamilton, J.K. Rebers, P.A. and Smith, F., (1956) Colorimetric method for determination of sugars and related substances Analytical Chemistry 28 350–356 10.1021/ac60111a017.CrossRefGoogle Scholar
Elimelech, M. Gregory, J. Jia, X. and Williams, R.A., (1995) Particle Deposition and Agglomeration: Measurement, Modeling and Simulation London Butterworth-Heinemann Ltd..Google Scholar
Follett, E.C., (1965) The retention of amorphous, colloidal ferric hydroxide by kaolinite Journal of Soil Science 16 334–341 10.1111/j.1365-2389.1965.tb01445.x.CrossRefGoogle 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.CrossRefGoogle Scholar
Fuller, L. Goh, T.B. Oscarson, D.W. and Biliaderis, C.G., (1995) Flocculation and coagulation of Ca- and Mg-saturated montmorillonite in the presence of a neutral polysaccharide Clays and Clay Minerals 43 533–539 10.1346/CCMN.1995.0430503.CrossRefGoogle Scholar
Gates, W.P. Wilkinson, H.T. and Stucki, J.W., (1993) Swelling properties of microbially reduced ferruginous smectite Clays and Clay Minerals 41 360–364 10.1346/CCMN.1993.0410312.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
Healy, T.W. and La Mer, V.K., (1964) Energetics of flocculation and redispersion by polymers Journal of Colloid and Interface Science 19 323–332 10.1016/0095-8522(64)90034-0.CrossRefGoogle Scholar
Hill, P.S., (1996) Sectional and discrete representations of floc breakage in agitated suspensions Deep Sea Research I 43 679–702 10.1016/0967-0637(96)00030-1.CrossRefGoogle Scholar
Hill, P.S. Voulgaris, G. and Trowbridge, J.H., (2001) Controls on floc size in a continental shelf bottom boundary layer Journal of Geophysical Research — Oceans 106 9543–9549 10.1029/2000JC900102.CrossRefGoogle Scholar
Hoggs, R., (1984) Collision efficiency factors for polymer flocculation Journal of Colloid and Interface Science 102 232–236 10.1016/0021-9797(84)90215-7.CrossRefGoogle Scholar
Hunter, R.J., (1981) Zeta Potential in Colloidal Science: Principles and Applications New York Academic Press.Google 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
Katoh, S. Danhara, T. Hart, W.K. and Wolde-Gabriel, G., (1999) Use of sodium polytungstate solution in the purification of volcanic glass shards for bulk chemical analysis Natural Human Acta 4 45–54.Google Scholar
Keeling, J.L. Raven, M.D. and Gates, W.P., (2000) Geology and characterization of two hydrothermal nontronites from weathered metamorphic rocks at the Uley graphite mine, South Australia Clays and Clay Minerals 48 537–548 10.1346/CCMN.2000.0480506.CrossRefGoogle 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
Kim, J.W. Furukawa, W. Dong, H. and Newell, S.W., (2005) The role of microbial Fe(III) reduction in clay flocculation Clays and Clay Minerals 53 572–579 10.1346/CCMN.2005.0530603.CrossRefGoogle Scholar
Korenevsky, A.A. Vinogradov, E. Gorby, Y. and Beveridge, T.J., (2002) Characterization of the lipopolysaccharides and capsules of Shewanella spp. Applied and Environmental Microbiology 68 4653–4657 10.1128/AEM.68.9.4653-4657.2002.CrossRefGoogle Scholar
Kostka, J.E. Stucki, J.W. Nealson, K.H. and Wu, J., (1996) Reduction of structural Fe(III) in smectite by a pure culture of Shewanella putrefaciens strain MR-1 Clays and Clay Minerals 44 522–529 10.1346/CCMN.1996.0440411.CrossRefGoogle 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.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 smectite clay minerals Geochimica et Cosmochimica Acta 63 3705–3713 10.1016/S0016-7037(99)00199-4.CrossRefGoogle Scholar
Kotylar, L.S. Sparks, B.D. and Schutte, R., (1996) Effect of salt on the flocculation behaviors of nano particles in oil sands fine tailings Clays and Clay Minerals 44 121–131 10.1346/CCMN.1996.0440111.CrossRefGoogle Scholar
Liao, B.Q. Allen, D.G. Droppo, I.G. Leppard, G.G. and Liss, S.N., (2001) Surface properties of sludge and their role in bioflocculation and settleability Water Research 35 339–350 10.1016/S0043-1354(00)00277-3.CrossRefGoogle ScholarPubMed
Lovley, D.R. Holmes, D.E. and Nevin, K.P., (2004) Dissimilatory Fe(III) and Mn(IV) reduction Advances in Microbial Physiology 49 219–286 10.1016/S0065-2911(04)49005-5.CrossRefGoogle ScholarPubMed
Malla, P.B. Robert, M. Douglass, L.A. Tessier, D. and Komarneni, S., (1993) Charge heterogeneity and nanostructure of 2:1 layer silicates by high resolution transmission electron microscopy Clays and Clay Minerals 41 412–422 10.1346/CCMN.1993.0410402.CrossRefGoogle Scholar
Moore, D.M. Reynolds, R.C. III, (1997) X-ray Diffraction and the Identification and Analysis of Clay Minerals New York Oxford University Press.Google Scholar
Moudgil, B.M. Shah, B.D. and Suto, H.S., (1987) Collision efficiency factors in polymer flocculation of fine particles Journal of Colloid and Interface Science 119 466–473 10.1016/0021-9797(87)90292-X.CrossRefGoogle Scholar
Nazarenko, E.L. Nadezhda, A. Komandrova, N.A. Gorshkova, R.P. Tomshich, S.V. Zubkov, V.A. Kilcoyne, M. and Savage, A.V., (2004) Structures of polysaccharides and oligosaccharides of some gram negative marine proteobacteria Carbohydrate Research 338 2449–2457 10.1016/j.carres.2003.06.004.CrossRefGoogle Scholar
Olness, A. and Clapp, C.E., (1975) Influence of polysaccharide structure on the dextran adsorption by montmorillonite Soil Biology and Biochemistry 7 113–118 10.1016/0038-0717(75)90008-5.CrossRefGoogle Scholar
O’Melia, C.R., (1980) Aquasols: the behavior of small particles in aquatic systems Environmental Science and Technology 14 1052–1060 10.1021/es60169a601.CrossRefGoogle Scholar
Orton, P.M. and Kineke, G.C., (2001) Comparing calculated and observed vertical suspended-sediment distributions from a Hudson River Estuary turbidity maximum Estuarine Coastal and Shelf Science 52 401–410 10.1006/ecss.2000.0747.CrossRefGoogle Scholar
Overbeek, J.T.G., (1988) Double layer interaction between spheres with unequal surface potentials Journal of the Chemical Society Faraday Transactions I 84 3079–3091 10.1039/f19888403079.CrossRefGoogle Scholar
Pignatello, J.J. and Xing, B., (1996) Mechanisms of slow sorption of organic chemicals to natural particles Environmental Science and Technology 30 1–5 10.1021/es940683g.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.K.G., (2006) Iron redox processes in clay minerals Handbook of Clay Science Amsterdam Elsevier Chapter 8.Google 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, J.W. Low, F.P. Roth, C.B. and Golden, D.C., (1984) Effects of oxidation state of octahedral iron on clay swelling Clays and Clay Minerals 32 357–362 10.1346/CCMN.1984.0320503.CrossRefGoogle Scholar
Tallon, R. Bressollier, P. and Urdaci, M.C., (2003) Isolation and characterization of two exoploysachharides produced by Lactobacillus plantarum EP 56 Research in Microbiology 154 705–712 10.1016/j.resmic.2003.09.006.CrossRefGoogle Scholar
Theng, B.K.G., (1979) Formation and Properties of Clay-Polymer Complexes Amsterdam Elsevier Scientific Publishing Co..Google Scholar
Theilen, F.R. Pecher, I.A. et al. ,Hoven, J.M. (1991) et al. , Assessment of shear strength of the sea bottom from shear wave velocity measurements on box cores and in situ Shear Wave in Marine Sediments Dordrecht, The Netherlands Kluwer Academic Publishers 67–74 10.1007/978-94-011-3568-9_8.CrossRefGoogle Scholar
Tolhurst, T.J. Gust, G. Paterson, D.M., Winterwerp, J.C. and Kranenburg, C., (2002) The influence of an extra cellular polymeric substance (EPS) on cohesive sediment stability Fine Sediment Dynamics in the Marine Environment Amsterdam Elsevier Science 409–425 10.1016/S1568-2692(02)80030-4.CrossRefGoogle Scholar
Walker, H.W. and Bob, M.M., (2001) Stability of particle flocs upon addition of natural organic matter under quiescent conditions Water Research 35 875–882 10.1016/S0043-1354(00)00333-X.CrossRefGoogle ScholarPubMed
Walker, S.L. Redman, J.A. and Elimelech, M., (2004) Role of cells surface lipopolysaccharides in Escherichia coli K12 adhesion and transport Langmuir 20 7736–7746 10.1021/la049511f.CrossRefGoogle ScholarPubMed
Xu, R., (1993) Methods to resolve mobility from electrophoretic laser light scattering measurement Langmuir 9 2955–2962 10.1021/la00035a037.CrossRefGoogle Scholar
Yuehena, H. Wei, S. Haipu, L. and Xu, Z., (2004) Role of macromolecules on kaolinite floatation Minerals Engineering 17 1017–1022 10.1016/j.mineng.2004.04.012.Google Scholar