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Bacteria-clay interaction: Structural changes in smectite induced during biofilm formation

Published online by Cambridge University Press:  01 January 2024

Alexandra Alimova ,
A. Katz ,
Nicholas Steiner ,
Elizabeth Rudolph ,
Hui Wei ,
Jeffrey C. Steiner  and
Paul Gottlieb
Alexandra Alimova
Affiliation:
Institute for Ultrafast Spectroscopy and Lasers, The City College of New York, 160 Convent Ave, New York, NY 10031, USA
A. Katz
Affiliation:
Institute for Ultrafast Spectroscopy and Lasers, The City College of New York, 160 Convent Ave, New York, NY 10031, USA
Nicholas Steiner
Affiliation:
Department of Earth and Atmospheric Sciences, The City College of New York, 160 Convent Ave, New York, NY 10031, USA
Elizabeth Rudolph
Affiliation:
Department of Earth and Atmospheric Sciences, The City College of New York, 160 Convent Ave, New York, NY 10031, USA
Hui Wei
Affiliation:
Sophie Davis School of Biomedical Education, The City College of New York, 160 Convent Ave, New York, NY 10031, USA
Jeffrey C. Steiner
Affiliation:
Department of Earth and Atmospheric Sciences, The City College of New York, 160 Convent Ave, New York, NY 10031, USA
Paul Gottlieb*
Affiliation:
Sophie Davis School of Biomedical Education, The City College of New York, 160 Convent Ave, New York, NY 10031, USA
*
* E-mail address of corresponding author: pgottl@med.cuny.edu
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Abstract

Bacteria play an important role in determining the properties and behavior of clay minerals in natural environments and such interactions have great potential for creating stable biofilms and carbon storage sites in soils, but our knowledge of these interactions are far from complete. The purpose of this study was to understand better the effects of bacteria-generated biofilms on clay interlayer expansion. Mixtures of a colloidal, 2-water hectorite clay and Pseudomonas syringae in a minimal media suspension evolve into a polysaccharide-rich biofilm aggregate in time-series experiments lasting up to 1 week. X-ray diffraction analysis reveals that upon aggregation, the clay undergoes an initial interlayer contraction. Short-duration experiments, up to 72 h, result in a decrease in the d001 value from 1.50 to 1.26 nm. The initial interlayer contraction is followed in long-duration (up to 1 week) experiments by an expansion of the d001 value of 1.84 nm. The expansion is probably a result of large, biofilm-produced, polymeric molecules being emplaced in the interlayer site. The resultant organo-clay could provide a possible storage medium for carbon in a microbial colony setting.

Keywords

Bacteria-clay InteractionBiofilmsClay InterlayerSmectitePolysaccharidesPseudomonas syringae
Type
Article
Information
Clays and Clay Minerals , Volume 57 , Issue 2 , April 2009 , pp. 205 - 212
Copyright
Copyright © The Clay Minerals Society 2009

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References

Alimova, A. Roberts, M. Katz, A. Rudolph, E. Steiner, J.C. Alfano, R.R. and Gottlieb, P., 2006 Effects of smectite clay on biofilm formation by microorganisms Biofilms 3 47–54 10.1017/S1479050507002128.CrossRefGoogle Scholar
Amellal, N. Burtin, G. Bartoli, F. and Heulin, T., 1998 Colonization of wheat roots by an exopolysaccharide-producing pantoea agglomerans strain and its effect on rhizosphere soil aggregation Applied and Environmental Microbiology 64 3740–3747.CrossRefGoogle ScholarPubMed
Anderson, J.U., 1961 An improved pretreatment for mineralogical analysis of samples containing organic matter Clays and Clay Minerals 10 380–388 10.1346/CCMN.1961.0100134.CrossRefGoogle Scholar
Baumgartner, L.K. Reid, R.P. Dupraz, C. Decho, A.W. Buckley, D.H. Spear, J.R. Przekop, P.K.M. and Visscher, P.T., 2006 Sulfate reducing bacteria in microbial mats: Changing paradigms, new discoveries Sedimentary Geology 185 131–145 10.1016/j.sedgeo.2005.12.008.CrossRefGoogle Scholar
Bitton, G. Henis, Y. and Lahav, N., 1972 Effect of several clay minerals and humic acid on the survival of Klebsiella aerogenes exposed to ultraviolet irradiation Applied Microbiology 23 870–874.CrossRefGoogle ScholarPubMed
Bloemberg, G.V. and Lugtenberg, B.J.J., 2004 Bacterial Biofilms on Plants: Relevance and Phenotypic Aspects Washington, D.C. ASM Press.Google Scholar
Bulson, P.C. Johnstone, D.L. Gibbons, H.L. and Funk, W.H., 1984 Removal and inactivation of bacteria during alum treatment of a lake Applied and Environmental Microbiology 48 425–430.CrossRefGoogle ScholarPubMed
Burton, G.A. Jr. Gunnison, D. and Lanza, G.R., 1987 Survival of pathogenic bacteria in various freshwater sediments Applied and Environmental Microbiology 53 633–638.CrossRefGoogle ScholarPubMed
Chafetz, H.S. and Buczynski, C., 1992 Bacterially induced lithification of microbial mats Palaios 7 277–293 10.2307/3514973.CrossRefGoogle Scholar
Costerton, J.W. Cheng, K.J. Geesey, G.G. Ladd, T.I. Nickel, J.C. Dasgupta, M. and Marrie, T.J., 1987 Bacterial biofilms in nature and disease Annual Review of Microbiology 41 435–464 10.1146/annurev.mi.41.100187.002251.CrossRefGoogle ScholarPubMed
Costerton, J.W. Lewandowski, Z. Caldwell, D.E. Korber, D.R. and Lappin-Scott, H.M., 1995 Microbial biofilms Annual Review of Microbiology 49 711–745 10.1146/annurev.mi.49.100195.003431.CrossRefGoogle ScholarPubMed
Curry, K.J. Bennett, R.H. Mayer, L.M. Curry, A. Abril, M. Biesiot, P.M. and Hulbert, M.H., 2007 Direct visualization of clay microfabric signatures driving organic matter preservation in fine-grained sediment Geochimica et Cosmochimica Acta 71 1709–1720 10.1016/j.gca.2007.01.009.CrossRefGoogle Scholar
Darder, M. and Ruiz-Hitzky, E., 2005 Caramel-clay nanocomposites Journal of Materials Chemistry 15 3913–3918 10.1039/b505958e.CrossRefGoogle Scholar
Davey, M.E. and O’toole, G.A., 2000 Microbial biofilms: from ecology to molecular genetics Microbiology and Molecular Biology Reviews 64 847–867 10.1128/MMBR.64.4.847-867.2000.CrossRefGoogle ScholarPubMed
Difco, 1953 Manual of Dehydrated Culture Media and Reagents for Microbiological and Clinical Laboratory Procedures Laboratories Detroit, USA Difco Laboratories.Google Scholar
Dorioz, J.M. Robert, M. and Chenu, C., 1993 The role of roots, fungi and bacteria on clay particle organization. An experimental approach Geoderma 56 179–194 10.1016/0016-7061(93)90109-X.CrossRefGoogle Scholar
Dupraz, C. and Visscher, P.T., 2005 Microbial lithification in marine stromatolites and hypersaline mats Trends in Microbiology 13 429–438 10.1016/j.tim.2005.07.008.CrossRefGoogle ScholarPubMed
Fortin, D. and Beveridge, T.J., 1997 Microbial sulfate reduction within sulfidic mine tailings: formation of diagenetic Fe-sulfides Geomicrobiology Journal 14 1–21 10.1080/01490459709378030.CrossRefGoogle Scholar
Fortin, D. Ferris, F.G. Beveridge, T.J., Banfield, J.F. and Nealson, K.H., 1997 Surface-mediated mineral development by bacteria Geomicrobiology: Interactions Between Microbes and Minerals Washington, D.C. Mineralogical Society of America 161–180 10.1515/9781501509247-007.CrossRefGoogle Scholar
Gerbersdorf, S.U. Jancke, T. Westrich, B. and Paterson, D.M., 2008 Microbial stabilization of riverine sediments by extracellular polymeric substances Geobiology 6 57–69.CrossRefGoogle ScholarPubMed
Griffin, D. Garrison, V. Herman, J. and Shinn, E., 2001 African desert dust in the Caribbean atmosphere: Microbiology and public health Aerobiologia 17 203–213 10.1023/A:1011868218901.CrossRefGoogle Scholar
Griffin, D.W. Kellogg, C.A. Garrison, V.H. Lisle, J.T. Borden, T.C. and Shinn, E.A., 2003 Atmospheric microbiology in the northern Caribbean during African dust events Aerobiologia 19 143–157 10.1023/B:AERO.0000006530.32845.8d.CrossRefGoogle Scholar
Hedges, J.I. and Oades, J.M., 1997 Comparative organic geochemistries of soils and marine sediments Organic Geochemistry 27 319–361 10.1016/S0146-6380(97)00056-9.CrossRefGoogle Scholar
Jackson, G.A. and Burd, A.B., 1998 Aggregation in the marine environment Environmental Science and Technology 32 2805–2814 10.1021/es980251w.CrossRefGoogle Scholar
Konhauser, K.O. Schultze-Lam, S. Ferris, F.G. Fyfe, W.S. Longstaffe, F.J. and Beveridge, T.J., 1994 Mineral precipitation by epilithic biofilms in the Speed River, Ontario, Canada Applied and Environmental Microbiology 60 549–553.CrossRefGoogle ScholarPubMed
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
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
Lee, A.K. and Newman, D.K., 2003 Microbial iron respiration: impacts on corrosion processes Applied Microbiology and Biotechnology 62 134–139 10.1007/s00253-003-1314-7.CrossRefGoogle ScholarPubMed
Little, B.J. Wagner, P.A. and Mansfeld, F., 1991 Microbiologically influenced corrosion of metals and alloys International Materials Reviews 36 253–272 10.1179/imr.1991.36.1.253.CrossRefGoogle Scholar
Little, B.J. Wagner, P.A. Lewandowski, Z., Banfield, J.F. and Nealson, K.H., 1997 Spatial relationships between bacteria and mineral surfaces Geomicrobiology — Interactions Between Microbes and Minerals Washington D.C. Mineralogical Society of America 123–155 10.1515/9781501509247-006.CrossRefGoogle Scholar
McCarthy, M., 2001 Dust clouds implicated in spread of infection The Lancet 358 478 10.1016/S0140-6736(01)05677-X.CrossRefGoogle ScholarPubMed
Mikutta, R. Kleber, M. Kaiser, K. and Jahn, R., 2005 Review: organic matter removal from soils using hydrogen peroxide, sodium hypochlorite, and disodium peroxodisulfate Soil Science Society of America Journal 69 120–135 10.2136/sssaj2005.0120.CrossRefGoogle Scholar
Moore, D. and Reynolds, R.C. Jr., 1997 X-ray Diffraction and the Identification and Analysis of Clay Minerals New York Oxford University Press.Google Scholar
O’Toole, G.A. and Kolter, R., 1998 Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development Molecular Microbiology 30 295–304 10.1046/j.1365-2958.1998.01062.x.CrossRefGoogle ScholarPubMed
Pina, R.G. and Cervantes, C., 1996 Microbial interactions with aluminium Biometals 9 311–316 10.1007/BF00817932.CrossRefGoogle ScholarPubMed
Pope, D. Duquette, D. Wayner, P.C. and Johannes, A.H., 1984 Microbiologically Influenced Corrosion: A State of the Art Review Columbus, OH Materials Technology Institute of Chemical Process Industries.Google Scholar
Ransom, B. Kim, D. Kastner, M. and Wainwright, S., 1998 Organic matter preservation on continental slopes: importance of mineralogy and surface area Geochimica et Cosmochimica Acta 62 1329–1345 10.1016/S0016-7037(98)00050-7.CrossRefGoogle Scholar
Ransom, B. Bennett, R.H. Baerwald, R. Hulbert, M.H. and Burkett, P.-J., 1999 In situ conditions and interactions between microbes and minerals in fine-grained marine sediments; a TEM microfabric perspective American Mineralogist 84 183–192 10.2138/am-1999-1-220.CrossRefGoogle Scholar
Reid, R.P. Visscher, P.T. Decho, A.W. Stolz, J.F. Bebout, B.M. Dupraz, C. Macintyre, I.G. Paerl, H.W. Pinckney, J.L. Prufert-Bebout, L. Steppe, T.F. and Desmarais, D.J., 2000 The role of microbes in accretion, lamination and early lithification of modern marine stromatolites Nature 406 989–992 10.1038/35023158.CrossRefGoogle ScholarPubMed
Roberts, J.A., 2004 Inhibition and enhancement of microbial surface colonization: the role of silicate composition Chemical Geology 212 313–327 10.1016/j.chemgeo.2004.08.021.CrossRefGoogle Scholar
Ruiz-Conde, A. Ruiz-Amil, A. Perez-Rodriguez, J.L. Sanchez-Soto, P.J. and De La Cruz, F.A., 1997 Interaction of vermiculite with aliphatic amides (formamide, acetamide and propionamide): formation and study of interstratified phases in the transformation of Mg- to NH4-vermiculite Clays and Clay Minerals 45 311–326 10.1346/CCMN.1997.0450302.CrossRefGoogle Scholar
Scappini, F. Casadei, F. Zamboni, R. Franchi, M. Gallori, E. and Monti, S., 2004 Protective effect of clay minerals on adsorbed nucleic acid against UV radiation: possible role in the origin of life International Journal of Astrobiology 3 17–19 10.1017/S147355040400179X.CrossRefGoogle Scholar
Stal, L.J., 2003 Microphytobenthos, their extracellular polymeric substances, and the morphogenesis of intertidal sediments Geomicrobiology Journal 20 463–478 10.1080/713851126.CrossRefGoogle Scholar
Stucki, J.W. and Kostka, J.E., 2006 Microbial reduction of iron in smectite Comptes Rendus Geosciences 338 468–475 10.1016/j.crte.2006.04.010.CrossRefGoogle Scholar
Stucki, J.W. Komadel, P. and Wilkinson, H.T., 1987 Microbial reduction of structural iron(III) in smectites Soil Science Society of America Journal 51 1663–1665 10.2136/sssaj1987.03615995005100060047x.CrossRefGoogle Scholar
Stucki, J.W. Jun, W. Gan, H. Komadel, P. and Banin, A., 2000 Effects of iron oxidation state and organic cations on dioctahedral smectite hydration Clays and Clay Minerals 48 290–298 10.1346/CCMN.2000.0480216.CrossRefGoogle Scholar
Sutherland, T.F. Amos, C.L. and Grant, J., 1998 The effect of buoyant biofilms on the erodibility of sublittoral sediments of a temperate microtidal estuary Limnology and Oceanography 43 225–235 10.4319/lo.1998.43.2.0225.CrossRefGoogle Scholar
Taylor, D.A., 2002 DUST in the WIND Environmental Health Perspectives 110 A80–87.CrossRefGoogle ScholarPubMed
Ueshima, M. and Tazaki, K., 2001 Possible role of microbial polysaccharides in nontronite formation Clays and Clay Minerals 49 292–299 10.1346/CCMN.2001.0490403.CrossRefGoogle Scholar
Vieira, M.J. Pacheco, A.P. Pinho, I.A. and Melo, L.F., 2001 The effect of clay particles on the activity of suspended autotrophic nitrifying bacteria and on the performance of an air-lift reactor Environmental Technology 22 123–135 10.1080/09593332208618298.CrossRefGoogle ScholarPubMed
Zhang, S.-Y. Wang, J.-S. Jiang, Z.-C. and Chen, M.-X., 2000 Nitrite accumulation in an Attapulgas clay biofilm reactor by fulvic acids Bioresource Technology 73 91–93 10.1016/S0960-8524(99)00133-9.CrossRefGoogle Scholar