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Reduction of Structural Fe(III) in Smectite by a Pure Culture of Shewanella Putrefaciens Strain MR-1

Published online by Cambridge University Press:  28 February 2024

Joel E. Kostka ,
Joseph W. Stucki ,
Kenneth H. Nealson  and
Jun Wu
Joel E. Kostka*
Affiliation:
Center for Great Lakes Studies, University of Wisconsin-Milwaukee, 600 E. Greenfield Avenue, Milwaukee, WI 53204
Joseph W. Stucki
Affiliation:
Department of Natural Resources and Environmental Sciences, University of Illinois, 1102 South Goodwin Avenue, Urbana, IL 61801
Kenneth H. Nealson
Affiliation:
Center for Great Lakes Studies, University of Wisconsin-Milwaukee, 600 E. Greenfield Avenue, Milwaukee, WI 53204
Jun Wu
Affiliation:
Department of Natural Resources and Environmental Sciences, University of Illinois, 1102 South Goodwin Avenue, Urbana, IL 61801
*
†Current Address: Skidaway Institute of Oceanography, 10 Ocean Science Circle, Savannah, GA 31411. joel@skio.peachnet.edu
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Abstract

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Shewanella putrefaciens is a species of metal-reducing bacteria with a versatile respiratory metabolism. This study reports that S. putrefaciens strain MR-1 rapidly reduces Fe(III) within smectite clay minerals. Up to 15% of the structural Fe within ferruginous smectite (sample SWa-1, Source Clays Repository of the Clay Minerals Society) was reduced by MR-1 in 4 h, and a range of 25% to 41% of structural Fe was reduced after 6 to 12 d during culture. Conditions for which smectite reduction was optimal, that is, pH 5 to 6, at 25 to 37 °C, are consistent with an enzymatic process and not with simple chemical reduction. Smectite reduction required viable cells, and was coupled to energy generation and carbon metabolism for MR-1 cultures with smectite added as the sole electron acceptor. Iron(III) reduction catalyzed by MR-1 was inhibited under aerobic conditions, and under anaerobic conditions it was inhibited by the addition of nitrate as an alternate electron acceptor or by the metabolic inhibitors tetrachlorosali-cylanilide (TCS) or quinacrine hydrochloride. Genetic mutants of MR-1 deficient in anaerobic respiration reduced significantly less structural Fe than wild-type cells. In a minimal medium with formate or lactate as the electron donor, more than three times the amount of smectite was reduced over no-carbon controls. These data point to at least one mechanism that may be responsible for the microbial reduction of clay minerals within soils, namely, anaerobic respiration, and indicate that pure cultures of MR-1 provide an effective model system for soil scientists and mineralogists interested in clay reduction. Given the ubiquitous distribution and versatile metabolism of MR-1, these studies may have further implications for bioremediation and water quality in soils and sediments.

Keywords

ClayFe(III) reductionMetal-reducing bacteriaSedimentsSmectiteSoils
Type
Research Article
Information
Clays and Clay Minerals , Volume 44 , Issue 4 , August 1996 , pp. 522 - 529
Copyright
Copyright © 1996, The Clay Minerals Society

References

Amonette, J.E., Stucki, J.W., Khan, F., Gan, H. and Scott, A.D.. 1994. Quantitative oxidation state analysis of soils. In: Amonette, J.E., Zelazny, L.W., editors. Quantitative methods in soil mineralogy. Soil Sci Soc Am Miscellaneous Publication. Madison, WI: Soil Sci Soc Am p 83–113.CrossRefGoogle Scholar
Arnold, R., DiChristina, T. and Hoffman, M.. 1988. Reductive dissolution of Fe(III) oxides by Pseudomonas sp. 200. Biotechnol Bioeng 32: 1081–1096.CrossRefGoogle ScholarPubMed
Brettar, I. and Hoefle, M.. 1993. Nitrous oxide producing heterotrophic bacteria from the water column of the central Baltic: abundance and molecular identification. Mar Ecol Prog Ser 94: 253–265.CrossRefGoogle Scholar
Burdige, D.J.. 1993. The biogeochemistry of manganese and iron reduction in marine sediments. Earth Sci Rev 35: 249–284.CrossRefGoogle Scholar
Canfield, D.E., Thamdrup, B. and Hansen, J.W.. 1993. The anaerobic degradation of organic matter in Danish coastal sediments: iron reduction, manganese reduction, and sulfate reduction. Geochim Cosmochim Acta 57: 3867.CrossRefGoogle ScholarPubMed
Chapelle, F.H. and Lovley, D.R.. 1992. Competitive exclusion of sulfate reduction by Fe3+-reducing bacteria: a mechanism for producing discrete zones of high-iron ground water. Ground Water 30: 29–36.CrossRefGoogle Scholar
Chen, S.A., Low, P.F. and Roth, C.B.. 1987. Relation between potassium fixation and the oxidation state of octahedral iron. Soil Sci Soc Am J 51: 82–86.CrossRefGoogle Scholar
Gate, W.P., Wilkinson, H.T. and Stucki, J.W.. 1993. Swelling properties of microbially reduced ferruginous smectite. Clays & Clay Miner 41: 360–364.CrossRefGoogle Scholar
Goodman, B.A., Russell, J.D., Fraser, A.R. and Woodhams, F.W.D.. 1976. A Mössbauer and I.R. spectroscopic study of the structure of nontronite. Clays & Clay Miner 24: 53–59.CrossRefGoogle Scholar
Isphording, W.C.. 1975. Primary nontronite from Venezuelan Guyana. Am Miner 60: 840–848.Google Scholar
Jenne, E.A.. 1977. Trace element sorption by sediments and soil sites and processes. In: Chappel, W., Petersen, K., editors. Symposium on molybdenum in the environment. New York: Marcel Dekker. p 425–453.Google Scholar
Keller, M.D., Bellows, W.K. and Guillard, R.R.L.. 1988. Microwave treatment for sterilization of phytoplankton culture media. J Exp Mar Biol Ecol 117: 279–283.CrossRefGoogle Scholar
Komadel, P. and Stucki, J.W.. 1988. Quantitative assay of minerals for Fe2+ and Fe3+ using 1,10-phenanthroline: III. A rapid photochemical method. Clays & Clay Miner 36: 379–381.CrossRefGoogle Scholar
Kostka, J.E. and Luther, G.W. III. 1994. Partitioning and speciation of solid phase iron in saltmarsh sediments. Geochim Cosmochim Acta 58: 1701–1710.CrossRefGoogle Scholar
Kostka, J.E., Luther, G.W. III and Nealson, K.H.. 1995. Chemical and biological reduction of Mn3+-pyrophosphate complexes: potential importance of dissolved Mn3+ as an environmental oxidant. Geochim Cosmochim Acta 59: 885–894.Google Scholar
Kostka, J.E. and Nealson, K.H.. 1995. Dissolution and reduction of magnetite by bacteria. Environ Sci Technol 29: 2535–2540.CrossRefGoogle ScholarPubMed
Lamb, C.A. and Grady, R.I.. 1963. A study of soil heaving with frost. Ohio Farm & Home Res 48: 43–47.Google Scholar
Lear, P.R. and Stucki, J.W.. 1989. Effects of iron oxidation state on the specific surface area of nontronite. Clays & Clay Miner 37: 547–552.CrossRefGoogle Scholar
Lovley, D.R.. 1991. Dissimilatory Fe3+ and Mn4+ reduction. Microbiol Rev 55: 259–287.CrossRefGoogle Scholar
Lovley, D.R.. 1993a. Anaerobes into heavy metal: dissimilatory metal reduction in anoxic environments. Trends in Ecol & Evol 8: 213–217.CrossRefGoogle ScholarPubMed
Lovley, D.R.. 1993b. Dissimilatory metal reduction. Ann Rev Microbiol 47: 263–290.CrossRefGoogle ScholarPubMed
Lovley, D.R., Chapelle, F.H. and Phillips, E.J.P.. 1990. Fe(III) reducing bacteria in deeply buried sediments of the Atlantic Coastal Plain. Geology 18: 954–957.2.3.CO;2>CrossRefGoogle Scholar
Myers, C.R. and Myers, J.M.. 1992. Localization of cytochromes to the outer membrane of anaerobically grown Shewanella putrefaciens MR-1. J Bacteriol 174: 3429–3438.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.CrossRefGoogle ScholarPubMed
Nealson, K.H. and Myers, C.R.. 1992. Microbial reduction of manganese and iron: new approaches to carbon cycling. Appl Environ Microbiol 58: 439–443.CrossRefGoogle ScholarPubMed
Nealson, K.H. and Saffarini, D.A.. 1994. Iron and manganese in anaerobic respiration: environmental significance, physiology, and regulation. Ann Rev Microbiol 48: 311–343.CrossRefGoogle ScholarPubMed
Nealson, K.H., Myers, C.R. and Wimpee, B.B.. 1991. Isolation and identification of manganese-reducing bacteria and estimates of microbial Mn(IV)-reducing potential in the Black Sea. Deep-Sea Res 38: S907–S920.CrossRefGoogle Scholar
Nealson, K.H., Saffarini, D.A. and Moser, D.. 1995. Anaerobic respiration of Shewanella putrefaciens: potential use of solid electron acceptors for pollutant removal and bioremediation in anoxic environments. In: DeLuca, M., editor. Bioremediation of Contaminants in Soils and Sediments. New Brunswick, NJ: Rutgers University Press (In press.)Google Scholar
Obuekwe, C. and Westlake, D.W.. 1982. Effects of medium composition on cell pigmentation, cytochrome content, and ferric iron reduction in a Pseudomonas sp. isolated from crude oil. Can J Microbiol 28: 989–992.CrossRefGoogle Scholar
Petrovskis, E.A., Vogel, T.M. and Adriaens, P.. 1994. Effects of electron acceptors and donors on transformation of tetrachlo-romethane by Shewanella putrefaciens MR-1. FEMS Microbiol Lett 121: 357–364.CrossRefGoogle ScholarPubMed
Ponnamperuma, F.N., Tianco, E.M. and Loy, T.. 1967. Redox equilibria in flooded soils: 1. The iron hydroxide systems. Soil Sci 103: 374–382.CrossRefGoogle Scholar
Saffarini, D.A., DiChristina, T.J., Bermudes, D. and Nealson, K.H.. 1994. Anaerobic respiration of Shewanella putrefaciens requires both chromosomal and plasmid-borne genes. FEMS Microbio Lett 119: 271–278.CrossRefGoogle Scholar
Schlautman, M.A. and Morgan, J.J.. 1994. Sorption of perylene on a nonporous inorganic silica surface: effects of aqueous chemistry on sorption rates. Environ Sci Technol 28: 2184–2190.CrossRefGoogle ScholarPubMed
Scott, J.H. and Nealson, K.H.. 1994. Anaerobic methylotrophy in a facultative anaerobe: Shewanella. J Bacteriol 176: 3408–3411.CrossRefGoogle Scholar
Shen, S. and Stucki, J.W.. 1994. Effects of iron oxidation state on the fate and behavior of potassium in soils. In: Havlin, J.L., Jacobsen, J., Fixen, P., Hergert, G., editors. Soil testing: Prospects for improving nutrient recommendations. SSSA Special Publication 40. Madison, WI: Soil Sci Soc Am p 173–185.Google Scholar
Stookey, L.L.. 1970. Ferrozine-a new spectrophotometric reagent for iron. Anal Chem 42: 779–781.CrossRefGoogle Scholar
Stucki, J.W.. 1981. The quantitative assay of minerals for Fe3+ and Fe3+ using 1,10-phenanthroline: II. A photochemical method. Soil Sci Soc Am J 45: 638–641.CrossRefGoogle Scholar
Stucki, J.W.. 1988. Structural iron in smectites. In: Stucki, J.W., Goodman, B.A., Schwertmann, U., editors. Iron in soils and clay minerals. Dordrecht, The Netherlands: D. Reidel p 625–675.CrossRefGoogle Scholar
Stucki, J.W. and Lear, P.R.. 1990. Variable oxidation states of iron in the crystal structure of smectite clay minerals. In: Coyne, L.M., Blake, D., McKeever, S., editors. Structures and active sites of minerals. Washington, D.C.: Am Chem Soc p 330–358.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 & Clay Miner 39: 137–143.CrossRefGoogle Scholar
Stucki, J.W., Golden, D.C. and Roth, C.B.. 1984a. Preparation and handling of dithionite reduced smectite suspensions. Clays & Clay Miner 32: 191–197.CrossRefGoogle Scholar
Stucki, J.W., Low, P.F., Roth, C.B. and Golden, D.C.. 1984b. Effect of iron oxidation state on clay swelling. Clays & Clay Miner 32: 357–362.CrossRefGoogle Scholar
Stucki, J.W., Komadel, P. and Wilkinson, H.T.. 1987. Microbial reduction of structural Fe3+ in smectites. Soil Sci Soc Am J 51: 1663–1665.CrossRefGoogle Scholar
Wu, J., Roth, C.B. and Low, P.F.. 1988. Biological reduction of structural Fe in sodium-nontronite. Soil Sci Soc Am J 52: 295–296.CrossRefGoogle Scholar