AEM Accepts, published online ahead of print on 2 November 2007

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Appl. Environ. Microbiol. doi:10.1128/AEM.01580-07
Copyright (c) 2007, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved.

Growth of Thermophilic and Hyperthermophilic Fe(III)-Reducing Microorganisms on a Ferruginous Smectite as the Sole Electron Acceptor

Kazem Kashefi^*, Evgenya S. Shelobolina, W. Crawford Elliott, and Derek R. Lovley

Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824; Department of Geology and Geophysics, University of Wisconsin, Madison, WI 53706; Department of Geosciences, Georgia State University, P.O. Box 4105, Atlanta, GA 30302-4105; Department of Microbiology, University of Massachusetts, Amherst, MA 01003

^* To whom correspondence should be addressed. Email: kashefi{at}msu.edu.

Recent studies have suggested that the structural Fe(III) within phyllosilicate minerals, including smectite and illite, is an important electron acceptor for Fe(III)-reducing microorganisms in sedimentary environments at moderate temperatures. The reduction of structural Fe(III) by thermophiles, however, has not previously been described. A wide range of thermophilic and hyperthermophilic Archaea and Bacteria from marine and freshwater environments that are known to reduce poorly crystalline Fe(III) oxides were tested for their ability to reduce structural (octahedrally coordinated) Fe(III) in smectite (SWa-1) as the sole electron acceptor. Two out of the ten organisms tested, Geoglobus ahangari and Geothermobacterium ferrireducens, were not able to conserve energy to support growth by reduction of Fe(III) in SWa-1 despite the fact that both organisms were originally isolated with solid phase Fe(III) as the electron acceptor. The other organisms tested were able to grow on SWa-1 and reduced 6.3 to 15.1 % of the Fe(III). This is 20-50% less than the reported amounts of Fe(III) reduced in the same smectite (SWa-1), by mesophilic Fe(III) reducers. Two organisms, Geothermobacter ehrlichii and archaeal strain 140, produced copious amounts of an exopolysaccharide material, which may have played an active role in the dissolution of the structural iron in SWa-1 smectite. The reduction of structural Fe(III) in SWa-1 by archaeal strain 140 was studied in detail. Microbial Fe(III) reduction was accompanied by an increase in interlayer and octahedral charges and some incorporation of potassium and magnesium into the smectite structure. However, these changes in the major element chemistry of SWa-1 smectite did not result in the formation of an illite-like structure, as reported for a mesophilic Fe(III) reducer. These results suggest that thermophilic Fe(III)-reducing organisms differ in their ability to reduce and solubilize structural Fe(III) in SWa-1 smectite and that SWa-1 is not easily transformed to illite by these organisms.

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