University of Massachusetts Amherst From the SelectedWorks of Derek Lovley November 2, 2007 Growth of Thermophilic and Hyperthermophilic Fe(III)-Reducing Microorganisms on a Ferruginous Smectite as the Sole Electron Acceptor Derek Lovley, University of Massachusetts - Amherst Kazem Kashefi Evgenya S Shelobolina W. Crawford Elliott Available at: https://works.bepress.com/derek_lovley/100/ 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 Downloaded from Appl. Environ. Microbiol. 2008, 74(1):251. DOI: 10.1128/AEM.01580-07. Published Ahead of Print 2 November 2007. Updated information and services can be found at: http://aem.asm.org/ http://aem.asm.org/content/74/1/251 These include: REFERENCES This article cites 53 articles, 28 of which can be accessed free at: http://aem.asm.org/content/74/1/251#ref-list-1 on March 14, 2013 by Univ of Massachusetts Amherst CONTENT ALERTS Receive: RSS Feeds, eTOCs, free email alerts (when new articles cite this article), more» Information about commercial reprint orders: http://journals.asm.org/site/misc/reprints.xhtml To subscribe to to another ASM Journal go to: http://journals.asm.org/site/subscriptions/ APPLIED AND ENVIRONMENTAL MICROBIOLOGY, Jan. 2008, p. 251–258 Vol. 74, No. 1 0099-2240/08/$08.00ϩ0 doi:10.1128/AEM.01580-07 Copyright © 2008, American Society for Microbiology. All Rights Reserved. Growth of Thermophilic and Hyperthermophilic Fe(III)-Reducing Microorganisms on a Ferruginous Smectite as the Sole Electron Acceptorᰔ Kazem Kashefi,1* Evgenya S. Shelobolina,2 W. Crawford Elliott,3 and Derek R. Lovley4 Downloaded from Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan 488241; Department of Geology and Geophysics, University of Wisconsin, Madison, Wisconsin 537062; Department of Geosciences, Georgia State University, P.O. Box 4105, Atlanta, Georgia 30302-41053; and Department of Microbiology, University of Massachusetts, Amherst, Massachusetts 010034 Received 11 July 2007/Accepted 26 October 2007 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 http://aem.asm.org/ 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 10 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 to 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 on March 14, 2013 by Univ of Massachusetts Amherst 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. Dissimilatory Fe(III) reduction has an important influence on (hereinafter SWa-1) (28, 51). The addition of both ferrihydrite the geochemistry of both moderate-temperature (8 to 42°C) and and SWa-1 (31, 33, 46) to methanogenic sediments promotes hot (42 to 121°C) environments (27, 28). In freshwater and ma- the activity of indigenous Fe(III)-reducing microorganisms rine sediments and submerged soils, mesophilic Fe(III)-reducing and switches the terminal electron-accepting process in these organisms are responsible for the anaerobic oxidation of a sub- sediments from methane production to Fe(III) reduction. stantial portion of organic carbon and often play an important Fe(III) hydroxides have been the focus of most studies of role in the bioremediation of organic and metal contaminants at microbial Fe(III) reduction (26), and the importance of moderate temperatures (26). In hot anaerobic environments, Fe(III)-bearing phyllosilicates for Fe(III) respiration has only such as the deep continental subsurface and in marine and ter- recently been recognized (28, 51). Thus far, structural Fe(III) restrial hydrothermal zones, hyperthermophilic microorganisms reduction has been tested only in mesophilic microorganisms can oxidize hydrogen and metabolize short- and long-chain or- (4, 6, 7, 21, 23, 25, 45, 47, 50, 58). ganic acids and aromatic compounds to carbon dioxide by using Here, we report on the potential for the microbial reduction Fe(III) as the electron acceptor (12, 14, 18, 27, 53, 54). All hy- of structural Fe(III) in SWa-1 by various thermophilic and perthermophiles available in pure culture that have been tested to hyperthermophilic Archaea and Bacteria, originally isolated date can reduce Fe(III), suggesting that the ability to reduce with Fe(III) oxide as the terminal electron acceptor, from a Fe(III) is a highly conserved characteristic of hyperthermophilic variety of hot environments. The results suggest that phyllo- microorganisms (12–18, 27, 29, 53, 56). silicates can serve as an electron acceptor for the growth of Recent studies suggest that the two main sources of Fe(III) Fe(III)-reducing microorganisms in sedimentary environments in sedimentary environments are ferrihydrite and Fe(III)-bear- at elevated temperatures. However, the conversion of smectite ing phyllosilicates including the iron-rich smectite SWa-1 to illite as previously reported for the mesophilic Shewanella oneidensis (19) was not observed. * Corresponding author. Mailing address: Microbiology and Molec- ular Genetics, 6191 Biomedical and Physical Sciences Bldg., Michigan MATERIALS AND METHODS State University, East Lansing, MI 48824. Phone: (517) 355-6463, ext. Sources of organisms and culture conditions. The microbial strains used in 1608. Fax: (517) 353-8957. E-mail: kashefi@msu.edu. this study are listed in Table 1. They were originally enriched and isolated with ᰔ Published ahead of print on 2 November 2007. poorly crystalline Fe(III) oxide (30) as the sole electron acceptor, from a wide 251 252 KASHEFI ET AL. APPL.ENVIRON.MICROBIOL. TABLE 1. Organisms used in this study Strain (other Freshwater (FW) Name Lineage Source Reference designations) or marine (M) FW1a (JCM 12379 ϭ Geothermobacterium Bacteria, Thermodesulfobacteria, FW Sediment from Obsidian 15 ATCC BAA-426) ferrireducens Geothermobacterium Pool in Yellowstone National Park, WY SS015 (JCM 12418 ϭ Geothermobacter Bacteria, Deltaproteobacteria, M Diffuse-flow vent fluid 13 ATCC BAA-635 ϭ ehrlichii Geobacteraceae, from the deep-sea DSM 15274) Geothermobacter hydrothermal chimney called Bag City in the Downloaded from Pacific Ocean (46°N, 130°W) 234 (JCM 12378 ϭ Geoglobus ahangari Archaea, Euryarchaeota, M Hydrothermal chimney at 18 ATCC BAA-426) Archaeoglobaceae, Geoglobus Guaymas Basin (27°N, 111°W), in the Pacific Ocean at the depth of 2,000 m 136 Geogemma pacifica Archaea, Crenarchaeota, M Sulfide rock from an Unpublished Desulfurococcales, active hydrothermal data Pyrodictiaceae, Geogemma vent sulfide chimney http://aem.asm.org/ called Godzilla in the Pacific Ocean (47°N, 129°W) 139 Ferroglobus pacificus Archaea, Euryarchaeota, M Sulfide rock from an Unpublished Archaeoglobaceae, active hydrothermal data Ferroglobus vent sulfide chimney called Godzilla in the Pacific Ocean (47°N, 129°W) 140 Archaea, Euryarchaeota, M Sulfide rock from an Unpublished on March 14, 2013 by Univ of Massachusetts Amherst Archaeoglobaceae active hydrothermal data vent sulfide chimney called Godzilla in the Pacific Ocean (47°N, 129°W) 121 Geogemma barossii Archaea, Crenarchaeota, M Vent fluid from an active 16 Desulfurococcales, hydrothermal sulfide Pyrodictiaceae, Geogemma chimney called Finn in the Pacific Ocean (47°N, 129°W) 296 Geogemma indica Archaea, Crenarchaeota, M Sulfide rock samples Unpublished Desulfurococcales, collected from the data Pyrodictiaceae, Geogemma Kairei hydrothermal vent field, located along the Central Indian Ridge (25°S, 70°E) in the Indian Ocean 297 Ferroglobus indicus Archaea, Euryarchaeota, M Sulfide rock samples Unpublished Archaeoglobaceae, collected from the data Ferroglobus Kairei hydrothermal vent field, located along the Central Indian Ridge (25°S, 70°E) in the Indian Ocean 301 Archaea M Sulfide rock samples Unpublished collected from the data Edmonds vent field