Use of Fe(III) as an Electron Acceptor To Recover Previously Uncultured Hyperthermophiles: Isolation and Characterization of Geothermobacterium ferrireducens gen. nov., sp. nov

Abstract

It has recently been recognized that the ability to use Fe(III) as a terminal electron acceptor is a highly conserved characteristic in hyperthermophilic microorganisms. This suggests that it may be possible to recover as-yet-uncultured hyperthermophiles in pure culture if Fe(III) is used as an electron acceptor. As part of a study of the microbial diversity of the Obsidian Pool area in Yellowstone National Park, Wyo., hot sediment samples were used as the inoculum for enrichment cultures in media containing hydrogen as the sole electron donor and poorly crystalline Fe(III) oxide as the electron acceptor. A pure culture was recovered on solidified, Fe(III) oxide medium. The isolate, designated FW-1a, is a hyperthermophilic anaerobe that grows exclusively by coupling hydrogen oxidation to the reduction of poorly crystalline Fe(III) oxide. Organic carbon is not required for growth. Magnetite is the end product of Fe(III) oxide reduction under the culture conditions evaluated. The cells are rod shaped, about 0.5 μm by 1.0 to 1.2 μm, and motile and have a single flagellum. Strain FW-1a grows at circumneutral pH, at freshwater salinities, and at temperatures of between 65 and 100°C with an optimum of 85 to 90°C. To our knowledge this is the highest temperature optimum of any organism in the Bacteria. Analysis of the 16S ribosomal DNA (rDNA) sequence of strain FW-1a places it within the Bacteria, most closely related to abundant but uncultured microorganisms whose 16S rDNA sequences have been previously recovered from Obsidian Pool and a terrestrial hot spring in Iceland. While previous studies inferred that the uncultured microorganisms with these 16S rDNA sequences were sulfate-reducing organisms, the physiology of the strain FW-1a, which does not reduce sulfate, indicates that these organisms are just as likely to be Fe(III) reducers. These results further demonstrate that Fe(III) may be helpful for recovering as-yet-uncultured microorganisms from hydrothermal environments and illustrate that caution must be used in inferring the physiological characteristics of at least some thermophilic microorganisms solely from 16S rDNA sequences. Based on both its 16S rDNA sequence and physiological characteristics, strain FW-1a represents a new genus among the Bacteria. The name Geothermobacterium ferrireducens gen. nov., sp. nov., is proposed (ATCC BAA-426)

Microbial Reduction of Structural Fe(III) in Illite and Goethite

“…Although the oxidation state of Fe in smectite-illite minerals can be altered by abiotic reactions, the role that microbes play in cycling Fe oxidation states has become increasingly recognized. Indeed, microbes and clay minerals can coexist in a number of geological environments ranging from surface soils to sandstones, siltstones and shales at great depth (up to 2700 m below the land surface), and high temperatures (up to 90-100°C) (3)(4)(5)(6). The close contact between microbes and clay minerals provides ample opportunities for their mutual interactions, where clays may provide nutrients and habitats for microbes, and microbes may influence clay mineral reactions.…”

Archaeoglobus sulfaticallidus sp. nov., a thermophilic and facultatively lithoautotrophic sulfate-reducer isolated from black rust exposed to hot ridge flank crustal fluids

“…To determine the ability of strain PM70-1 T to use alternative substrates and electron acceptors, both HEPES (20 mM) and NaHCO 3 (12 mM) buffered variants of the HYL medium were used, as HEPES is known for catalysing the reduction of ferric iron (Kashefi et al, 2002b). Besides the buffer change, the HYL medium was modified as follows: lactate, sulfate and yeast extract were omitted.…”

Caldimicrobium thiodismutans sp. nov., a sulfur-disproportionating bacterium isolated from a hot spring, and emended description of the genus Caldimicrobium

“…In addition, an iron reducer, 'Geothermobacterium ferrireducens' FW-1a, also belongs to this lineage (Kashefi et al, 2002). In this study, a thermophilic sulfur-disproportionating bacterium was isolated as a representative of a novel species in the family Thermodesulfobacteriaceae.…”