Reduction of Fe(III), Mn(IV), and Toxic Metals at 100°C by Pyrobaculum islandicum

Abstract

It has recently been noted that a diversity of hyperthermophilic microorganisms have the ability to reduce Fe(III) with hydrogen as the electron donor, but the reduction of Fe(III) or other metals by these organisms has not been previously examined in detail. When Pyrobaculum islandicum was grown at 100°C in a medium with hydrogen as the electron donor and Fe(III)-citrate as the electron acceptor, the increase in cell numbers of P. islandicum per mole of Fe(III) reduced was found to be ca. 10-fold higher than previously reported. Poorly crystalline Fe(III) oxide could also serve as the electron acceptor for growth on hydrogen. The stoichiometry of hydrogen uptake and Fe(III) oxide reduction was consistent with the oxidation of 1 mol of hydrogen resulting in the reduction of 2 mol of Fe(III). The poorly crystalline Fe(III) oxide was reduced to extracellular magnetite. P. islandicum could not effectively reduce the crystalline Fe(III) oxide minerals goethite and hematite. In addition to using hydrogen as an electron donor for Fe(III) reduction, P. islandicum grew via Fe(III) reduction in media in which peptone and yeast extract served as potential electron donors. The closely related species P. aerophilum grew via Fe(III) reduction in a similar complex medium. Cell suspensions of P. islandicum reduced the following metals with hydrogen as the electron donor: U(VI), Tc(VII), Cr(VI), Co(III), and Mn(IV). The reduction of these metals was dependent upon the presence of cells and hydrogen. The metalloids arsenate and selenate were not reduced. U(VI) was reduced to the insoluble U(IV) mineral uraninite, which was extracellular. Tc(VII) was reduced to insoluble Tc(IV) or Tc(V). Cr(VI) was reduced to the less toxic, less soluble Cr(III). Co(III) was reduced to Co(II). Mn(IV) was reduced to Mn(II) with the formation of manganese carbonate. These results demonstrate that biological reduction may contribute to the speciation of metals in hydrothermal environments and could account for such phenomena as magnetite accumulation and the formation of uranium deposits at ca. 100°C. Reduction of toxic metals with hyperthermophilic microorganisms or their enzymes might be applied to the remediation of metal-contaminated waters or waste streams.

Geomicrobiological factors that control uranium mobility in the environment: Update on recent advances in the bioremediation of uranium-contaminated sites

“…Since the first report on the ability of some Fe(III) reducing bacteria to enzymatically reduce U(VI) (Lovley et al, 1991), the number of known U(VI) reducing microorganisms has increased (Shelobolina et al, 2004;. As shown in Figure 2, more than 25 species of phylogenetically diverse prokaryotes are known to mediate enzymatic U(VI) reduction, including a hyperthermophilic archaeon (Kashefi and Lovley, 2000), thermophilic bacteria (Kieft et al, 1999), mesophilic Fe(III) reducing bacteria (Lovley et al, 1991, Coates et al, 1998Coates et al, 2001), mesophilic sulfate reducing bacteria (Lovley and Phillips, 1992;Lovley et al, 1993;Tebo and Obraztsova, 1998;Suzuki et al, 2005), fermentative bacteria (Francis et al, 1994;Sani et al, 2002), a heterotrophic bacterium (McLean and Beveridge, 2001), and an acidotolerant bacterium (Shelobolina et al, 2004). Some of these have been shown to grow using U(VI) as a sole terminal electron acceptor (Lovley et al, 1991;Tebo and Obraztsova, 1998;Pietzsch et al, 1999).…”

U(VI) reduction by spores of Clostridium acetobutylicum

“…, extremophiles (e.g., Thermoanaerobacter spp. (Roh et al, 2002) and Pyrobaculum islandicum (Kashefi and Lovley, 2000)) as well as Gram-positive non-spore-forming bacteria (e.g., Thermoterrabacterium sp.) (Khijniak et al, 2005).…”

Regulation of the aerobic respiratory chain in the facultatively aerobic and hyperthermophilic archaeon Pyrobaculum oguniense

“…Under anaerobic conditions, this organism grows with elemental sulfur, thiosulfate, glutathione (oxidized form) or L-cystine as terminal electron acceptor (Sako et al, 2001). From the aspect of respiration, the genus Pyrobaculum is uniquely variable among the hyperthermophilic archaea, which may be closest to the common ancestor of all organisms; P. aerophilum is not only a microaerophile but also a nitrate, nitrite, thiosulfate, arsenate and selenite reducer (Völkl et al, 1993;Huber et al, 2000); Pyrobaculum islandicum reduces sulfur and iron(II) compounds (Huber et al, 1987;Kashefi & Lovely, 2000;Vargas et al, 1998); Pyrobaculum organotrophum reduces sulfur compounds (Huber et al, 1987); Thermoproteus neutrophilus, which is classified in the genus Thermoproteus although the phylogenetic analysis of 16S rDNA indicated that it should be reclassified as a Pyrobaculum species (Ito et al, 1998), is a sulfur reducer (Fischer et al, 1983); Pyrobaculum arsenaticum is arsenite reducer . This diversity of respiration in close relatives suggests that this genus may show a good example of the evolution of respiration and also show the nature of adaptation to the aerobic environment.…”