Reduction of humic substances and Fe(III) by hyperthermophilic microorganisms

The ability of hyperthermophilic microorganisms to transfer electrons to humic substances (humics) and other extracellular quinones was evaluated. When H2 was provided as the electron donor, the hyperthermophile, Pyrobaculum islandicum, transferred electrons to highly purified humics and the humics analog, anthraquinone-2,6-disulfonate (AQDS). A diversity of other hyperthermophilic Archaea including: Pyrodictium abyssi, Pyrococcus furiosus, Archaeoglobus fulgidus, Thermococcus celer, Methanopyrus kandleri, as well as the thermophiles Methanococcus thermolithitrophicus and Methanobacterium thermoautotrophicum, exhibited H2-dependent AQDS reduction as did the hyperthermophilic bacterium Thermotoga maritima. AQDS acted as an electron shuttle between P. islandicum and poorly crystalline Fe(III) oxide and greatly accelerated rates of Fe(III) reduction. Electron shuttling by AQDS also promoted the reduction of the crystalline Fe(III) oxide forms, goethite and hematite. These results have implications for the potential mechanisms of Fe(III) reduction in various hot Fe(III)-containing environments such as near hydrothermal marine vents, terrestrial hot springs, and the deep terrestrial subsurface. The finding that the ability to reduce extracellular quinones is a characteristic of all of the hyperthermophiles evaluated and the fact that these hyperthermophiles are the organisms most closely related to the last common ancestor of extant organisms suggests that the last common ancestor had the ability to reduce humics. In combination with plausible geochemical scenarios, these results suggest that electron transfer to extracellular quinones and Fe(III) were initial steps in the eventual evolution of intracellular electron transport chains that employ quinones and iron-containing proteins.