The ability of hyperthermophilic microorganisms to transfer electrons to hu
mic substances (humics) and other extracellular quinones was evaluated. Whe
n H-2 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 hyperth
ermophilic Archaea including: Pyrodictium abyssi, Pyrococcus furiosus, Arch
aeoglobus fulgidus, Thermococcus celer, Methanopyrus kandleri, as well as t
he thermophiles Methanococcus thermolithitrophicus and Methanobacterium the
rmoautotrophicum, exhibited H-2-dependent AQDS reduction as did the hyperth
ermophilic bacterium Thermotoga maritima. AQDS acted as an electron shuttle
between P. islandicum and poorly crystalline Fe(III) oxide and greatly acc
elerated rates of Fe(III) reduction. Electron shuttling by AQDS also promot
ed the reduction of the crystalline Fe(III) oxide forms, goethite and hemat
ite. These results have implications for the potential mechanisms of Fe(III
) reduction in various hot Fe(III)-containing environments such as near hyd
rothermal marine vents, terrestrial hot springs, and the deep terrestrial s
ubsurface. The finding that the ability to reduce extracellular quinones is
a characteristic of ail of the hyperthermophiles evaluated and the fact th
at these hyperthermophiles are the organisms most closely related to the la
st common ancestor of extant organisms suggests that the last common ancest
or had the ability to reduce humics. In combination with plausible geochemi
cal scenarios, these results suggest that electron transfer to extracellula
r quinones and Fe(III) were initial steps in the eventual evolution of intr
acellular electron transport chains that employ quinones and iron-containin
g proteins. (C) 2000 Elsevier science B.V. All rights reserved.