Native metals, electron bifurcation, and CO2 reduction in early biochemical evolution.

Molecular hydrogen is an ancient source of energy and electrons. Anaerobic autotrophs that harness the H2/CO2 redox couple harbour ancient biochemical traits that trace back to the universal common ancestor. Aspects of their physiology, including the abundance of transition metals, radical reaction mechanisms, and their main exergonic bioenergetic reactions, forge links between ancient microbes and geochemical reactions at hydrothermal vents. The midpoint potential of H2 however requires anaerobes that reduce CO2 with H2 to use flavin based electron bifurcation-a mechanism to conserve energy as low potential reduced ferredoxins via soluble proteins-for CO2 fixation. This presents a paradox. At the onset of biochemical evolution, before there were proteins, how was CO2 reduced using H2? FeS minerals alone are probably not the solution, because biological CO2 reduction is a two electron reaction. Physiology can provide clues. Some acetogens and some methanogens can grow using native iron (Fe0) instead of H2 as the electron donor. In the laboratory, Fe0 efficiently reduces CO2 to acetate and methanol. Hydrothermal vents harbour awaruite, Ni3Fe, a natural compound of native metals. Native metals might have been the precursors of electron bifurcation in biochemical evolution.