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

Abstract

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.