Ferredoxin reduction by hydrogen with iron functions as an evolutionary precursor of flavin-based electron bifurcation

Abstract

Autotrophic theories for the origin of metabolism posit that the first cells satisfied their carbon needs from CO 2 and were chemolithoautotrophs that obtained their energy and electrons from H 2 . The acetyl-CoA pathway of CO 2 fixation is central to that view because of its antiquity: Among known CO 2 fixing pathways it is the only one that is i) exergonic, ii) occurs in both bacteria and archaea, and iii) can be functionally replaced in full by single transition metal catalysts in vitro. In order to operate in cells at a pH close to 7, however, the acetyl-CoA pathway requires complex multi-enzyme systems capable of flavin-based electron bifurcation that reduce low potential ferredoxin—the physiological donor of electrons in the acetyl-CoA pathway—with electrons from H 2 . How can the acetyl-CoA pathway be primordial if it requires flavin-based electron bifurcation? Here, we show that native iron (Fe 0 ), but not Ni 0 , Co 0 , Mo 0 , NiFe, Ni 2 Fe, Ni 3 Fe, or Fe 3 O 4 , promotes the H 2 -dependent reduction of aqueous Clostridium pasteurianum ferredoxin at pH 8.5 or higher within a few hours at 40 °C, providing the physiological function of flavin-based electron bifurcation, but without the help of enzymes or organic redox cofactors. H 2 -dependent ferredoxin reduction by iron ties primordial ferredoxin reduction and early metabolic evolution to a chemical process in the Earth’s crust promoted by solid-state iron, a metal that is still deposited in serpentinizing hydrothermal vents today.