Role of geochemical protoenzymes (geozymes) in primordial metabolism: specific abiotic hydride transfer by metals to the biological redox cofactor NAD .

Hydrogen gas, H 2 , is generated in serpentinizing hydrothermal systems, where it has supplied electrons and energy for microbial communities since there was liquid water on Earth. In modern metabolism, H 2 is converted by hydrogenases into organically bound hydrides (H - ), for example, the cofactor NADH. It transfers hydrides among molecules, serving as an activated and biologically harnessed form of H 2 . In serpentinizing systems, minerals can also bind hydrides and could, in principle, have acted as inorganic hydride donors-possibly as a geochemical protoenzyme, a 'geozyme'- at the origin of metabolism. To test this idea, we investigated the ability of H 2 to reduce NAD + in the presence of iron (Fe), cobalt (Co) and nickel (Ni), metals that occur in serpentinizing systems. In the presence of H 2 , all three metals specifically reduce NAD + to the biologically relevant form, 1,4-NADH, with up to 100% conversion rates within a few hours under alkaline aqueous conditions at 40 °C. Using Henry's law, the partial pressure of H 2 in our reactions corresponds to 3.6 mm, a concentration observed in many modern serpentinizing systems. While the reduction of NAD + by Ni is strictly H 2 -dependent, experiments in heavy water ( 2 H 2 O) indicate that native Fe can reduce NAD + both with and without H 2 . The results establish a mechanistic connection between abiotic and biotic hydride donors, indicating that geochemically catalysed, H 2 -dependent NAD + reduction could have preceded the hydrogenase-dependent reaction in evolution.