Conversion of pyridoxal to pyridoxamine with NH and H on nickel generates a protometabolic nitrogen shuttle under serpentinizing conditions.

Serpentinizing hydrothermal vents are likely sites for the origin of metabolism because they produce H as a source of electrons for CO reduction while depositing zero-valent iron, cobalt, and nickel as catalysts for organic reactions. Recent work has shown that solid-state nickel can catalyze the H-dependent reduction of CO to various organic acids and their reductive amination with H and NH to biological amino acids under the conditions of H-producing hydrothermal vents and that amino acid synthesis from NH, H, and 2-oxoacids is facile in the presence of Ni. Such reactions suggest a metallic origin of metabolism during early biochemical evolution because single metals replace the function of over 130 enzymatic reactions at the core of metabolism in microbes that use the acetyl-CoA pathway of CO fixation. Yet solid-state catalysts tether primordial amino synthesis to a mineral surface. Many studies have shown that pyridoxal catalyzes transamination reactions without enzymes. Here we show that pyridoxamine, the NH-transferring intermediate in pyridoxal-dependent transamination reactions, is generated from pyridoxal by reaction with NH (as little as 5 mm) and H (5 bar) on Ni as catalyst at pH 11 and 80 °C within hours. These conditions correspond to those in hydrothermal vents undergoing active serpentinization. The results indicate that at the origin of metabolism, pyridoxamine provided a soluble, organic amino donor for aqueous amino acid synthesis, mediating an evolutionary transition from NH-dependent amino acid synthesis on inorganic surfaces to pyridoxamine-dependent organic reactions in the aqueous phase.