Histidine accelerates electrochemical carbon dioxide reduction by metal sulfide mineral catalysts

Interactions between Fe-Ni-S cluster and amino acid play an essential role in the efficient carbon dioxide (CO2) reduction reaction catalyzed by [NiFe]-carbon monoxide dehydrogenase (CODH), one of the ancient CO2 reductases. Because of the structural similarity to the active core of CODH, the violarite (FeNi2S4) mineral has been postulated as the inorganic origin of CODH. However, how the mineral core could have been functionalized by the interaction with amino acids remains largely elusive. Here, we report that the selectivity of CO2 reduction by violarite is markedly influenced by the functional groups of amino acids. Bare violarite catalyzes CO2 reduction to form carbon monoxide and methane, while the coordination with histidine directs the reaction pathway for formate synthesis. Vibrational spectroscopic analysis using histamine and glycine as alternative amine compounds shows that the imidazole group coordinates directly with CO2 and acts as a cofactor in CO2 reduction, similar to the enzymatic reaction in CODH. Our study provides the first insight into the influence of amino acids on the CO2 reduction by metal sulfide minerals. This, in turn, sheds light on the origin of life model at deepsea hydrothermal vents, where metal sulfides are predicted to have functioned as proto-enzymes for the carbon fixation reaction.