Efficient and Selective Electrochemically Driven Enzyme-Catalyzed Reduction of Carbon Dioxide to Formate using Formate Dehydrogenase and an Artificial Cofactor

Abstract

Conspectus Increasing levels of carbon dioxide in the atmosphere and the growing need for energy necessitate a shift toward reliance on renewable energy sources and the utilization of carbon dioxide. Thus, producing carbonaceous fuel by the electrochemical reduction of carbon dioxide has been very appealing. We have focused on addressing the principal challenges of poor selectivity and poor energy efficiency in the electrochemical reduction of carbon dioxide. We have demonstrated here a viable pathway for the efficient and continuous electrochemical reduction of CO2 to formate using the metal-independent enzyme type of formate dehydrogenase (FDH) derived from Candida boidinii yeast. This type of FDH is attractive because it is commercially produced. In natural metabolic processes, this type of metal-independent FDH oxidizes formate to carbon dioxide using NAD+ as a cofactor. We show that FDH can catalyze the reverse process to generate formate when the natural cofactor NADH is replaced with an artificial cofactor, the methyl viologen radical cation. The methyl viologen radical cation is generated in situ, electrochemically. Our approach relies on the special properties of methyl viologen as a “unidirectional” redox cofactor for the conversion of CO2 to formate. Methyl viologen (in the oxidized form) does not catalyze formate oxidation, while the methyl viologen radical cation is an effective cofactor for the reduction of carbon dioxide. Thus, although the thermodynamic driving force is favorable for the oxidized form of methyl viologen to oxidize formate to carbon dioxide, the kinetic factors are not favorable. Only the reverse reaction of carbon dioxide reduction to formate is kinetically viable with the cofactor, methyl viologen radical cation. Binding free energy calculated from atomistic molecular dynamics (MD) simulations consolidate our understanding of these special binding properties of the methyl viologen radical cation and its ability to facilitate the two-electron reduction of carbon dioxide to formate in metal-independent FDH. By carrying out the reactions in a novel three-compartment cell, we have demonstrated the continuous production of formate at high energy efficiency and yield. This cell configuration uses judiciously selected ion-exchange membranes to separate the reaction compartments to preserve the yields of the methyl viologen radical cation and formate. By the electroregeneration of the methyl viologen radical cation at −0.44 V versus the normal hydrogen electrode, we could produce formate at 20 mV negative to the reversible electrode potential for carbon dioxide reduction to formate. Our results are in sharp contrast to the large overpotentials of −800 to −1000 mV required on metal catalysts, vindicating the selectivity and kinetic facility provided by FDH. Formate yields as high as 97% ± 1% could be realized by avoiding the adventitious reoxidation of the methyl viologen radical cation by molecular oxygen. We anticipate that the insights from the electrochemical studies and the MD simula...

Applications of Synthetic Biotechnology on Carbon Neutrality Research: A Review on Electrically Driven Microbial and Enzyme Engineering

“…However, Jayathilake et al developed a novel approach for CO 2 reduction catalyzed by metal-independent FDH with methyl viologen radical cation (MV•+) as the cofactor, which efficiently regenerated at a carbon electrode through electrochemical reduction without any additional reducing agent ( Figure 4 ). Formate yields as high as 97 ± 1% at 20 mV negative to the reversible electrode potential, much lower than that of metal catalysts (−800 mV to −1,000 mV) ( Jayathilake et al, 2019 ). By embedding the enzymes into the metal–organic framework ZIF-8, Rh complex–grafted electrode was used to regenerate NADH and significantly enhanced the catalytic enzyme rate by 12-fold from CO 2 to methanol compared to the free enzyme statue ( Zhang Z et al, 2021 ).…”

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“…microbes and enzymes, often perform reactions with high energy efficiency, near 100% product selectivity even at high single-pass conversion efficiency, low operational energy demand, and the ability to self-regenerate, making them potentially attractive for some industrial chemical transformations. 2–14 The advantages of process electrification and biological catalysis could be simultaneously realized by electrifying bioreactors.…”

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“…Moreover, investigations have demonstrated that the oxidation of formate to carbon dioxide does not occur readily with MV 2+ . Therefore, the overall yield of formate would be preserved without loss from reoxidation [ 150 ]. Ishibashi et al [ 151 ] used methyl viologen (MV 2+ ) instead of NADH.…”