Guilherme Vilela-Alves, Rita R. Manuel, Guilherme Martins, Philippe Carpentier, Agata Raczyńska, Maciej Szaleniec, Inês A Cardoso Pereira, Maria João Romão, Cristiano Mota
ABSTRACT Mo/W‐dependent formate dehydrogenases (Fdhs) catalyze the reversible reduction of CO 2 to formate and are key biocatalysts with high potential for CO 2 capture/conversion technologies. Although previous studies have suggested the presence of two substrate‐access tunnels in Fdhs, experimental evidence for CO 2 ‐specific pathways has been lacking. Here, we present an integrated study of Nitratidesulfovibrio vulgaris FdhAB combining crystallography, molecular dynamics simulations, mutagenesis, and kinetic assays. Nv FdhAB crystals pressurized with Kr, O 2 , and CO 2 were used to map gas diffusion routes and uncovered a substrate‐retention site consistently occupied by small molecules in multiple crystal structures. Our results indicate that both substrates mostly use the main tunnel to reach this retention site, but H 2 O and CO 2 can also enter through a novel side branch before following a shared route to the buried W active site. The retention site, located at the junction of both tunnels, plays a synergistic role in enhancing CO 2 reduction by increasing substrate concentration near the catalytic center, thereby improving catalytic efficiency. Notably, variants affecting this site showed a selective effect for CO 2 reduction, with no impact on formate oxidation. These findings provide experimental evidence of a CO 2 ‐specific pathway and identify structural determinants underpinning efficient CO 2 reduction in this enzyme family.