Computational study of the electronic structure and magnetic properties of the Ni-C state in [NiFe] hydrogenases including the second coordination sphere

[NiFe] hydrogenases catalyze the reversible formation of H-2. The [NiFe] heterobimetallic active site is rich in redox states. Here, we investigate the key catalytic state Ni-C of Desulfovibrio vulgaris Miyazaki F hydrogenase using a cluster model that includes the truncated amino acids of the entire second coordination sphere of the enzyme. The optimized geometries, computed g tensors, hyperfine coupling constants, and IR stretching frequencies all agree well with experimental values. For the hydride in the bridging position, only a single minimum on the potential energy surface is found, indicating that the hydride bridges and binds to both nickel and iron. The influence of the second coordination sphere on the electronic structure is investigated by comparing results from the large cluster models with truncated models. The largest interactions of the second coordination sphere with the active site concern the hydrogen bonds with the cyanide ligands, which modulate the bond between iron and these ligands. Secondly, the electronic structure of the active site is found to be sensitive to the protonation state of His88. This residue forms a hydrogen bond with the spin-carrying sulfur atom of Cys549, which in turn tunes the spin density at the nickel and coordinating sulfur atoms. In addition, the unequal distribution of spin density over the equatorial cysteine residues results from different orientations of the cysteine side chains, which are kept in their particular orientation by the secondary structure of the protein.