A first-principles quantum chemical study of coenzyme F430:: Interplay of skeletal stereoisomerism and conformation in the stabilization of Nickel(I)

Nonlocal density functional theory calculations, with full geometry optimization, are reported for the Ni(I) and low-spin Ni(II) forms of high-fidelity models of coenzyme F-430, the nickel tetracorphinoid cofactor of methylcoenzyme M reductase (MCR), and its 12,13-diepimer. The diepimer appears to exhibit the conformational characteristics of a typical hydroporphyrin in terms of a strong tendency to adopt highly ruffled conformations and short Ni(II)-N bond distances. In contrast, for native F-430, the steric effects of peripheral substituents impose a potent planarizing influence on the ring system. The relative inability to ruffle implies that the N-4 core of F-430 cannot contract sufficiently to optimally coordinate a small low-spin Ni(II) ion. This appears to be the key factor that results in the stabilization of the larger Ni(I) and high-spin Ni(II) ions by the F-430 ligand environment. The optimized Ni-N bond distances for the Ni(I)-F-430 model compound are 198, 200, 203, and 214 pm and span an extremely wide range of 16 pm, which qualitatively reproduces the central feature of the experimental EXAFS results. Understandably, these bond distances are similar to those found in a crystallographic study of a six-coordinate NI(II) form of MCR. The relatively long Ni-N distances in the optimized geometry of the low-spin Ni(II) form of the F-430 model compound provide a natural explanation for the enhanced axial ligand affinity of F-430 and its greater tendency to switch to the high-spin Ni(II) form, relative to its diepimer. Consistent with experiment, the calculations also predict that Ni(II)-diepi-F-430 is thermodynamically more stable than native Ni(II)-F-430 However, for the Ni(Ij oxidation level, the two epimers ale predicted to be equienergetic. In qualitative agreement with electrochemical measurements, the adiabatic ionization potential of Ni(I)-F-430 is about 0.2 eV higher than that of Ni(I)-diepi-F-430, again reflecting a unique destabilization of low-spin Ni(II) by the F-430 ligand. Finally, the nickel center in Ni(I)-F-430 is truly Ni(I): it carries approximately 82% of the molecular unpaired spin, compared to a nickel spin population of only 56% for Ni(I)-diepi-F-430.