DFT Fea3-O/O-O Vibrational Frequency Calculations over Catalytic Reaction Cycle States in the Dinuclear Center of Cytochrome c Oxidase

Density functional vibrational frequency calculations have been performed on eight geometry optimized cytochrome c oxidase (CcO) dinuclear center (DNC) reaction cycle intermediates and on the oxymyoglobin (oxyMb) active site. The calculated Fe-O and O-O stretching modes and their frequency shifts along the reaction cycle have been compared with the available resonance Raman (rR) measurements. The calculations support the proposal that in state A[Fe-a3(3+)-O-2(-center dot)center dot center dot center dot Cu-B(+)] of CcO, O-2 binds with Fe-a3(2+) in a similar bent end-on geometry to that in oxyMb. The calculations show that the observed 20 cm(-1) shift of the Fe-a3-O stretching mode from the P-R to F state is caused by the protonation of the OH- ligand on Cu-B(2+) (P-R[Fe-a3(4+)=O2-center dot center dot center dot HO--Cu-B(2+)] -> F[Fe-a3(4+)=O2-center dot center dot center dot H2O-Cu-B(2+)), and that the H2O ligand is still on the Cu-B(2+) site in the rR identified F[Fe-a3(4+)=O2-center dot center dot center dot H2O-Cu-B(2+)] state. Further, the observed rR band at 356 cm(-1) between states P-R and F is likely an O-Fe-a3-porphyrin bending mode. The observed 450 cm(-1) low Fe-a3-O frequency mode for the O-H active oxidized state has been reproduced by our calculations on a nearly symmetrically bridged Fe-a3(3+)-OH-Cu-B(2+) structure with a relatively long Fea3-O distance near 2 angstrom. Based on Badger's rule, the calculated Fe-a3-O distances correlate well with the calculated nu(-2.3)(Fe-O) (nu(Fe-O) is the Fe-a3-O stretching frequency) with correlation coefficient R = 0.973.