Vibrational Coherence from van der Waals Modes in the Native and Molten-Globule States of ZnII-Substituted Cytochrome c

The low-frequency vibrational coherence from Zn-II-substituted cytochrome c (ZnCytc) was characterized at room temperature in the native and acid/high-salt molten-globule states using femtosecond pump probe, dynamic-absorption spectroscopy and impulsive excitation of the Soret absorption band. The pump probe signals observed from the native state contain two types of modulation components in the vibrational coherence. The first type is a set of slowly damped (damping time) gamma > 1.5 ps) components with frequencies of 10, 30, 70, and 120 cm(-1) that are assigned to out-of-plane vibrations of the porphyrin macrocycle following similar assignments in other porphyrin systems. A similar set of components is observed in the pump-probe signal from the molten-globule state, but the signal is much less strongly modulated. The second type is a strong, very rapidly damped (gamma < 150 fs) 79 cm(-1) modulation component that is assigned to van der Waals interactions between the porphyrin and nonpolar groups in its first solvation shell from the surrounding protein structure; the line shape and intensity of this component are comparable to those observed previously for bacteriochlorophyll a and Zn-II meso-tetrakis(N-methylpyridyl)porphyrin in solution. This component is almost completely absent from the signal from the molten-globule state. The results suggest that the van der Waals modes obtain intensity enhancement in the vibrational coherence because the attacking groups are displaced by the change of extent and/or change in shape of the pi-electron density that accompanies the pi ->pi* optical transition of the Zn-II porphyrin. In the molten-globule state of ZnCytc, owing to the expanded hydrophobic core and to the loss of order for the groups that attack the pi-electron density of the Zn-II porphyrin, the van der Waals modes are rendered effectively inactive. These results support an assignment of the broad low-frequency background in the spectrum of the vibrational coherence in purple bacterial photosynthetic reaction centers to van der Waals interactions between the primary electron donor, P, and the nonpolar protein-derived groups in its first solvation shell.