Observation of Coherent Reaction Dynamics in Heme Proteins

Abstract

Femtosecond laser pulses, resonant with Soret band of the nitric oxide complex of myoglobin (MbNO), were used to probe coherent, low-frequency nuclear motion of the heme group after photolysis. Distinct oscillations with periods of 430 and 150 femtoseconds were observed and are attributed to heme doming and iron-histidine motion, respectively. These results verify that the nuclear motion of the heme is strongly coupled to the ligand binding reaction and demonstrate that such motion is not determined by overdamped (diffusive) dynamics. The relative phases and frequencies of the nuclear motion of the photoproduct suggest that the coherence arises from impulsive electronic forces associated with the spin-state change of the heme iron atom and the depopulation of its dz2 orbital during the bond-breaking event.

Investigations of Coherent Vibrational Oscillations in Myoglobin

“…More detailed studies of these modes 25 will be presented elsewhere; 69 here we simply wish to stress the existence of the mode near 40 cm -1 . Our earlier FCS studies 11 clearly showed this mode in the power spectrum, but direct 40 cm -1 oscillations in the time domain data could not be discerned under the large detuning conditions that were employed in that study. As a result, we made no assignment of the 40 cm -1 feature.…”

“…The ability to detect these "dark" reaction coupled coherences is a unique feature of FCS. 11,15,25 Such coherences are significant because they provide a window to understanding the electronic and electron-nuclear coupling forces associated with the reaction coordinates of the "dark" chemical reaction.…”

Spectroscopic identification of reactive porphyrin motions

“…42,93 In particular, VCS reveals oscillations below 200 cm −1 strongly coupled to ligand dissociation reactions in heme proteins. 35,[37][38][39]42 Some of these have been plausibly associated with heme doming, but there is no direct evidence for involvement of the Fe. The VCS measurements on porphine halides reveal a 77 cm −1 oscillation whose frequency downshifts by 15 cm −1 upon substitution of Br for Cl, 42 similar to the 19 cm −1 shift of γ 9 determined using NRVS.…”

“…(9), using the masses of Cl or Br for m 2 . We use the appropriately averaged masses of two most abundant isotopes of Cl and Br: 35 Cl, 37 Cl, 79 Br, and 81 Br (all predictions for halide compounds considered in this paper depend very little on which of the above isotopes to use for halide). Similarly, the 0.79 frequency ratio observed for these features slightly exceeds the 0.65 ratio predicted 78 for the two-body oscillator.…”

“…1) long believed to control biologically important reactions in heme proteins, such as cooperative oxygen binding in hemoglobin. [31][32][33] Far infrared measurements find vibrational signals in the frequency range expected for heme doming in iron porphyrins 34 and vibrational coherence spectroscopy (VCS) reveals low frequency molecular oscillations coupled to ligand binding reactions in heme proteins [35][36][37][38][39][40] and porphyrin model compounds. 41,42 However, these measurements do not exclude other vibrations that may appear in this frequency range, such as the FeCO distortion mode (in-phase bend/tilt) in iron carbonyl porphyrins [43][44][45] or other heme distortions that may control redox reactions.…”