Ultrafast carbon monoxide photolysis and heme spin-crossover in myoglobin via nonadiabatic quantum dynamics

TL;DR

This study uses quantum wavepacket dynamics to reveal how ultrafast nuclear vibrations drive the simultaneous photolysis of CO and spin crossover in myoglobin, elucidating their microscopic mechanisms on femtosecond timescales.

Contribution

It provides a detailed quantum mechanical analysis of the ultrafast photochemical reactions in a heme-CO complex, highlighting the role of nuclear vibrations in these processes.

Findings

Coherent oscillations of Fe-CO bond with 42 fs period

Irreversible CO dissociation driven by geometric reorganization

Rapid relaxation to triplet and quintet states within hundreds of femtoseconds

Abstract

Light absorption of myoglobin triggers diatomic ligand photolysis and spin crossover transition of iron(II) that initiate protein conformational change. The photolysis and spin crossover reactions happen concurrently on a femtosecond timescale. The microscopic origin of these reactions remains controversial. Here, we apply quantum wavepacket dynamics to elucidate the ultrafast photochemical mechanism for a heme--carbon monoxide (heme--CO) complex. We observe coherent oscillations of the Fe-CO bond distance with a period of 42 fs and an amplitude of $\sim$1 \AA{}. These nuclear motions induce pronounced geometric reorganization, which makes the CO dissociation irreversible. The reaction is initially dominated by symmetry breaking vibrations inducing an electron transfer from porphyrin to iron. Subsequently, the wavepacket relaxes to the triplet manifold in $\sim$75 fs and to the quintet manifold in $\sim$430 fs. Our results highlight the central role of nuclear vibrations at the origin of the ultrafast photodynamics of organometallic complexes.