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

Konstantin Falahati,Miquel Huix-Rotllant,Miquel Huix-Rotllant,Miquel Huix-Rotllant,Hiroyuki Tamura,Irene Burghardt

doi:10.1038/s41467-018-06615-1

Abstract

Light absorption of myoglobin triggers diatomic ligand photolysis and a 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 ∼1 Å. 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 ∼75 fs and to the quintet manifold in ∼430 fs. Our results highlight the central role of nuclear vibrations at the origin of the ultrafast photodynamics of organometallic complexes.

Highlights

Light absorption of myoglobin triggers diatomic ligand photolysis and a spin crossover transition of iron(II) that initiate protein conformational change
We find that carbon monoxide (CO) photolysis occurs in around 20 fs in the 1MLCT band, prior to the spin transition
Hereafter this model is referred to as heme–carbon monoxide (heme–CO) for the complex with carbon monoxide and heme for the remaining ligands

Summary

Introduction

Light absorption of myoglobin triggers diatomic ligand photolysis and a spin crossover transition of iron(II) that initiate protein conformational change. Despite the numerous studies on heme-CO photolysis, the kinetics and mechanism of dissociation are still under debate, notably regarding the ultrafast nature of the reaction, and the spin and character of the photolytic state. Franzen, Martin et al, based on time-resolved absorption and Raman experiments, described a “rapid spin state change that must precede photolysis”[20] They consider that photolysis is occurring from a triplet metal→porphyrin ring transfer (3MLCT dissociation)[20,21]. In the model by Franzen et al, the ultrafast reaction is due to valence tautomerism This mechanism implies a rapid interconversion of several quasidegenerate electronic states involving d-transitions, some of which are dissociative for the CO bond.

Methods

Results

Conclusion