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

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.

Short-lived metal-centered excited state initiates iron-methionine photodissociation in ferrous cytochrome c

“…This study does not make clear the mechanism for populating such a configuration but they conclude from their calculated ES energies that the transition can be directly assigned to a 1 [ ] ( 1 MC) state and does not require intersystem crossing to a 3 [ ] ( 3 MC) state 26 . Similar conclusions have been drawn in the theoretical study by Falahati et al with the additional complication of significant configuration interaction between the 1 π−π * and the 1 [ ] metal-centered ES 27 .…”

Molecular Photochemistry: Recent Developments in Theory

“…Moreover, more specific variants of MCTDH, such as multilayered MCTDH, permit inclusion of about 100 degrees of freedom . The significantly expanded applicability of MCTDH is easily recognizable from its large number of diverse applications, such as thermally activated delayed fluorescence in organic light‐emitting diodes, organic photovoltaics, carbon monoxide photolysis in myoglobin, and correlated dynamics in highly excited molecules …”

Molekulare Photochemie: Moderne Entwicklungen in der theoretischen Chemie

“…Kurzaufsätze organischer Photovoltaik, [154] zur Photolyse von Kohlenmonoxid in Myoglobin [155] oder zur korrelierten Dynamik hochangeregter Moleküle. [156] Sowohl die Standardmethode der Quantendynamik als auch MCTDH sind dadurch beschränkt, dass vor Beginn der Dynamiksimulationen die vollständigen PES aller involvierten Zustände berechnet werden müssen.…”

“…Zusätzlich erlauben spezialisierte Varianten von MCTDH, wie das Multi‐Layer‐MCTDH, bis zu etwa 100 Freiheitsgrade zu berücksichtigen . Diese deutliche Erweiterung des Einsatzbereiches von Quantendynamik hat eine große Anzahl verschiedener Untersuchungen ermöglicht, beispielsweise zur thermisch aktivierten verzögerten Fluoreszenz in organischen Leuchtdioden, zu organischer Photovoltaik, zur Photolyse von Kohlenmonoxid in Myoglobin oder zur korrelierten Dynamik hochangeregter Moleküle …”