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

Marco Reinhard ,S Nelson ,Dimosthenis Sokaras,Tim Brandt Van Driel,Clemens Weninger,Michael W Mara,Roberto Alonso-Mori,Uwe Bergmann,Thomas Kröll ,Britt Hedman,Robert J Hartsock ,Edward I Solomon,Ryan G Hadt,Kristjan Kunnus,Keith O Hodgson,Hyeongtaek Lim,Matthieu Chollet,Kasper Skov Kjær ,Leland B Gee,Elisa Biasin,James M Glownia,Kelly J Gaffney

doi:10.1038/s41467-021-21423-w

Abstract

Highlights

The dynamics of photodissociation and recombination in heme proteins represent an archetypical photochemical reaction widely used to understand the interplay between chemical dynamics and reaction environment
The potential significance of photochemical dynamics for cytochrome c has been enhanced by the discovery that changes in axial ligand coordination are necessary to convert cyt c to a peroxidase enzyme involved in apoptosis[5,6]
The Kβ XES spectrum of 3d transition metal ions is sensitive to the effective 3d spin moment due to the strong exchange interaction between the unpaired 3d electrons and the one unpaired 3p electron in the final state created by the X-ray emission process (Fig. 2a)[24,25]

Summary

Introduction

The dynamics of photodissociation and recombination in heme proteins represent an archetypical photochemical reaction widely used to understand the interplay between chemical dynamics and reaction environment. We report a study of the photodissociation mechanism for the Fe(II)-S bond between the heme iron and methionine sulfur of ferrous cytochrome c This bond dissociation is an essential step in the conversion of cytochrome c from an electron transfer protein to a peroxidase enzyme. While the ultrafast nature of ligand dissociation has been robustly confirmed by ultrafast vibrational spectroscopies[7,9,10], the electronic ES that initiates the dissociation has not been clearly identified For these heme proteins, the light absorption generates a 1π−π* excitation of the porphyrin ring. The MLCT promotes a dπ (dxz, dyz) electron into the π orbital vacated by light absorption, weakening the Fe–CO backbonding and initiating the Fe–CO dissociation Such a mechanism appears less viable for cyt c Fe(II)–S dissociation, since this bond lacks π character[12]. In a prior study of ferrous cyt c8, we used the Fe K-edge X-ray absorption near-edge structure (XANES)[17,18,19] spectrum to characterize the structure around Fe in photoexcited heme confirming the dissociation of Met[80], and 1s3p X-ray emission spectroscopy (Kβ XES) to confirm the highspin quintet state of the resulting five-coordinate Fe(II)[8]

Methods

Results

Conclusion