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

Marco E. Reinhard, Michael W. Mara, Thomas Kroll, Hyeongtaek Lim, Ryan G. Hadt, Roberto Alonso-Mori, Matthieu Chollet, James M. Glownia, Silke Nelson, Dimosthenis Sokaras, Kristjan Kunnus, Tim Brandt van Driel, Robert W. Hartsock, Kasper S. Kjaer, Clemens Weninger, Elisa Biasin, Leland B. Gee, Keith O. Hodgson, Britt Hedman, Uwe BergmannEdward I. Solomon, Kelly J. Gaffney*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

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. We use ultrafast X-ray solution scattering to follow the dynamics of Fe(II)-S bond dissociation and 1s3p (Kβ) X-ray emission spectroscopy to follow the dynamics of the iron charge and spin multiplicity during bond dissociation. From these measurements, we conclude that the formation of a triplet metal-centered excited state with anti-bonding Fe(II)-S interactions triggers the bond dissociation and precedes the formation of the metastable Fe high-spin quintet state.

Original languageEnglish (US)
Article number1086
JournalNature communications
Volume12
Issue number1
DOIs
StatePublished - Dec 2021

ASJC Scopus subject areas

  • Chemistry(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physics and Astronomy(all)

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