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 Bergmann; Edward I Solomon; Kelly J Gaffney

doi:10.1038/s41467-021-21423-w

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

Nat Commun. 2021 Feb 17;12(1):1086. doi: 10.1038/s41467-021-21423-w.

Authors

Marco E Reinhard^{1

2}, Michael W Mara^{3

4}, Thomas Kroll², Hyeongtaek Lim³, Ryan G Hadt^{3

5}, Roberto Alonso-Mori⁶, Matthieu Chollet⁶, James M Glownia⁶, Silke Nelson⁶, Dimosthenis Sokaras², Kristjan Kunnus¹, Tim Brandt van Driel⁶, Robert W Hartsock¹, Kasper S Kjaer¹, Clemens Weninger⁶, Elisa Biasin¹, Leland B Gee³, Keith O Hodgson^{2

3}, Britt Hedman², Uwe Bergmann¹, Edward I Solomon^{7

8}, Kelly J Gaffney^{9

10}

Affiliations

¹ PULSE Institute, SLAC National Accelerator Laboratory, Stanford University, Stanford, CA, USA.
² Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, Stanford University, Menlo Park, CA, USA.
³ Department of Chemistry, Stanford University, Stanford, CA, USA.
⁴ Department of Chemistry, Northwestern University, Evanston, IL, USA.
⁵ Division of Chemistry and Chemical Engineering, Arthur Amos Noyes Laboratory of Chemical Physics, California Institute of Technology, Pasadena, CA, USA.
⁶ Linac Coherent Light Source, SLAC National Accelerator Laboratory, Stanford University, Menlo Park, CA, USA.
⁷ Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, Stanford University, Menlo Park, CA, USA. edward.solomon@stanford.edu.
⁸ Department of Chemistry, Stanford University, Stanford, CA, USA. edward.solomon@stanford.edu.
⁹ PULSE Institute, SLAC National Accelerator Laboratory, Stanford University, Stanford, CA, USA. kgaffney@slac.stanford.edu.
¹⁰ Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, Stanford University, Menlo Park, CA, USA. kgaffney@slac.stanford.edu.

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.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Cytochromes c / chemistry
Cytochromes c / metabolism*
Electron Transport / radiation effects
Ferrous Compounds / chemistry
Ferrous Compounds / metabolism*
Heme / chemistry
Heme / metabolism
Iron / chemistry
Iron / metabolism*
Metals / chemistry
Metals / metabolism*
Methionine / chemistry
Methionine / metabolism*
Molecular Dynamics Simulation
Photolysis
Spectrometry, X-Ray Emission

Substances

Ferrous Compounds
Metals
Heme
Cytochromes c
Methionine
Iron

Abstract

Publication types

MeSH terms

Substances

Grants and funding