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

Reinhard, Marco E. and Mara, Michael W. and Kroll, Thomas and Lim, Hyeongtaek and Hadt, Ryan G. and Alonso-Mori, Roberto and Chollet, Matthieu and Glownia, James M. and Nelson, Silke and Sokaras, Dimosthenis and Kunnus, Kristjan and van Driel, Tim Brandt and Hartsock, Robert W. and Kjaer, Kasper S. and Weninger, Clemens and Biasin, Elisa and Gee, Leland B. and Hodgson, Keith O. and Hedman, Britt and Bergmann, Uwe and Solomon, Edward I. and Gaffney, Kelly J. (2021) Short-lived metal-centered excited state initiates iron-methionine photodissociation in ferrous cytochrome c. Nature Communications, 12 . Art. No. 1086. ISSN 2041-1723. https://resolver.caltech.edu/CaltechAUTHORS:20210223-105233904

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41467-021-21423-wDOIArticle
ORCID:
AuthorORCID
Lim, Hyeongtaek0000-0003-3470-8296
Hadt, Ryan G.0000-0001-6026-1358
Alonso-Mori, Roberto0000-0002-5357-0934
Biasin, Elisa0000-0002-7276-4224
Bergmann, Uwe0000-0001-5639-166X
Solomon, Edward I.0000-0003-0291-3199
Gaffney, Kelly J.0000-0002-0525-6465
Additional Information:© The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 24 July 2020; Accepted 22 January 2021; Published 17 February 2021. M.E.R., K.K. and K.J.G. acknowledge support from the U.S. Department of Energy, Office of Science, Basic Energy Sciences, Chemical Sciences, Geosciences, and Biosciences Division. This research was also supported by the National Institute of General Medical Sciences under awards R01GM040392 (E.I.S.) and F32GM122194 (L.B.G.). Use of the Linac Coherent Light Source (LCLS) and the Stanford Synchrotron Radiation Lightsource (SSRL) of the SLAC National Accelerator Laboratory is supported by the U.S. Department of Energy (DOE) Office of Science, Office of Basic Energy Sciences under contract DE-AC02-76SF00515. The SSRL Structural Molecular Biology Program is supported by the DOE Office of Biological and Environmental Research and by the National Institutes of Health, National Institute of General Medical Sciences (P41GM103393). R.G.H. acknowledges a Gerhard Casper Stanford Graduate Fellowship and an Achievement Rewards for College Scientists Fellowship. Data availability: The XES and XSS data shown in Figs. 2b and 4a are provided as Source Data files. Source data are provided with this paper. Code availability: All relevant data and analysis scripts used in this study are available from the corresponding authors upon reasonable request. Author Contributions: K.J.G., E.I.S., R.G.H., M.W.M., U.B. and R.A.M. designed the experiments. M.E.R., M.W.M., T.K., H.L., R.G.H., R.A.M., T.B.v.D., M.C., J.M.G., S.N., D.S., K.K., R.W.H., C.W. and L.B.G. conducted the experiment at the LCLS. M.E.R. and K.J.G. analyzed the data with help from K.S.K. and E.B. M.W.M. performed DFT calculations and purified and prepared protein samples. K.J.G., M.E.R., M.W.M. and E.I.S. wrote the manuscript with input from all authors. The authors declare no competing interests. Peer review information: Nature Communications thanks Hyotcherl Iheethe and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.
Funders:
Funding AgencyGrant Number
NIHR01GM040392
NIH Postdoctoral FellowshipF32GM122194
Department of Energy (DOE)DE-AC02-76SF00515
NIHP41GM103393
Stanford UniversityUNSPECIFIED
ARCS FoundationUNSPECIFIED
Subject Keywords:Biophysical chemistry; Chemical physics; Excited states
Record Number:CaltechAUTHORS:20210223-105233904
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210223-105233904
Official Citation:Reinhard, M.E., Mara, M.W., Kroll, T. et al. Short-lived metal-centered excited state initiates iron-methionine photodissociation in ferrous cytochrome c. Nat Commun 12, 1086 (2021). https://doi.org/10.1038/s41467-021-21423-w
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:108151
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:23 Feb 2021 22:49
Last Modified:23 Feb 2021 22:49

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