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

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

Chemistry

Research output: Contribution to journal › Article › peer-review

13 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 language	English (US)
Article number	1086
Journal	Nature communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-21423-w
State	Published - Dec 1 2021

ASJC Scopus subject areas

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

Access to Document

10.1038/s41467-021-21423-w

Cite this

Reinhard, M. E., Mara, M. W., Kroll, T., Lim, H., Hadt, R. G., Alonso-Mori, R., Chollet, M., Glownia, J. M., Nelson, S., Sokaras, D., Kunnus, K., Driel, T. B. V., Hartsock, R. W., Kjaer, K. S., Weninger, C., Biasin, E., Gee, L. B., Hodgson, K. O., Hedman, B., ... Gaffney, K. J. (2021). Short-lived metal-centered excited state initiates iron-methionine photodissociation in ferrous cytochrome c. Nature communications, 12(1), Article 1086. https://doi.org/10.1038/s41467-021-21423-w

@article{663f7b4b2fa14ff893e20c8541d70f7f,

title = "Short-lived metal-centered excited state initiates iron-methionine photodissociation in ferrous cytochrome c",

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.",

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

note = "Funding Information: 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 Light-source (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. Publisher Copyright: {\textcopyright} 2021, The Author(s).",

year = "2021",

month = dec,

day = "1",

doi = "10.1038/s41467-021-21423-w",

language = "English (US)",

volume = "12",

journal = "Nature communications",

issn = "2041-1723",

publisher = "Nature Publishing Group",

number = "1",

}

Reinhard, ME, Mara, MW, Kroll, T, Lim, H, Hadt, RG, Alonso-Mori, R, Chollet, M, Glownia, JM, Nelson, S, Sokaras, D, Kunnus, K, Driel, TBV, Hartsock, RW, Kjaer, KS, Weninger, C, Biasin, E, Gee, LB, Hodgson, KO, Hedman, B, Bergmann, U, Solomon, EI & Gaffney, KJ 2021, 'Short-lived metal-centered excited state initiates iron-methionine photodissociation in ferrous cytochrome c', Nature communications, vol. 12, no. 1, 1086. https://doi.org/10.1038/s41467-021-21423-w

TY - JOUR

T1 - Short-lived metal-centered excited state initiates iron-methionine photodissociation in ferrous cytochrome c

AU - Reinhard, Marco E.

AU - Mara, Michael W.

AU - Kroll, Thomas

AU - Lim, Hyeongtaek

AU - Hadt, Ryan G.

AU - Alonso-Mori, Roberto

AU - Chollet, Matthieu

AU - Glownia, James M.

AU - Nelson, Silke

AU - Sokaras, Dimosthenis

AU - Kunnus, Kristjan

AU - Driel, Tim Brandt van

AU - Hartsock, Robert W.

AU - Kjaer, Kasper S.

AU - Weninger, Clemens

AU - Biasin, Elisa

AU - Gee, Leland B.

AU - Hodgson, Keith O.

AU - Hedman, Britt

AU - Bergmann, Uwe

AU - Solomon, Edward I.

AU - Gaffney, Kelly J.

N1 - Funding Information: 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 Light-source (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. Publisher Copyright: © 2021, The Author(s).

PY - 2021/12/1

Y1 - 2021/12/1

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85101098244&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85101098244&partnerID=8YFLogxK

U2 - 10.1038/s41467-021-21423-w

DO - 10.1038/s41467-021-21423-w

M3 - Article

C2 - 33597529

AN - SCOPUS:85101098244

SN - 2041-1723

VL - 12

JO - Nature communications

JF - Nature communications

IS - 1

M1 - 1086

ER -

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

Abstract

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this