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Can ferric-oxyl excited states explain elongated iron-oxygen bonds in heme peroxidase catalytic intermediates?

Williams, Lewis J. ; Kamps, Jos J.A.G. ; Brânzanic, Adrian M. V. ; Lehene, Maria ; Lundgren, Kristoffer J. M. LU ; Ryde, Ulf LU orcid ; Chatterjee, Kuntal ; Doyle, Margaret D. ; Simon, Philipp S. and Makita, Hiroki , et al. (2026) In Nature Communications 17.
Abstract
The use of X-ray structures to determine and interpret the ferryl iron-oxygen bond order in molecular oxygen-activating heme enzymes has, in the past, been controversial. This has mainly stemmed from the susceptibility of ferryl species to X-ray-induced electronic state changes. In this work we establishe using time-resolved serial femtosecond X-ray crystallography (tr-SFX) on a dye-decolourising peroxidase that the ferryl intermediate species (Compounds I and II) captured following in situ mixing of microcrystals with H2O2 have single, rather than the double bond character expected. X-ray emission validated tr-SFX data with quantum refinement, time-dependent-DFT calculations and QM/MM geometry optimizations together... (More)
The use of X-ray structures to determine and interpret the ferryl iron-oxygen bond order in molecular oxygen-activating heme enzymes has, in the past, been controversial. This has mainly stemmed from the susceptibility of ferryl species to X-ray-induced electronic state changes. In this work we establishe using time-resolved serial femtosecond X-ray crystallography (tr-SFX) on a dye-decolourising peroxidase that the ferryl intermediate species (Compounds I and II) captured following in situ mixing of microcrystals with H2O2 have single, rather than the double bond character expected. X-ray emission validated tr-SFX data with quantum refinement, time-dependent-DFT calculations and QM/MM geometry optimizations together support the concept that the single iron-oxygen bond character is not an indication of ferryl reduction or a protonated form (FeIV-OH) but is instead attributed to the existence of accessible excited states possessing ferric-oxyl (FeIII–O•–) character. Such states offer insight into the nature of ferryl heme. (Less)
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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Oxygen/chemistry, Heme/chemistry, Iron/chemistry, Crystallography, X-Ray, Hydrogen Peroxide/chemistry, Catalysis, Peroxidase/chemistry, Models, Molecular, Oxidation-Reduction
in
Nature Communications
volume
17
article number
2324
pages
14 pages
publisher
Nature Publishing Group
external identifiers
  • pmid:41634046
  • scopus:105033286731
ISSN
2041-1723
DOI
10.1038/s41467-026-69192-8
language
English
LU publication?
yes
additional info
© 2026. The Author(s).
id
71cfbc91-f13d-47a8-9052-e3468d9ffc00
date added to LUP
2026-04-03 09:46:49
date last changed
2026-06-27 12:47:17
@article{71cfbc91-f13d-47a8-9052-e3468d9ffc00,
  abstract     = {{The use of X-ray structures to determine and interpret the ferryl iron-oxygen bond order in molecular oxygen-activating heme enzymes has, in the past, been controversial. This has mainly stemmed from the susceptibility of ferryl species to X-ray-induced electronic state changes. In this work we establishe using time-resolved serial femtosecond X-ray crystallography (tr-SFX) on a dye-decolourising peroxidase that the ferryl intermediate species (Compounds I and II) captured following in situ mixing of microcrystals with H<sub>2</sub>O<sub>2</sub> have single, rather than the double bond character expected. X-ray emission validated tr-SFX data with quantum refinement, time-dependent-DFT calculations and QM/MM geometry optimizations together support the concept that the single iron-oxygen bond character is not an indication of ferryl reduction or a protonated form (Fe<sup>IV</sup>-OH) but is instead attributed to the existence of accessible excited states possessing ferric-oxyl (Fe<sup>III</sup>–O<sup>•–</sup>) character. Such states offer insight into the nature of ferryl heme.}},
  author       = {{Williams, Lewis J. and Kamps, Jos J.A.G. and Brânzanic, Adrian M. V. and Lehene, Maria and Lundgren, Kristoffer J. M. and Ryde, Ulf and Chatterjee, Kuntal and Doyle, Margaret D. and Simon, Philipp S. and Makita, Hiroki and Thompson, Amy J. and Brewster, Aaron S. and Zhou, Tiankun and Lučić, Marina and Wilson, Michael T. and Aller, Pierre and Sanchez-Weatherby, Juan and Gee, Leland and Dehe, Sebastian and Mous, Sandra and Yano, Junko and Yachandra, Vittal K. and Hough, Michael A. and Orville, Allen M. and Kern, Jan F. and Silaghi-Dumitrescu, Radu L. and Worrall, Jonathan A. R.}},
  issn         = {{2041-1723}},
  keywords     = {{Oxygen/chemistry; Heme/chemistry; Iron/chemistry; Crystallography, X-Ray; Hydrogen Peroxide/chemistry; Catalysis; Peroxidase/chemistry; Models, Molecular; Oxidation-Reduction}},
  language     = {{eng}},
  month        = {{02}},
  publisher    = {{Nature Publishing Group}},
  series       = {{Nature Communications}},
  title        = {{Can ferric-oxyl excited states explain elongated iron-oxygen bonds in heme peroxidase catalytic intermediates?}},
  url          = {{http://dx.doi.org/10.1038/s41467-026-69192-8}},
  doi          = {{10.1038/s41467-026-69192-8}},
  volume       = {{17}},
  year         = {{2026}},
}