Does Serial Femtosecond Crystallography Depict State-Specific Catalytic Intermediates of the Oxygen-Evolving Complex?
dc.contributor.author
dc.date.accessioned
2023-05-19T11:50:43Z
dc.date.available
2023-05-19T11:50:43Z
dc.date.issued
2023-05-03
dc.identifier.issn
0002-7863
dc.identifier.uri
dc.description.abstract
Recent advances in serial femtosecond crystallography (SFX) of photosystem II (PSII), enabled by X-ray free electron lasers (XFEL), provided the first geometric models of distinct intermediates in the catalytic S-state cycle of the oxygen-evolving complex (OEC). These models are obtained by flash-advancing the OEC from the dark-stable state (S1) to more oxidized intermediates (S2 and S3), eventually cycling back to the most reduced S0. However, the interpretation of these models is controversial because geometric parameters within the Mn4CaO5 cluster of the OEC do not exactly match those expected from coordination chemistry for the spectroscopically verified manganese oxidation states of the distinct S-state intermediates. Here we focus on the first catalytic transition, S1 → S2, which represents a one-electron oxidation of the OEC. Combining geometric and electronic structure criteria, including a novel effective oxidation state approach, we analyze existing 1-flash (1F) SFX-XFEL crystallographic models that should depict the S2 state of the OEC. We show that the 1F/S2 equivalence is not obvious, because the Mn oxidation states and total unpaired electron counts encoded in these models are not fully consistent with those of a pure S2 state and with the nature of the S1 → S2 transition. Furthermore, the oxidation state definition in two-flashed (2F) structural models is practically impossible to elucidate. Our results advise caution in the extraction of electronic structure information solely from the literal interpretation of crystallographic models and call for re-evaluation of structural and mechanistic interpretations that presume exact correspondence of such models to specific catalytic intermediates of the OEC
dc.description.sponsorship
M.D., F.N., and D.A.P. acknowledge support by the Max Planck Society. P.S. and G.C. were supported by the Spanish MCIU, Grant Number PGC2018-098212-B-C22. G.C. also acknowledges support from FPU Grant 19/02781
dc.format.mimetype
application/pdf
dc.language.iso
eng
dc.publisher
Wiley
dc.relation
PGC2018-098212-B-C22
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Reproducció digital del document publicat a: https://doi.org/10.1021/jacs.3c00489
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Journal of the American Chemical Society (JACS), 2023, vol. 145, núm. 19, p. 10604-10621
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Articles publicats (D-Q)
dc.rights
Attribution 4.0 International
dc.rights.uri
dc.subject
dc.title
Does Serial Femtosecond Crystallography Depict State-Specific Catalytic Intermediates of the Oxygen-Evolving Complex?
dc.type
info:eu-repo/semantics/article
dc.rights.accessRights
info:eu-repo/semantics/openAccess
dc.relation.projectID
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PGC2018-098212-B-C22/ES/DESCOMPOSICION EN EL ESPACIO REAL DE PROPIEDADES OPTICAS NO LINEALES PARA EL DISEÑO RACIONAL DE MATERIALES OPTOELECTRONICOS/
dc.type.version
info:eu-repo/semantics/publishedVersion
dc.identifier.doi
dc.identifier.idgrec
036915
dc.contributor.funder
dc.type.peerreviewed
peer-reviewed
dc.relation.FundingProgramme
dc.relation.ProjectAcronym
dc.identifier.eissn
1520-5126