Quantum mechanics/molecular mechanics study of the catalytic cycle of water splitting in photosystem II

Eduardo M. Sproviero, José A. Gascón, James P. McEvoy, Gary W Brudvig, Victor S. Batista

Research output: Contribution to journalArticle

259 Citations (Scopus)

Abstract

This paper investigates the mechanism of water splitting in photosystem II (PSII) as described by chemically sensible models of the oxygen-evolving complex (OEC) in the S0-S4 states. The reaction is the paradigm for engineering direct solar fuel production systems since it is driven by solar light and the catalyst involves inexpensive and abundant metals (calcium and manganese). Molecular models of the OEC Mn3CaO4Mn catalytic cluster are constructed by explicitly considering the perturbational influence of the surrounding protein environment according to state-of-the-art quantum mechanics/molecular mechanics (QM/MM) hybrid methods, in conjunction with the X-ray diffraction (XRD) structure of PSII from the cyanobacterium Thermosynechococcus elongatus. The resulting models are validated through direct comparisons with high-resolution extended X-ray absorption fine structure spectroscopic data. Structures of the S3, S4, and S 0 states include an additional μ-oxo bridge between Mn(3) and Mn(4), not present in XRD structures, found to be essential for the deprotonation of substrate water molecules. The structures of reaction intermediates suggest a detailed mechanism of dioxygen evolution based on changes in oxidization and protonation states and structural rearrangements of the oxomanganese cluster and surrounding water molecules. The catalytic reaction is consistent with substrate water molecules coordinated as terminal ligands to Mn(4) and calcium and requires the formation of an oxyl radical by deprotonation of the substrate water molecule ligated to Mn(4) and the accumulation of four oxidizing equivalents. The oxyl radical is susceptible to nucleophilic attack by a substrate water molecule initially coordinated to calcium and activated by two basic species, including CP43-R357 and the μ-oxo bridge between Mn(3) and Mn(4). The reaction is concerted with water ligand exchange, swapping the activated water by a water molecule in the second coordination shell of calcium.

Original languageEnglish
Pages (from-to)3428-3442
Number of pages15
JournalJournal of the American Chemical Society
Volume130
Issue number11
DOIs
Publication statusPublished - Mar 19 2008

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Water Cycle
Molecular mechanics
Photosystem II Protein Complex
Quantum theory
Mechanics
Water
Molecules
Calcium
Deprotonation
Substrates
Oxygen
X-Ray Diffraction
Ligands
X ray diffraction
Reaction intermediates
Molecular Models
Protonation
X ray absorption
Cyanobacteria
Manganese

ASJC Scopus subject areas

  • Chemistry(all)

Cite this

Quantum mechanics/molecular mechanics study of the catalytic cycle of water splitting in photosystem II. / Sproviero, Eduardo M.; Gascón, José A.; McEvoy, James P.; Brudvig, Gary W; Batista, Victor S.

In: Journal of the American Chemical Society, Vol. 130, No. 11, 19.03.2008, p. 3428-3442.

Research output: Contribution to journalArticle

Sproviero, Eduardo M. ; Gascón, José A. ; McEvoy, James P. ; Brudvig, Gary W ; Batista, Victor S. / Quantum mechanics/molecular mechanics study of the catalytic cycle of water splitting in photosystem II. In: Journal of the American Chemical Society. 2008 ; Vol. 130, No. 11. pp. 3428-3442.
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