A fIVe-coordinate Mn(IV) intermediate in biological water oxidation: Spectroscopic signature and a pIVot mechanism for water binding

Marius Retegan, Vera Krewald, Fikret Mamedov, Frank Neese, Wolfgang Lubitz, Nicholas Cox, Dimitrios A. Pantazis

Research output: Contribution to journalArticlepeer-review

109 Citations (Scopus)

Abstract

Among the four photo-driven transitions of the water-oxidizing tetramanganese-calcium cofactor of biological photosynthesis, the second-last step of the catalytic cycle, that is the S2 to S3 state transition, is the crucial step that poises the catalyst for the final O-O bond formation. This transition, whose intermediates are not yet fully understood, is a multi-step process that involves the redox-active tyrosine residue and includes oxidation and deprotonation of the catalytic cluster, as well as the binding of a water molecule. Spectroscopic data has the potential to shed light on the sequence of events that comprise this catalytic step, which still lacks a structural interpretation. In this work the S2-S3 state transition is studied and a key intermediate species is characterized: it contains a Mn3O4Ca cubane subunit linked to a five-coordinate Mn(iv) ion that adopts an approximately trigonal bipyramidal ligand field. It is shown using high-level density functional and multireference wave function calculations that this species accounts for the near-infrared absorption and electron paramagnetic resonance observations on metastable S2-S3 intermediates. The results confirm that deprotonation and Mn oxidation of the cofactor must precede the coordination of a water molecule, and lead to identification of a novel low-energy water binding mode that has important implications for the identity of the substrates in the mechanism of biological water oxidation.

Original languageEnglish
Pages (from-to)72-84
Number of pages13
JournalChemical Science
Volume7
Issue number1
Early online date17 Nov 2015
DOIs
Publication statusPublished - 16 Jan 2016

ASJC Scopus subject areas

  • Chemistry(all)

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