Photosynthetic water oxidation: binding and activation of substrate waters for O-O bond formation.

David J Vinyard,Gary W Brudvig,Sahr Khan

doi:10.1039/c5fd00087d

David J Vinyard, Gary W Brudvig + Show 1 more

Open Access

https://doi.org/10.1039/c5fd00087d

Copy DOI

Abstract

Photosynthetic water oxidation occurs at the oxygen-evolving complex (OEC) of Photosystem II (PSII). The OEC, which contains a Mn4CaO5 inorganic cluster ligated by oxides, waters and amino-acid residues, cycles through five redox intermediates known as S(i) states (i = 0-4). The electronic and structural properties of the transient S4 intermediate that forms the O-O bond are not well understood. In order to gain insight into how water is activated for O-O bond formation in the S4 intermediate, we have performed a detailed analysis of S-state dependent substrate water binding kinetics taking into consideration data from Mn coordination complexes. This analysis supports a model in which the substrate waters are both bound as terminal ligands and react via a water-nucleophile attack mechanism.

Highlights

The climate, biology and geology of Earth were transformed by the evolution of oxygenic photosynthesis approximately three billion years ago.[1]
Kinetics of substrate water exchange throughout the Kok cycle have been determined by membrane inlet mass spectrometry (MIMS) measurements following rapid mixing of Photosystem II (PSII) with H218O
We have proposed that ammonia, a “harder” Lewis base than water, binds in S2 to the dangler Mn4 in an analogous site as water binds in S3 to the dangler Mn4.63 The addition of a ligand to Mn4 in either S2 or S3 trans to O5 would cause the other terminal water ligands (W1 and W2) to shi their positions towards the cuboidal core of the oxygen-evolving complex (OEC)

Summary

Introduction

The climate, biology and geology of Earth were transformed by the evolution of oxygenic photosynthesis approximately three billion years ago.[1]. Kinetics of substrate water exchange throughout the Kok cycle have been determined by membrane inlet mass spectrometry (MIMS) measurements following rapid mixing of PSII with H218O. This technique, which was pioneered in the Wydrzynski laboratory, allows 34O2 and 36O2 release by PSII in speci c S states (advanced by single-turnover ashes) to be monitored as a function of incubation time with H218O.39,40. We detail models for substrate binding and O–O bond formation in the OEC in light of experimental evidence and comparisons to well-studied inorganic systems

Where are the substrate binding sites?

Mechanism of O–O bond formation

Conclusions