New water oxidation mechanism in Photosystem II resolves major experimental controversies

TL;DR

This paper proposes a new water oxidation mechanism in Photosystem II that resolves longstanding experimental controversies by identifying specific oxygen ligands and their interactions, offering insights into the O-O bond formation process.

Contribution

It introduces a novel mechanism involving the O3 and O6 oxygens and their coupling, clarifying the role of the protein environment in water oxidation.

Findings

O3 oxygen ligated by His337 acts as a slow exchanging substrate.

Coupling of O3 with O6 explains the O-O bond formation.

The proposed peroxide intermediate is energetically more favorable.

Abstract

Light driven oxygen formation in Photosystem II protein is a fundamental process that sustains our biosphere and serves as a blue print to future clean energy solutions due to its high energy conversion efficiency. Last decade of intense research by advanced physical techniques delivered new insights on the structure and function of the Mn4CaO5 cluster a center of the oxygen evolving complex (OEC). However, discrepancies in experimental observations and computational models persist impeding the understanding of the O-O bond formation and the role of the protein environment in the process. Here we show that i) assignment of the OEC unique oxygen O3 ligated by histidine (His337) via dynamic H-bond as a slow exchanging substrate and ii) its coupling with O6 oxygen generated at Mn1 in the S2 to S3 transition give the O-O bond formation mechanism most consistent with all currently available experimental data. Proposal shows how protein environment can steer the O-O bond formation by charge control via H-bond and open coordination of Mn1. Obtained O3-O6 peroxide is at lower energy than peroxides in the most studied O5-O6 bond formation pathway. His337 appears to be similar to distal His in globins used for management of the O2 and H2O2 intermediates. The new mechanism breaks the prior impasse and will undoubtedly invigorate future detailed studies uncovering its further details.