Oxygen‐evolving PhotosystemII

Abstract

Photosystem II is the enzyme that catalyzes the thermodynamically demanding splitting of water, yielding dioxygen, protons, and electrons, a sunlight‐driven reaction that forms the foundation of oxygenic photosynthesis. The latest results from high‐resolution crystallographic models have led to a refined view of the overall structure of the enzyme and the arrangement of the cofactors involved in light harvesting, charge separation, and electron transfer. In addition, combined efforts from protein crystallography, spectroscopy, and computational chemistry have greatly improved the understanding of the tetramanganese–calcium cluster of the oxygen‐evolving complex, the site of water oxidation. The most important features of the geometric and electronic structures of the oxygen‐evolving complex for the earlier reaction cycle intermediates are now sufficiently well understood such that connections between several structural features and spectroscopic observables can be made with confidence. Advanced spectroscopic techniques have also identified possible sites where the substrate water binds. Although the details of the actual mechanism of biological water oxidation remain elusive, experimental and theoretical studies impose an increasing number of constraints that significantly limit the number of mechanistic possibilities for O–O bond formation.

Metal oxidation states in biological water splitting

“…The oxygen evolving complex (OEC) of PSII contains a catalytically active oxo-bridged Mn 4 Ca cluster that stores the four oxidizing equivalents required to oxidize water into dioxygen. 8 – 12 During catalysis the OEC passes through five oxidation states S i of the Kok cycle, 13 , 14 where i = 0–4 denotes the number of oxidizing equivalents stored in each step ( Fig. 1 ).…”

“…Although these latter questions are of fundamental importance for understanding the function of the natural system and for establishing the principles for the rational design of synthetic water splitting systems, they have remained contentious even after decades of intense research. 8 , 12 , 15 …”

Infrared Spectroscopy of Gas-Phase MnxOy(CO2)z+ Complexes

“…This property is used in nature, for example, for the photocatalytic oxidation of water to molecular oxygen. Here, a small 10-atomic calcium–manganese oxide cluster, CaMn 4 O 5 , acts as a catalytically active center, which cycles through a series of five different oxidation states upon sequential absorption of four photons. − Inspired by this biocatalyst, we have recently started a research project that employs free gas-phase manganese oxide clusters, in particular, to probe fundamental concepts of water activation but also of other molecules such as acids. − …”

What Can We Learn from a Biomimetic Model of Nature’s Oxygen-Evolving Complex?

“…The S0 state is the most reduced physiological form, Mn(III)3Mn(IV), advancing to a Mn(IV)4 S3 state [10][11][12][13] before the final oxidation step to the transient S4 state that evolves dioxygen and resets the system to S0. 14 Owing to its extraordinary ability to catalyze this challenging redox transformation efficiently, the OEC is considered a blueprint for the development of synthetic water-oxidizing systems based on first-row transition metals. [15][16][17][18][19][20][21][22] Synthetic chemistry has targeted various structural aspects of the OEC, including nuclearity, metal composition, and bonding topology.…”