Oxygenic photosynthesis: history, status and perspective

Abstract

Cyanobacteria and plants carry out oxygenic photosynthesis. They use water to generate the atmospheric oxygen we breathe and carbon dioxide to produce the biomass serving as food, feed, fibre and fuel. This paper scans the emergence of structural and mechanistic understanding of oxygen evolution over the past 50 years. It reviews speculative concepts and the stepped insight provided by novel experimental and theoretical techniques. Driven by sunlight photosystem II oxidizes the catalyst of water oxidation, a hetero-metallic Mn4CaO5(H2O)4 cluster. Mn3Ca are arranged in cubanoid and one Mn dangles out. By accumulation of four oxidizing equivalents before initiating dioxygen formation it matches the four-electron chemistry from water to dioxygen to the one-electron chemistry of the photo-sensitizer. Potentially harmful intermediates are thereby occluded in space and time. Kinetic signatures of the catalytic cluster and its partners in the photo-reaction centre have been resolved, in the frequency domain ranging from acoustic waves via infra-red to X-ray radiation, and in the time domain from nano- to milli-seconds. X-ray structures to a resolution of 1.9 Å are available. Even time resolved X-ray structures have been obtained by clocking the reaction cycle by flashes of light and diffraction with femtosecond X-ray pulses. The terminal reaction cascade from two molecules of water to dioxygen involves the transfer of four electrons, two protons, one dioxygen and one water. A rigorous mechanistic analysis is challenging because of the kinetic enslaving at millisecond duration of six partial reactions (4e−, 1H+, 1O2). For the time being a peroxide-intermediate in the reaction cascade to dioxygen has been in focus, both experimentally and by quantum chemistry. Homo sapiens has relied on burning the products of oxygenic photosynthesis, recent and fossil. Mankind's total energy consumption amounts to almost one-fourth of the global photosynthetic productivity. If the average power consumption equalled one of those nations with the highest consumption per capita it was four times greater and matched the total productivity. It is obvious that biomass should be harvested for food, feed, fibre and platform chemicals rather than for fuel.

Structural basis of light‐harvesting in the photosystem II core complex

“…Many organisms use solar energy in a very efficient way, and it is of great interest to understand, how they can achieve this . Cyanobacteria, algae, and plants carry out oxygenic photosynthesis . In this variant, two light‐powered molecular machines known as photosystem I (PSI) and photosystem II (PSII) operate in series to ultimately transfer electrons from water to nicotinamide adenine dinucleotide phosphate (NADPH in its reduced form) and to produce adenosine triphosphate.…”

“…The oxidation reaction of water is catalyzed by a protein‐bound manganese (i.e., Mn 4 CaO 5 ) complex known as the water‐oxidizing complex (WOC; or oxygen‐evolving complex). In recent years, much effort has been put toward unraveling the structure and inner workings of the WOC, and the struggle still goes on . The WOC is situated next to the reaction center (RC) of PSII.…”

The S3 State of the Oxygen-Evolving Complex: Overview of Spectroscopy and XFEL Crystallography with a Critical Evaluation of Early-Onset Models for O–O Bond Formation

“…The OEC is oxidized by successive light-induced electron transfers along a sequence of storage states S i (i = 0-4 denotes the number of stored oxidizing equivalents) with S 4 being a transient state that evolves dioxygen resetting the cluster to S 0 ( Figure 1d). Among the many open questions regarding aspects of the structure and function of PSII, the definition of the geometric/electronic structure and mechanistic principles of the OEC remain in primary focus [3][4][5][6][7][8][9][10][11][12], not least because of the potential relevance of this unique biological catalyst for the development of bioinspired artificial photosynthetic systems [13][14][15][16][17][18][19][20][21][22][23][24][25][26].…”

Dynamic pH‐induced conformational changes of the PsbO protein in the fluctuating acidity of the thylakoid lumen

“…the Mn 4 CaO 5 cluster) and several cofactors of the electron transfer chain (Ferreira et al , Umena et al , Kern et al ). Although the general process of photosynthetic electron transfer at PSII is well‐characterized (Nelson and Junge , Junge ), the specific roles of many of the involved proteins (most of which are essential) remain unclear (Bricker et al ). PsbO is among the most prominent of these proteins.…”