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Water cleavage by solar radiation—an inspiring challenge of photosynthesis research

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Abstract

Solar energy exploitation by photosynthetic water cleavage is of central relevance for the development and sustenance of all higher forms of living matter in the biosphere. The key steps of this process take place within an integral protein complex referred to as Photosystem II (PS II) which is anisotropically incorporated into the thylakoid membrane. This minireview concentrates on mechanistic questions related to i) the generation of strongly oxidizing equivalents (holes) at a special chlorophyll a complex (designated as P680) and ii) the cooperative reaction of four holes with two water molecules at a manganese containing unit WOC (water oxidizing complex) resulting in the release of molecular oxygen and four protons. The classical work of Pierre Joliot and Bessel Kok and their coworkers revealed that water oxidation occurs via a sequence of univalent oxidation steps including intermediary redox states Si (i = number of accumulated holes within the WOC). Based on our current stage of knowledge, an attempt is made a) to identify the nature of the redox states Si, b) to describe the structural arrangement of the (four) manganese centers and their presumed coordination and ligation within the protein matrix, and c) to propose a mechanism of photosynthetic water oxidation with special emphasis on the key step, i.e. oxygen-oxygen bond formation. It is assumed that there exists a dynamic equilibrium in S3 with one state attaining the nuclear geometry and electronic configuration of a complexed peroxide. This state is postulated to undergo direct oxidation to complexed dioxygen by univalent electron abstraction with YZ ox and simultaneous internal ligand to metal charge transfer.

Key questions on the mechanism will be raised. The still fragmentary answers to these questions not only reflect our limited knowledge but also illustrate the challenges for future research.

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Abbreviations

b559:

cytochrome b559

BChl:

bacteriochlorophyll

Chl:

chlorophyll

CP47:

Chl a containing a 47 kDa polypeptide

D1/D2:

polypeptides of the PS II reaction center

ENDOR:

electron nuclear double resonance

EPR:

electron paramagnetic resonance

ESEEM:

electron spin echo envelope modulation

EXAFS:

extended X-ray absorption fine structure

FTIR:

Fourier transform infrared

NMR:

nuclear magnetic resonance

P680, P700:

photoactive Chl a of PS II and PS I, respectively

PS II:

Photosystem II

QA :

special plastoquinone of PS II

Si :

redox states of WOC

WOC:

water oxidizing complex

WOS:

water oxidizing site

UV/VIS:

ultraviolet/visible

YD, YZ :

redox active tyrosines of polypeptides D2 and D1, respectively

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  1. Max-Volmer-Institute for Biophysical and Physical Chemistry, Technical University Berlin, Straße des 17. Juni 135, D-10623, Berlin, Germany

    Gernot Renger

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Renger, G. Water cleavage by solar radiation—an inspiring challenge of photosynthesis research. Photosynth Res 38, 229–247 (1993). https://doi.org/10.1007/BF00046749

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