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Time-resolved X-ray spectroscopy leads to an extension of the classical S-state cycle model of photosynthetic oxygen evolution

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Abstract

In oxygenic photosynthesis, a complete water oxidation cycle requires absorption of four photons by the chlorophylls of photosystem II (PSII). The photons can be provided successively by applying short flashes of light. Already in 1970, Kok and coworkers [Photochem Photobiol 11:457–475, 1970] developed a basic model to explain the flash-number dependence of O2 formation. The third flash applied to dark-adapted PSII induces the S3→S4⇒S0 transition, which is coupled to dioxygen formation at a protein-bound Mn4Ca complex. The sequence of events leading to dioxygen formation and the role of Kok’s enigmatic S4-state are only incompletely understood. Recently we have shown by time-resolved X-ray spectroscopy that in the S3⇒S0 transition an interesting intermediate is formed, prior to the onset of O–O bond formation [Haumann et al. Science 310:1019–1021, 2005]. The experimental results of the time-resolved X-ray experiments are discussed. The identity of the reaction intermediate is considered and the question is addressed how the novel intermediate is related to the S4-state proposed in 1970 by Bessel Kok. This leads us to an extension of the classical S-state cycle towards a basic model which describes sequence and interplay of electron and proton abstraction events at the donor side of PSII [Dau and Haumann, Science 312:1471–1472, 2006].

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Abbreviations

Chl:

chlorophyll

EPR:

electron paramagnetic resonance

EXAFS:

extended X-ray absorption fine-structure

OEC:

oxygen-evolving complex

PSII:

photosystem II

P680:

primary chlorophyll donor in PSII

Pheo:

specific pheophytin acting as the primary electron acceptor in PSII

Q:

‘quencher’ of PSII fluorescence and electron acceptor in PSII

QA :

primary quinone acceptor in PSII

QB :

secondary quinone acceptor in PSII

YZ :

Tyr 160/161 of the D1 protein of PSII

Y •+Z :

oxidized form of YZ

XANES:

X-ray absorption near-edge structure

XAS:

X-ray absorption spectroscopy

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Acknowledgments

The time-resolved X-ray experiments were carried out at the experimental station ID26 of the European Synchrotron Radiation Facility (ESRF, Grenoble, France). We thank Drs. Thomas Neisius, Sigrid Eeckhout, and especially Pieter Glatzel (all ESRF) who contributed significantly to the preparation of the X-ray experiment. Dr. Peter Liebisch, Dr. Claudia Müller, Marcos Barra, and Paola Loja (all Berlin) contributed strongly to the time-resolved X-ray experiments by sample preparation and XAS data collection; Dr. Markus Grabolle (Berlin) measured and analyzed the discussed time-resolved delayed fluorescence data. Drs. Jens Dittmer (Aarhus, Denmark), Pavel Pospíšil (Olomouc, Czech Republic), and Armando Solè (Grenoble, France) contributed significantly to preliminary experiments. Financial support by the DFG (SFB 498) and the BMBF (grant 05KS1KEA/6 in the BioH2 consortium) is gratefully acknowledged.

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    Holger Dau & Michael Haumann

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Dau, H., Haumann, M. Time-resolved X-ray spectroscopy leads to an extension of the classical S-state cycle model of photosynthetic oxygen evolution. Photosynth Res 92, 327–343 (2007). https://doi.org/10.1007/s11120-007-9141-9

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  • DOI: https://doi.org/10.1007/s11120-007-9141-9

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