Structures of the intermediates of Kok’s photosynthetic water oxidation clock

Jan Kern, Ruchira Chatterjee, Iris D. Young, Franklin D. Fuller, Louise Lassalle, Mohamed Ibrahim, Sheraz Gul, Thomas Fransson, Aaron S. Brewster, Roberto Alonso-Mori, Rana Hussein, Miao Zhang, Lacey Douthit, Casper Lichtenberg, Mun Hon Cheah, Dmitry Shevela, Julia Wersig, Ina Seuffert, Dimosthenis Sokaras, Ernest Pastor, Clemens Weninger, Thomas Kroll, Raymond G. Sierra, Pierre Aller, Agata Butryn, Allen M. Orville, Mengning Liang, Alexander Batyuk, Jason E. Koglin, Sergio Carbajo, Sébastien Boutet, Nigel W. Moriarty, James M. Holton, Holger Dobbek, Paul D. Adams, Uwe Bergmann, Nicholas K. Sauter, Athina Zouni (), Johannes Messinger (), Junko Yano () and Vittal K. Yachandra ()
Additional contact information
Jan Kern: Lawrence Berkeley National Laboratory
Ruchira Chatterjee: Lawrence Berkeley National Laboratory
Iris D. Young: Lawrence Berkeley National Laboratory
Franklin D. Fuller: Lawrence Berkeley National Laboratory
Louise Lassalle: Lawrence Berkeley National Laboratory
Mohamed Ibrahim: Institut für Biologie, Humboldt-Universität zu Berlin
Sheraz Gul: Lawrence Berkeley National Laboratory
Thomas Fransson: SLAC National Accelerator Laboratory
Aaron S. Brewster: Lawrence Berkeley National Laboratory
Roberto Alonso-Mori: LCLS, SLAC National Accelerator Laboratory
Rana Hussein: Institut für Biologie, Humboldt-Universität zu Berlin
Miao Zhang: Institut für Biologie, Humboldt-Universität zu Berlin
Lacey Douthit: Lawrence Berkeley National Laboratory
Casper Lichtenberg: Kemiskt Biologiskt Centrum, Umeå Universitet
Mun Hon Cheah: Molecular Biomimetics, Uppsala University
Dmitry Shevela: Kemiskt Biologiskt Centrum, Umeå Universitet
Julia Wersig: Institut für Biologie, Humboldt-Universität zu Berlin
Ina Seuffert: Institut für Biologie, Humboldt-Universität zu Berlin
Dimosthenis Sokaras: SSRL, SLAC National Accelerator Laboratory
Ernest Pastor: Lawrence Berkeley National Laboratory
Clemens Weninger: LCLS, SLAC National Accelerator Laboratory
Thomas Kroll: SSRL, SLAC National Accelerator Laboratory
Raymond G. Sierra: LCLS, SLAC National Accelerator Laboratory
Pierre Aller: Diamond Light Source Ltd, Harwell Science and Innovation Campus
Agata Butryn: Diamond Light Source Ltd, Harwell Science and Innovation Campus
Allen M. Orville: Diamond Light Source Ltd, Harwell Science and Innovation Campus
Mengning Liang: LCLS, SLAC National Accelerator Laboratory
Alexander Batyuk: LCLS, SLAC National Accelerator Laboratory
Jason E. Koglin: LCLS, SLAC National Accelerator Laboratory
Sergio Carbajo: LCLS, SLAC National Accelerator Laboratory
Sébastien Boutet: LCLS, SLAC National Accelerator Laboratory
Nigel W. Moriarty: Lawrence Berkeley National Laboratory
James M. Holton: Lawrence Berkeley National Laboratory
Holger Dobbek: Institut für Biologie, Humboldt-Universität zu Berlin
Paul D. Adams: Lawrence Berkeley National Laboratory
Uwe Bergmann: SLAC National Accelerator Laboratory
Nicholas K. Sauter: Lawrence Berkeley National Laboratory
Athina Zouni: Institut für Biologie, Humboldt-Universität zu Berlin
Johannes Messinger: Kemiskt Biologiskt Centrum, Umeå Universitet
Junko Yano: Lawrence Berkeley National Laboratory
Vittal K. Yachandra: Lawrence Berkeley National Laboratory

Nature, 2018, vol. 563, issue 7731, 421-425

Abstract: Abstract Inspired by the period-four oscillation in flash-induced oxygen evolution of photosystem II discovered by Joliot in 1969, Kok performed additional experiments and proposed a five-state kinetic model for photosynthetic oxygen evolution, known as Kok’s S-state clock or cycle1,2. The model comprises four (meta)stable intermediates (S0, S1, S2 and S3) and one transient S4 state, which precedes dioxygen formation occurring in a concerted reaction from two water-derived oxygens bound at an oxo-bridged tetra manganese calcium (Mn4CaO5) cluster in the oxygen-evolving complex3–7. This reaction is coupled to the two-step reduction and protonation of the mobile plastoquinone QB at the acceptor side of PSII. Here, using serial femtosecond X-ray crystallography and simultaneous X-ray emission spectroscopy with multi-flash visible laser excitation at room temperature, we visualize all (meta)stable states of Kok’s cycle as high-resolution structures (2.04–2.08 Å). In addition, we report structures of two transient states at 150 and 400 µs, revealing notable structural changes including the binding of one additional ‘water’, Ox, during the S2→S3 state transition. Our results suggest that one water ligand to calcium (W3) is directly involved in substrate delivery. The binding of the additional oxygen Ox in the S3 state between Ca and Mn1 supports O–O bond formation mechanisms involving O5 as one substrate, where Ox is either the other substrate oxygen or is perfectly positioned to refill the O5 position during O2 release. Thus, our results exclude peroxo-bond formation in the S3 state, and the nucleophilic attack of W3 onto W2 is unlikely.

Keywords: Photosystem II (PSII); PSII Crystals; Target Unit Cell; Omit Densities; Membrane Inlet Mass Spectrometry (MIMS) (search for similar items in EconPapers)
Date: 2018
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Citations: View citations in EconPapers (3)

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DOI: 10.1038/s41586-018-0681-2

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