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

DOI: 10.1038/s41586-018-0681-2 DOI Help

Authors: Jan Kern (Lawrence Berkeley National Laborator) , Ruchira Chatterjee (Lawrence Berkeley National Laborator) , Iris D. Young (Lawrence Berkeley National Laborator) , Franklin D. Fuller (Lawrence Berkeley National Laborator) , Louise Lassalle (Lawrence Berkeley National Laborator) , Mohamed Ibrahim (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 (SLAC National Accelerator Laboratory) , Rana Hussein (Humboldt-Universität zu Berlin) , Miao Zhang (Humboldt-Universität zu Berlin) , Lacey Douthit (Lawrence Berkeley National Laboratory) , Casper De Lichtenberg (Umeå Universitet) , Mun Hon Cheah (Uppsala University) , Dmitry Shevela (Umeå Universitet) , Julia Wersig (Humboldt-Universität zu Berlin) , Ina Seuffert (Humboldt-Universität zu Berlin) , Dimosthenis Sokaras (SLAC National Accelerator Laboratory) , Ernest Pastor (Lawrence Berkeley National Laboratory) , Clemens Weninger (SLAC National Accelerator Laboratory) , Thomas Kroll (SLAC National Accelerator Laboratory) , Raymond G. Sierra (SLAC National Accelerator Laboratory) , Pierre Aller (Diamond Light Source) , Agata Butryn (Diamond Light Source) , Allen M. Orville (Diamond Light Source) , Mengning Liang (SLAC National Accelerator Laboratory) , Alexander Batyuk (SLAC National Accelerator Laboratory) , Jason E. Koglin (SLAC National Accelerator Laboratory) , Sergio Carbajo (SLAC National Accelerator Laboratory) , Sébastien Boutet (SLAC National Accelerator Laboratory) , Nigel W. Moriarty (Lawrence Berkeley National Laboratory) , James M. Holton (Lawrence Berkeley National Laboratory; SLAC National Accelerator Laboratory; University of California, San Francisco) , Holger Dobbek (Humboldt-Universität zu Berlin) , Paul D. Adams (Lawrence Berkeley National Laboratory; University of California Berkeley) , Uwe Bergmann (SLAC National Accelerator Laboratory) , Nicholas K. Sauter (Lawrence Berkeley National Laboratory) , Athina Zouni (Humboldt-Universität zu Berlin) , Johannes Messinger (Umeå Universitet; Uppsala University) , Junko Yano (Lawrence Berkeley National Laboratory) , Vittal K. Yachandra (Lawrence Berkeley National Laboratory)
Co-authored by industrial partner: No

Type: Journal Paper
Journal: Nature , VOL 11

State: Published (Approved)
Published: November 2018

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 complex3,4,5,6,7. 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.

Subject Areas: Chemistry

Facility: ALS; SSRL