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

• Published in: Nature (London) Vol. 563; no. 7731; pp. 421 - 425
• Main Authors: Kern, Jan, Chatterjee, Ruchira, Young, Iris D., Fuller, Franklin D., Lassalle, Louise, Ibrahim, Mohamed, Gul, Sheraz, Fransson, Thomas, Brewster, Aaron S., Alonso-Mori, Roberto, Hussein, Rana, Zhang, Miao, Douthit, Lacey, de Lichtenberg, Casper, Cheah, Mun Hon, Shevela, Dmitry, Wersig, Julia, Seuffert, Ina, Sokaras, Dimosthenis, Pastor, Ernest, Weninger, Clemens, Kroll, Thomas, Sierra, Raymond G., Aller, Pierre, Butryn, Agata, Orville, Allen M., Liang, Mengning, Batyuk, Alexander, Koglin, Jason E., Carbajo, Sergio, Boutet, Sébastien, Moriarty, Nigel W., Holton, James M., Dobbek, Holger, Adams, Paul D., Bergmann, Uwe, Sauter, Nicholas K., Zouni, Athina, Messinger, Johannes, Yano, Junko, Yachandra, Vittal K.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.11.2018; Nature Publishing Group
• Subjects: 631/449/1734/2076; 631/535/1266/1265; Calcium - metabolism; Circadian rhythms; Crystallography, X-Ray; Cyanobacteria - chemistry; Humanities and Social Sciences; INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Lasers; Letter; Manganese - metabolism; Models, Molecular; multidisciplinary; Observations; Oxidation-Reduction; Oxidation-reduction reactions; Oxygen - metabolism; Photosynthesis; Photosystem II Protein Complex - chemistry; Photosystem II Protein Complex - metabolism; Plastoquinone - metabolism; Science; Science (multidisciplinary); Spectroscopy; Water; Water - chemistry; Water - metabolism; Photosystem II (PSII); PSII Crystals; Target Unit Cell; Membrane Inlet Mass Spectrometry (MIMS); Omit Densities
• ISSN: 0028-0836; 1476-4687; 1476-4687
• DOI: 10.1038/s41586-018-0681-2

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 cycle 1 , 2 . The model comprises four (meta)stable intermediates (S 0 , S 1 , S 2 and S 3 ) and one transient S 4 state, which precedes dioxygen formation occurring in a concerted reaction from two water-derived oxygens bound at an oxo-bridged tetra manganese calcium (Mn 4 CaO 5 ) cluster in the oxygen-evolving complex 3 – 7 . This reaction is coupled to the two-step reduction and protonation of the mobile plastoquinone Q B 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 S 2 →S 3 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 S 3 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 O 2 release. Thus, our results exclude peroxo-bond formation in the S 3 state, and the nucleophilic attack of W3 onto W2 is unlikely. Crystallography and spectroscopy are used to solve high-resolution structures of the intermediates of Kok’s S-state clock in photosystem II.