Untangling the sequence of events during the S 2 -> S 3 transition in photosystem II and implications for the water oxidation mechanism

• Published in: Proceedings of the National Academy of Sciences - PNAS 2020, Vol.117 (23), p.12624
• Main Authors: Ibrahim, Mohamed, Fransson, Thomas, Chatterjee, Ruchira, Cheah, Mun Hon, Hussein, Rana, Lassalle, Louise, Sutherlin, Kyle D., Young, Iris D., Fuller, Franklin D., Gul, Sheraz, Kim, In-Sik, Simon, Philipp S., de Lichtenberg, Casper, Chernev, Petko, Bogacz, Isabel, Pham, Cindy C., Orville, Allen M., Saichek, Nicholas, Northen, Trent, Batyuk, Alexander, Carbajo, Sergio, Alonso-Mori, Roberto, Tono, Kensuke, Owada, Shigeki, Bhowmick, Asmit, Bolotovsky, Robert, Mendez, Derek, Moriarty, Nigel W., Holton, James M., Dobbek, Holger, Brewster, Aaron S., Adams, Paul D., Sauter, Nicholas K., Bergmann, Uwe, Zouni, Athina, Messinger, Johannes, Kern, Jan, Yachandra, Vittal K., Yano, Junko
• Format: Article
• Language: English
• Subjects: oxygen-evolving complex; photosynthesis; photosystem II; water oxidation; X-ray free electron laser
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.2000529117

In oxygenic photosynthesis, light-driven oxidation of water to molecular oxygen is carried out by the oxygen-evolving complex (OEC) in photosystem II (PS II). Recently, we reported the room-temperature structures of PS II in the four (semi)stable S-states, S 1 , S 2 , S 3 , and S 0 , showing that a water molecule is inserted during the S 2  -> S 3  transition, as a new bridging O(H)-ligand between Mn1 and Ca. To understand the sequence of events leading to the formation of this last stable intermediate state before O 2 formation, we recorded diffraction and Mn X-ray emission spectroscopy (XES) data at several time points during the S 2  -> S 3  transition. At the electron acceptor site, changes due to the two-electron redox chemistry at the quinones, Q A and Q B , are observed. At the donor site, tyrosine Y Z and His190 H-bonded to it move by 50 μs after the second flash, and Glu189 moves away from Ca. This is followed by Mn1 and Mn4 moving apart, and the insertion of O X (H) at the open coordination site of Mn1. This water, possibly a ligand of Ca, could be supplied via a "water wheel"-like arrangement of five waters next to the OEC that is connected by a large channel to the bulk solvent. XES spectra show that Mn oxidation (τ of ∼350 μs) during the S 2  -> S 3  transition mirrors the appearance of O X electron density. This indicates that the oxidation state change and the insertion of water as a bridging atom between Mn1 and Ca are highly correlated.