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

DOI: 10.1073/pnas.2000529117 DOI Help

Authors: Mohamed Ibrahim (Humboldt-Universität zu Berlin) , Thomas Fransson (University of Heidelberg) , Ruchira Chatterjee (Lawrence Berkeley National Laboratory) , Mun Hon Cheah (Uppsala University) , Rana Hussein (Humboldt-Universität zu Berlin) , Louise Lassalle (Lawrence Berkeley National Laboratory) , Kyle D. Sutherlin (Lawrence Berkeley National Laboratory) , Iris D. Young (Lawrence Berkeley National Laboratory) , Franklin D. Fuller (Linac Coherent Light Source, SLAC National Accelerator Laboratory) , Sheraz Gul (Lawrence Berkeley National Laboratory) , In-sik Kim (Lawrence Berkeley National Laboratory) , Philipp S. Simon (Lawrence Berkeley National Laboratory) , Casper De Lichtenberg (Uppsala University; Umeå Universitet) , Petko Chernev (Uppsala University) , Isabel Bogacz (Lawrence Berkeley National Laboratory) , Cindy C. Pham (Lawrence Berkeley National Laboratory) , Allen M. Orville (Diamond Light Source; Research Complex at Harwell) , Nicholas Saichek (Lawrence Berkeley National Laboratory) , Trent Northen (Lawrence Berkeley National Laboratory) , Alexander Batyuk (Linac Coherent Light Source, SLAC National Accelerator Laboratory) , Sergio Carbajo (Linac Coherent Light Source, SLAC National Accelerator Laboratory) , Roberto Alonso-mori (Linac Coherent Light Source, SLAC National Accelerator Laboratory) , Kensuke Tono (Japan Synchrotron Radiation Research Institute; RIKEN SPring-8 Center) , Shigeki Owada (Lawrence Berkeley National Laboratory; Japan Synchrotron Radiation Research Institute) , Asmit Bhowmick (Lawrence Berkeley National Laboratory) , Robert Bolotovsky (Lawrence Berkeley National Laboratory) , Derek Mendez (Lawrence Berkeley National Laboratory) , Nigel W. Moriarty (Lawrence Berkeley National Laboratory) , James M. Holton (Lawrence Berkeley National Laboratory; Stanford Synchrotron Radiation Lightsource; University of California) , Holger Dobbek (Humboldt-Universität zu Berlin) , Aaron S. Brewster (Lawrence Berkeley National Laboratory) , Paul D. Adams (Lawrence Berkeley National Laboratory; University of California) , Nicholas K. Sauter (Lawrence Berkeley National Laboratory) , Uwe Bergmann (SLAC National Accelerator Laboratory) , Athina Zouni (Humboldt-Universität zu Berlin) , Johannes Messinger (Uppsala University; Kemiskt Biologiskt Centrum) , Jan Kern (Lawrence Berkeley National Laboratory) , Vittal K. Yachandra (Lawrence Berkeley National Laboratory) , Junko Yano (Lawrence Berkeley National Laboratory)
Co-authored by industrial partner: No

Type: Journal Paper
Journal: Proceedings Of The National Academy Of Sciences , VOL 766

State: Published (Approved)
Published: May 2020

Open Access Open Access

Abstract: 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, S1, S2, S3, and S0, showing that a water molecule is inserted during the S2 → S3 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 O2 formation, we recorded diffraction and Mn X-ray emission spectroscopy (XES) data at several time points during the S2 → S3 transition. At the electron acceptor site, changes due to the two-electron redox chemistry at the quinones, QA and QB, are observed. At the donor site, tyrosine YZ 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 OX(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 S2 → S3 transition mirrors the appearance of OX 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.

Journal Keywords: photosynthesis; photosystem II; water oxidation; oxygen-evolving complex; X-ray free electron laser

Subject Areas: Chemistry

Facility: Advanced Light Source (ALS); Stanford Synchrotron Radiation Lightsource (SSRL); BESSY-II