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Structure of photosystem II and substrate binding at room temperature

DOI: 10.1038/nature20161 DOI Help

Authors: Iris D. Young (Lawrence Berkeley National Laboratory) , Mohamed Ibrahim (Institut für Biologie, Humboldt-Universität zu Berlin) , Ruchira Chatterjee (Lawrence Berkeley National Laboratory) , Sheraz Gul (Lawrence Berkeley National Laboratory) , Franklin D. Fuller (Lawrence Berkeley National Laboratory) , Sergey Koroidov (Umeå Universitet) , Aaron S. Brewster (Lawrence Berkeley National Laboratory) , Rosalie Tran (Lawrence Berkeley National Laboratory) , Roberto Alonso-mori (SLAC National Accelerator Laboratory) , Thomas Kroll (SLAC National Accelerator Laboratory) , Tara Michels-clark (Lawrence Berkeley National Laboratory) , Hartawan Laksmono (SLAC National Accelerator Laboratory) , Raymond G. Sierra (SLAC National Accelerator Laboratory) , Claudiu A. Stan (SLAC National Accelerator Laboratory) , Rana Hussein (Humboldt-Universität zu Berlin) , Miao Zhang (Humboldt-Universität zu Berlin) , Lacey Douthit (Lawrence Berkeley National Laboratory) , Markus Kubin (Institute for Methods and Instrumentation on Synchrotron Radiation Research) , Casper De Lichtenberg (Umeå Universitet) , Long Vo Pham (Umeå Universitet) , Håkan Nilsson (Umeå Universitet) , Mun Hon Cheah (Umeå Universitet) , Dmitriy Shevela , Claudio Saracini (Umeå Universitet) , Mackenzie A. Bean (Lawrence Berkeley National Laboratory) , Ina Seuffert (Humboldt-Universität zu Berlin) , Dimosthenis Sokaras (SLAC National Accelerator Laboratory) , Tsu-chien Weng (SLAC National Accelerator Laboratory) , Ernest Pastor (Lawrence Berkeley National Laboratory) , Clemens Weninger (SLAC National Accelerator Laboratory) , Thomas Fransson (SLAC National Accelerator Laboratory) , Louise Lassalle (Lawrence Berkeley National Laboratory) , Philipp Bräuer (University of Oxford) , Pierre Aller (Diamond Light Source) , Peter T. Docker (Diamond Light Source) , Babak Andi (National Synchrotron Light Source II) , Allen M. Orville (Diamond Light Source) , James M. Glownia (SLAC National Accelerator Laboratory) , Silke Nelson (SLAC National Accelerator Laboratory) , Marcin Sikorski (SLAC National Accelerator Laboratory) , Diling Zhu (SLAC National Accelerator Laboratory) , Mark S. Hunter (SLAC National Accelerator Laboratory) , Thomas J. Lane (SLAC National Accelerator Laboratory) , Andy Aquila (SLAC National Accelerator Laboratory) , Jason E. Koglin (SLAC National Accelerator Laboratory) , Joseph Robinson (SLAC National Accelerator Laboratory) , Mengning Liang (SLAC National Accelerator Laboratory) , Sébastien Boutet (SLAC National Accelerator Laboratory) , Artem Y. Lyubimov (Stanford University) , Monarin Uervirojnangkoorn (Stanford University) , Nigel W. Moriarty (Lawrence Berkeley National Laboratory) , Dorothee Liebschner (Lawrence Berkeley National Laboratory) , Pavel V. Afonine (Lawrence Berkeley National Laboratory) , David G. Waterman (STFC) , Gwyndaf Evans (Diamond Light Source) , Philippe Wernet (Institute for Methods and Instrumentation on Synchrotron Radiation Research) , Holger Dobbek (Humboldt-Universität zu Berlin) , William I. Weis (Stanford University) , Axel T. Brunger (Stanford University) , Petrus H. Zwart (Lawrence Berkeley National Laboratory) , Paul D. Adams (Lawrence Berkeley National Laboratory) , Athina Zouni (Humboldt-Universität zu Berlin) , Johannes Messinger (Umeå Universitet) , Uwe Bergmann (SLAC National Accelerator Laboratory) , Nicholas K. Sauter (Lawrence Berkeley National Laboratory) , 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: Nature

State: Published (Approved)
Published: November 2016

Abstract: Light-induced oxidation of water by photosystem II (PS II) in plants, algae and cyanobacteria has generated most of the dioxygen in the atmosphere. PS II, a membrane-bound multi-subunit pigment protein complex, couples the one-electron photochemistry at the reaction centre with the four-electron redox chemistry of water oxidation at the Mn4CaO5 cluster in the oxygen-evolving complex (OEC). Under illumination, the OEC cycles through five intermediate S-states (S0 to S4)1, in which S1 is the dark-stable state and S3 is the last semi-stable state before O–O bond formation and O2 evolution2, 3. A detailed understanding of the O–O bond formation mechanism remains a challenge, and will require elucidation of both the structures of the OEC in the different S-states and the binding of the two substrate waters to the catalytic site4, 5, 6. Here we report the use of femtosecond pulses from an X-ray free electron laser (XFEL) to obtain damage-free, room temperature structures of dark-adapted (S1), two-flash illuminated (2F; S3-enriched), and ammonia-bound two-flash illuminated (2F-NH3; S3-enriched) PS II. Although the recent 1.95 Å resolution structure of PS II at cryogenic temperature using an XFEL7 provided a damage-free view of the S1 state, measurements at room temperature are required to study the structural landscape of proteins under functional conditions8, 9, and also for in situ advancement of the S-states. To investigate the water-binding site(s), ammonia, a water analogue, has been used as a marker, as it binds to the Mn4CaO5 cluster in the S2 and S3 states10. Since the ammonia-bound OEC is active, the ammonia-binding Mn site is not a substrate water site10, 11, 12, 13. This approach, together with a comparison of the native dark and 2F states, is used to discriminate between proposed O–O bond formation mechanisms.

Subject Areas: Biology and Bio-materials, Chemistry

Facility: Advanced Light Source; SLAC National Accelerator Laboratory; Stanford Synchrotron Radiation Lightsource