Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy

Jan Kern, Rosalie Tran, Roberto Alonso-Mori, Sergey Koroidov, Nathaniel Echols, Johan Hattne, Mohamed Ibrahim, Sheraz Gul, Hartawan Laksmono, Raymond G. Sierra, Richard J. Gildea, Guangye Han, Julia Hellmich, Benedikt Lassalle-Kaiser, Ruchira Chatterjee, Aaron S. Brewster, Claudiu A. Stan, Carina Glöckner, Alyssa Lampe, Dörte DiFiore, Despina Milathianaki, Alan R. Fry, M. Marvin Seibert, Jason E. Koglin, Erik Gallo, Jens Uhlig, Dimosthenis Sokaras, Tsu-Chien Weng, Petrus H. Zwart, David E. Skinner, Michael J. Bogan, Marc Messerschmidt, Pieter Glatzel, Garth J. Williams, Sébastien Boutet, Paul D. Adams, Athina Zouni, Johannes Messinger, Nicholas K. Sauter, Uwe Bergmann (), Junko Yano () and Vittal K. Yachandra ()
Additional contact information
Jan Kern: Lawrence Berkeley National Laboratory
Rosalie Tran: Lawrence Berkeley National Laboratory
Roberto Alonso-Mori: LCLS, SLAC National Accelerator Laboratory
Sergey Koroidov: Institutionen för Kemi, Kemiskt Biologiskt Centrum, Umeå Universitet
Nathaniel Echols: Lawrence Berkeley National Laboratory
Johan Hattne: Lawrence Berkeley National Laboratory
Mohamed Ibrahim: Institut für Biologie, Humboldt-Universität zu Berlin
Sheraz Gul: Lawrence Berkeley National Laboratory
Hartawan Laksmono: PULSE Institute, SLAC National Accelerator Laboratory
Raymond G. Sierra: PULSE Institute, SLAC National Accelerator Laboratory
Richard J. Gildea: Lawrence Berkeley National Laboratory
Guangye Han: Lawrence Berkeley National Laboratory
Julia Hellmich: Institut für Biologie, Humboldt-Universität zu Berlin
Benedikt Lassalle-Kaiser: Lawrence Berkeley National Laboratory
Ruchira Chatterjee: Lawrence Berkeley National Laboratory
Aaron S. Brewster: Lawrence Berkeley National Laboratory
Claudiu A. Stan: PULSE Institute, SLAC National Accelerator Laboratory
Carina Glöckner: Max-Volmer-Laboratorium für Biophysikalische Chemie, Technische Universität
Alyssa Lampe: Lawrence Berkeley National Laboratory
Dörte DiFiore: Max-Volmer-Laboratorium für Biophysikalische Chemie, Technische Universität
Despina Milathianaki: LCLS, SLAC National Accelerator Laboratory
Alan R. Fry: LCLS, SLAC National Accelerator Laboratory
M. Marvin Seibert: LCLS, SLAC National Accelerator Laboratory
Jason E. Koglin: LCLS, SLAC National Accelerator Laboratory
Erik Gallo: European Synchrotron Radiation Facility
Jens Uhlig: European Synchrotron Radiation Facility
Dimosthenis Sokaras: SSRL, SLAC National Accelerator Laboratory
Tsu-Chien Weng: SSRL, SLAC National Accelerator Laboratory
Petrus H. Zwart: Lawrence Berkeley National Laboratory
David E. Skinner: National Energy Research Scientific Computing Center, Lawrence Berkeley National Laboratory
Michael J. Bogan: LCLS, SLAC National Accelerator Laboratory
Marc Messerschmidt: LCLS, SLAC National Accelerator Laboratory
Pieter Glatzel: European Synchrotron Radiation Facility
Garth J. Williams: LCLS, SLAC National Accelerator Laboratory
Sébastien Boutet: LCLS, SLAC National Accelerator Laboratory
Paul D. Adams: Lawrence Berkeley National Laboratory
Athina Zouni: Institut für Biologie, Humboldt-Universität zu Berlin
Johannes Messinger: Institutionen för Kemi, Kemiskt Biologiskt Centrum, Umeå Universitet
Nicholas K. Sauter: Lawrence Berkeley National Laboratory
Uwe Bergmann: LCLS, SLAC National Accelerator Laboratory
Junko Yano: Lawrence Berkeley National Laboratory
Vittal K. Yachandra: Lawrence Berkeley National Laboratory

Nature Communications, 2014, vol. 5, issue 1, 1-11

Abstract: Abstract The dioxygen we breathe is formed by light-induced oxidation of water in photosystem II. O2 formation takes place at a catalytic manganese cluster within milliseconds after the photosystem II reaction centre is excited by three single-turnover flashes. Here we present combined X-ray emission spectra and diffraction data of 2-flash (2F) and 3-flash (3F) photosystem II samples, and of a transient 3F’ state (250 μs after the third flash), collected under functional conditions using an X-ray free electron laser. The spectra show that the initial O–O bond formation, coupled to Mn reduction, does not yet occur within 250 μs after the third flash. Diffraction data of all states studied exhibit an anomalous scattering signal from Mn but show no significant structural changes at the present resolution of 4.5 Å. This study represents the initial frames in a molecular movie of the structural changes during the catalytic reaction in photosystem II.

Date: 2014
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DOI: 10.1038/ncomms5371

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