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

Author

Listed:
  • Jan Kern

    (Lawrence Berkeley National Laboratory
    LCLS, SLAC National Accelerator 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
    Max-Volmer-Laboratorium für Biophysikalische Chemie, Technische Universität)

  • 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
    Present address: Diamond Light Source, Harwell Science and Innovation Campus, Didcot, Oxfordshire OX11 0DE, UK)

  • Guangye Han

    (Lawrence Berkeley National Laboratory)

  • Julia Hellmich

    (Institut für Biologie, Humboldt-Universität zu Berlin
    Max-Volmer-Laboratorium für Biophysikalische Chemie, Technische Universität)

  • Benedikt Lassalle-Kaiser

    (Lawrence Berkeley National Laboratory
    Present address: Synchrotron SOLEIL, F-91192 Gif-Sur-Yvette, France)

  • 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
    Present address: Department of Cell and Molecular Biology, Uppsala Universitet, 751 24 Uppsala, Sweden)

  • 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
    PULSE Institute, 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
    Max-Volmer-Laboratorium für Biophysikalische Chemie, Technische Universität)

  • 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)

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.

Suggested Citation

  • 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 H, 2014. "Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy," Nature Communications, Nature, vol. 5(1), pages 1-11, September.
    • Handle: RePEc:nat:natcom:v:5:y:2014:i:1:d:10.1038_ncomms5371
    DOI: 10.1038/ncomms5371
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    Cited by:

    1. Kevin M. Dalton & Jack B. Greisman & Doeke R. Hekstra, 2022. "A unifying Bayesian framework for merging X-ray diffraction data," Nature Communications, Nature, vol. 13(1), pages 1-13, December.

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