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Abstract

Photosynthesis, a process catalysed by plants, algae and cyanobacteria converts sunlight to energy thus sustaining all higher life on Earth. Two large membrane protein complexes, photosystem I and II (PSI and PSII), act in series to catalyse the light-driven reactions in photosynthesis. PSII catalyses the light-driven water splitting process, which maintains the Earth’s oxygenic atmosphere1. In this process, the oxygen-evolving complex (OEC) of PSII cycles through five states, S0 to S4, in which four electrons are sequentially extracted from the OEC in four light-driven charge-separation events. Here we describe time resolved experiments on PSII nano/microcrystals from Thermosynechococcus elongatus performed with the recently developed2 technique of serial femtosecond crystallography. Structures have been determined from PSII in the dark S1 state and after double laser excitation (putative S3 state) at 5 and 5.5 Å resolution, respectively. The results provide evidence that PSII undergoes significant conformational changes at the electron acceptor side and at the Mn4CaO5 core of the OEC. These include an elongation of the metal cluster, accompanied by changes in the protein environment, which could allow for binding of the second substrate water molecule between the more distant protruding Mn (referred to as the ‘dangler’ Mn) and the Mn3CaOx cubane in the S2 to S3 transition, as predicted by spectroscopic and computational studies3,4. This work shows the great potential for time-resolved serial femtosecond crystallography for investigation of catalytic processes in biomolecules.

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Change history

  • 10 September 2014

    Minor changes were made to Fig. 3c labelling.

Accessions

Primary accessions

Data deposits

The structure factors and coordinates have been deposited in the Protein Data Bank and accession codes for S1 and putative S3 states are 4PBU and 4Q54, respectively.

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Acknowledgements

Experiments were carried out at the Linac Coherent Light Source (LCLS), a national user facility operated by Stanford University on behalf of the US Department of Energy (DOE), Office of Basic Energy Sciences (OBES). This work was supported by the following agencies: the Center for Bio-Inspired Solar Fuel Production, an Energy Frontier Research Center funded by the DOE, Office of Basic Energy Sciences (award DE-SC0001016), the National Institutes of Health (award 1R01GM095583), the US National Science Foundation (award MCB-1021557 and MCB-1120997), the DFG Clusters of Excellence ‘Inflammation at Interfaces’ (EXC 306) and the ‘Center for Ultrafast Imaging’; the Deutsche Forschungsgemeinschaft (DFG); the Max Planck Society, the Atomic, Molecular and Optical Sciences Program; Chemical Sciences Geosciences and Biosciences Division, DOE OBES (M.J.B.) and the SLAC LDRD program (M.J.B., H.L.); the US DOE through Lawrence Livermore National Laboratory under the contract DE-AC52-07NA27344 and supported by the UCOP Lab Fee Program (award no. 118036) and the LLNL LDRD program (12-ERD-031); the Hamburg Ministry of Science and Research and Joachim Herz Stiftung as part of the Hamburg Initiative for Excellence in Research. The research at Purdue University was supported by the U.S. Department of Energy (DOE), Office of Basic Energy Sciences DE-FG02-12ER16340 (Y.P.) and the National Science Foundation Graduate Research Fellowship under Grant 0833366 (K.M.D.). We also want to thank the National Science Foundation for providing funding for the publication of this work through the BioFEL Science Technology Center (award 1231306). We thank H. Isobe, M. Shoji, S. Yamanaka, Y. Umena, K. Kawakami, N. Kamiya, J. R. Shen and K. Yamaguchi for permission to show a section of Fig. 6 of their publication ref. 4 in Fig. 3d of this publication. We thank R. Neutze and his team for support and discussions during joint beamtime for the PSII project and his projects on time-resolved wide-angle scattering studies. We thank A. T. Brunger for discussions concerning data analysis. We thank T. Terwilliger for support with parameter setting of phenix.autobuild program for the SA-omit maps. We also wish to thank R. Burnap for discussions concerning interpretation of results of ligand mutagenesis. We thank J. D. Zook for his contributions concerning plastoquinone quantification. We thank M. Zhu for helping to create high resolution figures for this publication. We thank Raytheon for support of our studies by providing night-vision devices.

Author information

Author notes

    • Christopher Kupitz
    •  & Shibom Basu

    These authors contributed equally to this work.

Affiliations

  1. Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA

    • Christopher Kupitz
    • , Shibom Basu
    • , Ingo Grotjohann
    • , Raimund Fromme
    • , Kimberly N. Rendek
    • , Mark S. Hunter
    • , Jay-How Yang
    • , Danielle E. Cobb
    • , Brenda Reeder
    • , Jesse J. Bergkamp
    • , Tzu-Chiao Chao
    • , Chelsie E. Conrad
    • , Alexandra Ros
    • , Shatabdi Roy-Chowdhury
    • , Thomas A. Moore
    • , Ana L. Moore
    •  & Petra Fromme
  2. Department of Physics, Arizona State University, Tempe, Arizona 85287, USA

    • Nadia A. Zatsepin
    • , Dingjie Wang
    • , Daniel James
    • , Haiguang Liu
    • , Richard A. Kirian
    • , Kevin Schmidt
    • , R. Bruce Doak
    • , Uwe Weierstall
    •  & John C. H. Spence
  3. Lawrence Livermore National Laboratory, Livermore, California 94550, USA

    • Mark S. Hunter
    • , Stefan P. Hau-Riege
    •  & Matthias Frank
  4. Max-Planck-Institut für medizinische Forschung, Jahnstrasse 29, 69120 Heidelberg, Germany

    • Robert L. Shoeman
    • , Stephan Kassemeyer
    • , Lukas Lomb
    • , Karol Nass
    •  & Jan Steinbrener
  5. Center for Free-Electron Laser Science, DESY, Notkestrasse 85, 22607 Hamburg, Germany

    • Thomas A. White
    • , Anton Barty
    • , Andrew L. Aquila
    • , Daniel Deponte
    • , Richard A. Kirian
    • , Kenneth R. Beyerlein
    • , Carl Caleman
    • , Holger Fleckenstein
    • , Lorenzo Galli
    • , Mengning Liang
    • , Andrew V. Martin
    • , Karol Nass
    • , Francesco Stellato
    • , Chunhong Yoon
    •  & Henry N. Chapman
  6. Stanford PULSE Institute, SLAC National Accelerator Laboratory, 2575 Sand Hill Road, Menlo Park, California 94025, USA

    • Raymond G. Sierra
    • , Michael J. Bogan
    •  & Hartawan Laksmono
  7. European XFEL GmbH, Notkestrasse 85, 22607 Hamburg, Germany

    • Andrew L. Aquila
    •  & Chunhong Yoon
  8. Linac Coherent Light Source, Stanford Linear Accelerator Center (SLAC) National Accelerator Laboratory, 2575 Sand Hill Road, Menlo Park, California 94025, USA

    • Daniel Deponte
    • , Marc Messerschmidt
    • , Despina Milathianaki
    • , Marvin Seibert
    • , Garth J. Williams
    •  & Sébastien Boutet
  9. Max Planck Advanced Study Group, Center for Free-Electron Laser Science (CFEL), Notkestrasse 85, 22607 Hamburg, Germany

    • Sadia Bari
    •  & Stephan Kassemeyer
  10. Max-Planck-Institut für Kernphysik, Saupfercheckweg 1, 69117 Heidelberg, Germany

    • Sadia Bari
  11. Department of Physics and Astronomy, Uppsala University, Regementsvägen 1, SE-752 37 Uppsala, Sweden

    • Carl Caleman
  12. University of Regina, 3737 Wascana Pkwy Regina, Saskatchewan S4S 0A2, Canada

    • Tzu-Chiao Chao
  13. Department of Physics, Purdue University, 525 Northwestern Avenue, West Lafayette, Indiana 47907, USA

    • Katherine M. Davis
    • , Lifen Yan
    •  & Yulia Pushkar
  14. University of Hamburg, Luruper Chaussee 149, 22761 Hamburg, Germany

    • Lorenzo Galli
    • , Karol Nass
    •  & Henry N. Chapman
  15. Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA

    • Stefano Marchesini
  16. Department ARC Centre of Excellence for Coherent X-ray Science, Department of Physics, University of Melbourne, Parkville VIC 3010, Australia

    • Andrew V. Martin
  17. Uppsala University, Sankt Olofsgatan 10B, 753 12 Uppsala, Sweden

    • Marvin Seibert
  18. Center for Ultrafast Imaging, Luruper Chaussee 149, 22761 Hamburg, Germany

    • Henry N. Chapman

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Contributions

C.K., I.G., R.F., M.S.H., R.L.S., A.R., K.S., G.J.W., S. Boutet, H.N.C., U.W., R.B.D., M.F., J.C.H.S. and P.F. contributed to the design of the experiment; C.K., I.G., K.N.R., J.-H.Y., D.E.C., B.R., C.E.C. and S.R.-C. worked on cell growth and photosystem II isolation; J.J.B., T.A.M. and A.L.M. worked on plastoquinone synthesis; C.K., I.G., K.N.R., D.E.C., B.R. and J.J.B. worked on biochemical and biophysical characterization of the photosystem II samples; C.K., K.M.D., L.Y. and Y.P. worked on EPR experiments to confirm the S3 population; C.K., I.G., M.S.H., D.E.C. and P.F. developed nano/microcrystallization conditions of photosystem II; C.K., I.G., R.F., K.N.R., M.S.H. and D.E.C. grew crystals of photosystem II; C.K., I.G., R.F., K.N.R., J.-H.Y., D.E.C., R.G.S., H. Laksmono, M.J.B., T.-C.C. and P.F. conducted biophysical characterization of photosystem II crystals; C.K., I.G., L.G., M.L., L.L., J. Steinbrener, F.S. and P.F. designed and/or fabricated calibration or backup samples; C.K., I.G., D.W., D.J., D.D., U.W., R.B.D. and P.F. tested and optimized buffer and crystal suspension conditions for injection; D.W., D.J., D.D., R.A.K., U.W. and R.B.D. designed and produced nozzles; R.B.D., U.W., R.L.S., D.W., D.J., D.D., R.A.K., S. Bari. and L.L. developed and operated the injector; R.L.S., J. Steinbrener and L.L. developed and operated the sample delivery system and the anti-settling device; S. Boutet, M.M. and G.J.W. developed diffraction instrumentation; M.M., M.S., G.J.W. and S. Boutet set up and operated the CXI beamline; M.S.H., R.A.K., D.M., S. Boutet, M.F. and P.F. designed and optimized the laser excitation scheme and aligned the lasers; C.K., S. Basu., I.G., R.F., N.A.Z., M.S.H., R.L.S., T.A.W., D.W., D.J., D.E.C., H.F., H. Laskmono, H. Liu, A.B., A.L.A., D.D., R.A.K., S. Bari., K.R.B., M.J.B., T.-C.C., L.G., S.K., C.C., M.L., M.M., K.N., M.S., J. Steinbrener, F.S., C.Y., G.J.W., S. Boutet, H.N.C., U.W., R.B.D., M.F., J.C.H.S. and P.F. collected X-ray diffraction data at the CXI beamline; S. Basu, R.F., N.A.Z., T.A.W., H. Liu, A.B., A.L.A., R.A.K., K.R.B., S.K., K.N., L.G., C.Y., J.C.H.S. and P.F. analysed the femtosecond crystallography X-ray diffraction data; T.A.W., A.B., A.L.A., R.A.K. and H.N.C. developed the data evaluation and/or hit finding programs; S. Basu, R.F. and N.A.Z. merged the 3D data; S. Basu and R.F. refined the structure and calculated the electron density maps; S. Basu, R.F., N.A.Z. and P.F. designed and made the figures; R.L.S., T.A.W., D.W., D.J., R.L.S., A.B., A.L.A., A.R., K.S., S.M., A.V.M., S.P.H.-R., R.G.S., H.N.C., U.W., R.B.D., M.F., J.C.H.S., T.A.M. and A.L.M. contributed to the writing of the manuscript with discussion, comments or edits; C.K., S. Basu, R.F., N.A.Z., K.N.R., H.N.C., M.F., J.C.H.S. and P.F. contributed to the interpretation of the results; C.K., S. Basu, I.G., R.F., N.A.Z., K.N.R., C.E.C., H.N.C., U.W., R.B.D., M.F., S.R.-C., J.C.H.S. and P.F. wrote and edited the manuscript with discussion and input from all authors.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Petra Fromme.

Extended data

Supplementary information

Videos

  1. 1.

    Graphic representation of the structure factor amplitudes for the dark data set.

    Graphic representation of the structure factor amplitudes for the dark data set. The video shows the structure factor amplitudes from photosystem II nanocrystal SFX data collected in the dark at 5.0 Å , representing the dark S1 state of the oxygen evolving complex. The graphic representation was generated using the CrystFEL suite17.

  2. 2.

    Graphic representation of the structure factor amplitudes for the double-flash data set.

    The video shows the structure factor amplitudes from photosystem II nanocrystal SFX data collected at 5.5 Å from the double flash state, representing the putative S3 state of the oxygen evolving complex. The graphic representation was generated using the CrystFEL suite17.

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