Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser

Christopher Kupitz; Shibom Basu; Ingo Grotjohann; Raimund Fromme; Nadia Zatsepin; Kimberly N. Rendek; Mark S. Hunter; Robert L. Shoeman; Thomas A. White; Dingjie Wang; Daniel James; Jay How Yang; Danielle E. Cobb; Brenda Reeder; Raymond G. Sierra; Haiguang Liu; Anton Barty; Andrew L. Aquila; Daniel Deponte; Richard Kirian; Sadia Bari; Jesse J. Bergkamp; Kenneth R. Beyerlein; Michael J. Bogan; Carl Caleman; Tzu Chiao Chao; Chelsie E. Conrad; Katherine M. Davis; Holger Fleckenstein; Lorenzo Galli; Stefan P. Hau-Riege; Stephan Kassemeyer; Hartawan Laksmono; Mengning Liang; Lukas Lomb; Stefano Marchesini; Andrew V. Martin; Marc Messerschmidt; Despina Milathianaki; Karol Nass; Alexandra Ros; Shatabdi Roy-Chowdhury; Kevin Schmidt; Marvin Seibert; Jan Steinbrener; Francesco Stellato; Lifen Yan; Chunhong Yoon; Thomas Moore; Ana Moore; Yulia Pushkar; Garth J. Williams; Sébastien Boutet; R. Bruce Doak; Uwe Weierstall; Matthias Frank; Henry N. Chapman; John Spence; Petra Fromme

doi:10.1038/nature13453

Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser

Christopher Kupitz, Shibom Basu, Ingo Grotjohann, Raimund Fromme, Nadia Zatsepin, Kimberly N. Rendek, Mark S. Hunter, Robert L. Shoeman, Thomas A. White, Dingjie Wang, Daniel James, Jay How Yang, Danielle E. Cobb, Brenda Reeder, Raymond G. Sierra, Haiguang Liu, Anton Barty, Andrew L. Aquila, Daniel Deponte, Richard KirianSadia Bari, Jesse J. Bergkamp, Kenneth R. Beyerlein, Michael J. Bogan, Carl Caleman, Tzu Chiao Chao, Chelsie E. Conrad, Katherine M. Davis, Holger Fleckenstein, Lorenzo Galli, Stefan P. Hau-Riege, Stephan Kassemeyer, Hartawan Laksmono, Mengning Liang, Lukas Lomb, Stefano Marchesini, Andrew V. Martin, Marc Messerschmidt, Despina Milathianaki, Karol Nass, Alexandra Ros, Shatabdi Roy-Chowdhury, Kevin Schmidt, Marvin Seibert, Jan Steinbrener, Francesco Stellato, Lifen Yan, Chunhong Yoon, Thomas Moore, Ana Moore, Yulia Pushkar, Garth J. Williams, Sébastien Boutet, R. Bruce Doak, Uwe Weierstall, Matthias Frank, Henry N. Chapman, John Spence, Petra Fromme

Research output: Contribution to journal › Letter › peer-review

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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 atmosphere. 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 developed 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 Mn₃CaO_x cubane in the S₂ to S₃transition, as predicted by spectroscopic and computational studies. This work shows the great potential for time-resolved serial femtosecond crystallography for investigation of catalytic processes in biomolecules.

Original language	English (US)
Pages (from-to)	261-265
Number of pages	5
Journal	Nature
Volume	513
Issue number	7517
DOIs	https://doi.org/10.1038/nature13453
State	Published - 2014

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Kupitz, C., Basu, S., Grotjohann, I., Fromme, R., Zatsepin, N., Rendek, K. N., Hunter, M. S., Shoeman, R. L., White, T. A., Wang, D., James, D., Yang, J. H., Cobb, D. E., Reeder, B., Sierra, R. G., Liu, H., Barty, A., Aquila, A. L., Deponte, D., ... Fromme, P. (2014). Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser. Nature, 513(7517), 261-265. https://doi.org/10.1038/nature13453

Kupitz, C, Basu, S, Grotjohann, I, Fromme, R, Zatsepin, N, Rendek, KN, Hunter, MS, Shoeman, RL, White, TA, Wang, D, James, D, Yang, JH, Cobb, DE, Reeder, B, Sierra, RG, Liu, H, Barty, A, Aquila, AL, Deponte, D, Kirian, R, Bari, S, Bergkamp, JJ, Beyerlein, KR, Bogan, MJ, Caleman, C, Chao, TC, Conrad, CE, Davis, KM, Fleckenstein, H, Galli, L, Hau-Riege, SP, Kassemeyer, S, Laksmono, H, Liang, M, Lomb, L, Marchesini, S, Martin, AV, Messerschmidt, M, Milathianaki, D, Nass, K, Ros, A, Roy-Chowdhury, S, Schmidt, K, Seibert, M, Steinbrener, J, Stellato, F, Yan, L, Yoon, C, Moore, T , Moore, A, Pushkar, Y, Williams, GJ, Boutet, S, Doak, RB, Weierstall, U, Frank, M, Chapman, HN, Spence, J & Fromme, P 2014, 'Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser', Nature, vol. 513, no. 7517, pp. 261-265. https://doi.org/10.1038/nature13453

@article{7a8e12419fcd4229a14689e6428da4ff,

title = "Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser",

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{\textquoteright}s oxygenic atmosphere. 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 developed 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 {\AA} 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 {\textquoteleft}dangler{\textquoteright} Mn) and the Mn3CaOx cubane in the S2 to S3transition, as predicted by spectroscopic and computational studies. This work shows the great potential for time-resolved serial femtosecond crystallography for investigation of catalytic processes in biomolecules.",

author = "Christopher Kupitz and Shibom Basu and Ingo Grotjohann and Raimund Fromme and Nadia Zatsepin and Rendek, {Kimberly N.} and Hunter, {Mark S.} and Shoeman, {Robert L.} and White, {Thomas A.} and Dingjie Wang and Daniel James and Yang, {Jay How} and Cobb, {Danielle E.} and Brenda Reeder and Sierra, {Raymond G.} and Haiguang Liu and Anton Barty and Aquila, {Andrew L.} and Daniel Deponte and Richard Kirian and Sadia Bari and Bergkamp, {Jesse J.} and Beyerlein, {Kenneth R.} and Bogan, {Michael J.} and Carl Caleman and Chao, {Tzu Chiao} and Conrad, {Chelsie E.} and Davis, {Katherine M.} and Holger Fleckenstein and Lorenzo Galli and Hau-Riege, {Stefan P.} and Stephan Kassemeyer and Hartawan Laksmono and Mengning Liang and Lukas Lomb and Stefano Marchesini and Martin, {Andrew V.} and Marc Messerschmidt and Despina Milathianaki and Karol Nass and Alexandra Ros and Shatabdi Roy-Chowdhury and Kevin Schmidt and Marvin Seibert and Jan Steinbrener and Francesco Stellato and Lifen Yan and Chunhong Yoon and Thomas Moore and Ana Moore and Yulia Pushkar and Williams, {Garth J.} and S{\'e}bastien Boutet and Doak, {R. Bruce} and Uwe Weierstall and Matthias Frank and Chapman, {Henry N.} and John Spence and Petra Fromme",

note = "Funding Information: 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 {\textquoteleft}Inflammation at Interfaces{\textquoteright} (EXC 306) and the {\textquoteleft}Center for Ultrafast Imaging{\textquoteright}; 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 ligandmutagenesis. WethankJ. 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. Publisher Copyright: {\textcopyright} 2014 Macmillan Publishers Limited. All rights reserved.",

year = "2014",

doi = "10.1038/nature13453",

language = "English (US)",

volume = "513",

pages = "261--265",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Publishing Group",

number = "7517",

}

TY - JOUR

T1 - Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser

AU - Kupitz, Christopher

AU - Basu, Shibom

AU - Grotjohann, Ingo

AU - Fromme, Raimund

AU - Zatsepin, Nadia

AU - Rendek, Kimberly N.

AU - Hunter, Mark S.

AU - Shoeman, Robert L.

AU - White, Thomas A.

AU - Wang, Dingjie

AU - James, Daniel

AU - Yang, Jay How

AU - Cobb, Danielle E.

AU - Reeder, Brenda

AU - Sierra, Raymond G.

AU - Liu, Haiguang

AU - Barty, Anton

AU - Aquila, Andrew L.

AU - Deponte, Daniel

AU - Kirian, Richard

AU - Bari, Sadia

AU - Bergkamp, Jesse J.

AU - Beyerlein, Kenneth R.

AU - Bogan, Michael J.

AU - Caleman, Carl

AU - Chao, Tzu Chiao

AU - Conrad, Chelsie E.

AU - Davis, Katherine M.

AU - Fleckenstein, Holger

AU - Galli, Lorenzo

AU - Hau-Riege, Stefan P.

AU - Kassemeyer, Stephan

AU - Laksmono, Hartawan

AU - Liang, Mengning

AU - Lomb, Lukas

AU - Marchesini, Stefano

AU - Martin, Andrew V.

AU - Messerschmidt, Marc

AU - Milathianaki, Despina

AU - Nass, Karol

AU - Ros, Alexandra

AU - Roy-Chowdhury, Shatabdi

AU - Schmidt, Kevin

AU - Seibert, Marvin

AU - Steinbrener, Jan

AU - Stellato, Francesco

AU - Yan, Lifen

AU - Yoon, Chunhong

AU - Moore, Thomas

AU - Moore, Ana

AU - Pushkar, Yulia

AU - Williams, Garth J.

AU - Boutet, Sébastien

AU - Doak, R. Bruce

AU - Weierstall, Uwe

AU - Frank, Matthias

AU - Chapman, Henry N.

AU - Spence, John

AU - Fromme, Petra

N1 - Funding Information: 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 ligandmutagenesis. WethankJ. 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. Publisher Copyright: © 2014 Macmillan Publishers Limited. All rights reserved.

PY - 2014

Y1 - 2014

N2 - 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 atmosphere. 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 developed 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 S3transition, as predicted by spectroscopic and computational studies. This work shows the great potential for time-resolved serial femtosecond crystallography for investigation of catalytic processes in biomolecules.

AB - 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 atmosphere. 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 developed 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 S3transition, as predicted by spectroscopic and computational studies. This work shows the great potential for time-resolved serial femtosecond crystallography for investigation of catalytic processes in biomolecules.

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U2 - 10.1038/nature13453

DO - 10.1038/nature13453

M3 - Letter

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AN - SCOPUS:84906087743

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VL - 513

SP - 261

EP - 265

JO - Nature

JF - Nature

IS - 7517

ER -

Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser

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