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

Christopher Kupitz, Shibom Basu, Ingo Grotjohann, Raimund Fromme, Nadia A. 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 A. 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 A Moore, Ana L Moore, Yulia Pushkar, Garth J. Williams, Sébastien Boutet, R. Bruce Doak, Uwe Weierstall, Matthias Frank, Henry N. Chapman, John C H Spence, Petra Fromme

Research output: Contribution to journalArticle

248 Citations (Scopus)

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 Mn3CaOx cubane in the S2 to S3 transition, 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 languageEnglish
Pages (from-to)261-265
Number of pages5
JournalNature
Volume513
Issue number7517
DOIs
Publication statusPublished - Sep 11 2014

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Crystallography
Photosystem II Protein Complex
Lasers
X-Rays
Photosynthesis
Oxygen
Light
Electrons
Photosystem I Protein Complex
Water
Sunlight
Cyanobacteria
Atmosphere
Membrane Proteins
Metals
Proteins

ASJC Scopus subject areas

  • General

Cite this

Kupitz, C., Basu, S., Grotjohann, I., Fromme, R., Zatsepin, N. A., Rendek, K. N., ... 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

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

In: Nature, Vol. 513, No. 7517, 11.09.2014, p. 261-265.

Research output: Contribution to journalArticle

Kupitz, C, Basu, S, Grotjohann, I, Fromme, R, Zatsepin, NA, 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, RA, 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, TA, Moore, AL, Pushkar, Y, Williams, GJ, Boutet, S, Doak, RB, Weierstall, U, Frank, M, Chapman, HN, Spence, JCH & 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
Kupitz C, Basu S, Grotjohann I, Fromme R, Zatsepin NA, Rendek KN et al. Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser. Nature. 2014 Sep 11;513(7517):261-265. https://doi.org/10.1038/nature13453
Kupitz, Christopher ; Basu, Shibom ; Grotjohann, Ingo ; Fromme, Raimund ; Zatsepin, Nadia A. ; Rendek, Kimberly N. ; Hunter, Mark S. ; Shoeman, Robert L. ; White, Thomas A. ; Wang, Dingjie ; James, Daniel ; Yang, Jay How ; Cobb, Danielle E. ; Reeder, Brenda ; Sierra, Raymond G. ; Liu, Haiguang ; Barty, Anton ; Aquila, Andrew L. ; Deponte, Daniel ; Kirian, Richard A. ; Bari, Sadia ; Bergkamp, Jesse J. ; Beyerlein, Kenneth R. ; Bogan, Michael J. ; Caleman, Carl ; Chao, Tzu Chiao ; Conrad, Chelsie E. ; Davis, Katherine M. ; Fleckenstein, Holger ; Galli, Lorenzo ; Hau-Riege, Stefan P. ; Kassemeyer, Stephan ; Laksmono, Hartawan ; Liang, Mengning ; Lomb, Lukas ; Marchesini, Stefano ; Martin, Andrew V. ; Messerschmidt, Marc ; Milathianaki, Despina ; Nass, Karol ; Ros, Alexandra ; Roy-Chowdhury, Shatabdi ; Schmidt, Kevin ; Seibert, Marvin ; Steinbrener, Jan ; Stellato, Francesco ; Yan, Lifen ; Yoon, Chunhong ; Moore, Thomas A ; Moore, Ana L ; Pushkar, Yulia ; Williams, Garth J. ; Boutet, Sébastien ; Doak, R. Bruce ; Weierstall, Uwe ; Frank, Matthias ; Chapman, Henry N. ; Spence, John C H ; Fromme, Petra. / Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser. In: Nature. 2014 ; Vol. 513, No. 7517. pp. 261-265.
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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 A.

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 A.

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

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AU - Moore, Ana L

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 C H

AU - Fromme, Petra

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