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

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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 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.

Original languageEnglish
Pages (from-to)261-265
Number of pages5
JournalNature
Volume513
Issue number7517
DOIs
Publication statusPublished - Jan 1 2014

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