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'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.
authors.affiliation: 1] Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA [2].
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authors.lastname: Kupitz
authors.affiliation: 1] Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA [2].
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authors.lastname: Basu
authors.affiliation: Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA.
authors.forename: Ingo
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authors.lastname: Grotjohann
authors.affiliation: Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA.
authors.forename: Raimund
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authors.lastname: Fromme
authors.affiliation: Department of Physics, Arizona State University, Tempe, Arizona 85287, USA.
authors.forename: Nadia A
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authors.lastname: Zatsepin
authors.affiliation: Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA.
authors.forename: Kimberly N
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authors.lastname: Rendek
authors.affiliation: 1] Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA [2] Lawrence Livermore National Laboratory, Livermore, California 94550, USA.
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authors.affiliation: Max-Planck-Institut für medizinische Forschung, Jahnstrasse 29, 69120 Heidelberg, Germany.
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authors.lastname: Shoeman
authors.affiliation: Center for Free-Electron Laser Science, DESY, Notkestrasse 85, 22607 Hamburg, Germany.
authors.forename: Thomas A
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authors.lastname: White
authors.affiliation: Department of Physics, Arizona State University, Tempe, Arizona 85287, USA.
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authors.affiliation: Department of Physics, Arizona State University, Tempe, Arizona 85287, USA.
authors.forename: Daniel
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authors.affiliation: Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA.
authors.forename: Jay-How
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authors.affiliation: Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA.
authors.forename: Danielle E
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authors.affiliation: Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA.
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authors.affiliation: Stanford PULSE Institute, SLAC National Accelerator Laboratory, 2575 Sand Hill Road, Menlo Park, California 94025, USA.
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authors.lastname: Sierra
authors.affiliation: Department of Physics, Arizona State University, Tempe, Arizona 85287, USA.
authors.forename: Haiguang
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authors.affiliation: Center for Free-Electron Laser Science, DESY, Notkestrasse 85, 22607 Hamburg, Germany.
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authors.affiliation: 1] Department of Physics, Arizona State University, Tempe, Arizona 85287, USA [2] Center for Free-Electron Laser Science, DESY, Notkestrasse 85, 22607 Hamburg, Germany.
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authors.affiliation: Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA.
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authors.affiliation: Center for Free-Electron Laser Science, DESY, Notkestrasse 85, 22607 Hamburg, Germany.
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authors.affiliation: Stanford PULSE Institute, SLAC National Accelerator Laboratory, 2575 Sand Hill Road, Menlo Park, California 94025, USA.
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authors.affiliation: 1] Center for Free-Electron Laser Science, DESY, Notkestrasse 85, 22607 Hamburg, Germany [2] Department of Physics and Astronomy, Uppsala University, Regementsvägen 1, SE-752 37 Uppsala, Sweden.
authors.forename: Carl
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authors.affiliation: 1] Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA [2] University of Regina, 3737 Wascana Pkwy Regina, Saskatchewan S4S 0A2, Canada.
authors.forename: Tzu-Chiao
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authors.affiliation: Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA.
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authors.initials: CE
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authors.affiliation: Department of Physics, Purdue University, 525 Northwestern Avenue, West Lafayette, Indiana 47907, USA.
authors.forename: Katherine M
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authors.affiliation: Center for Free-Electron Laser Science, DESY, Notkestrasse 85, 22607 Hamburg, Germany.
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authors.affiliation: 1] Center for Free-Electron Laser Science, DESY, Notkestrasse 85, 22607 Hamburg, Germany [2] University of Hamburg, Luruper Chaussee 149, 22761 Hamburg, Germany.
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authors.affiliation: Lawrence Livermore National Laboratory, Livermore, California 94550, USA.
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authors.affiliation: Center for Free-Electron Laser Science, DESY, Notkestrasse 85, 22607 Hamburg, Germany.
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authors.affiliation: Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA.
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authors.affiliation: Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA.
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authors.affiliation: Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA.
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authors.affiliation: Department of Physics, Arizona State University, Tempe, Arizona 85287, USA.
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authors.affiliation: Department of Physics, Arizona State University, Tempe, Arizona 85287, USA.
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authors.affiliation: Department of Physics, Arizona State University, Tempe, Arizona 85287, USA.
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authors.affiliation: Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA.
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mesh_terms: D018360:Crystallography, X-Ray; D000458:Cyanobacteria / Q000737:chemistry*; D008958:Models, Molecular; D045332:Photosystem II Protein Complex / Q000737:chemistry*; D017434:Protein Structure, Tertiary
chemical_list: D045332:Photosystem II Protein Complex