Membrane protein megahertz crystallography at the European XFEL

Chris Gisriel, Jesse Coe, Romain Letrun, Oleksandr M. Yefanov, Cesar Luna-Chavez, Natasha E. Stander, Stella Lisova, Valerio Mariani, Manuela Kuhn, Steve Aplin, Thomas D. Grant, Katerina Dörner, Tokushi Sato, Austin Echelmeier, Jorvani Cruz Villarreal, Mark S. Hunter, Max O. Wiedorn, Juraj Knoska, Victoria Mazalova, Shatabdi Roy-Chowdhury, Jay-How Yang, Alex Jones, Richard Bean, Johan Bielecki, Yoonhee Kim, Grant Mills, Britta Weinhausen, Jose D. Meza, Nasser Al-Qudami, Saša Bajt, Gerrit Brehm, Sabine Botha, Djelloul Boukhelef, Sandor Brockhauser, Barry D. Bruce, Matthew A. Coleman, Cyril Danilevski, Erin Discianno, Zachary Dobson, Hans Fangohr, Jose M. Martin-Garcia, Yaroslav Gevorkov, Steffen Hauf, Ahmad Hosseinizadeh, Friederike Januschek, Gihan K. Ketawala, Christopher Kupitz, Luis Maia, Maurizio Manetti, Marc Messerschmidt, Thomas Michelat, Jyotirmoy Mondal, Abbas Ourmazd, Gianpietro Previtali, Iosifina Sarrou, Silvan Schön, Peter Schwander, Megan L. Shelby, Alessandro Silenzi, Jolanta Sztuk-Dambietz, Janusz Szuba, Monica Turcato, Thomas A. White, Krzysztof Wrona, Chen Xu, Mohamed H. Abdellatif, James D. Zook, John C. H. Spence, Henry N. Chapman, Anton Barty, Richard A. Kirian, Matthias Frank, Alexandra Ros, Marius Schmidt, Raimund Fromme, Adrian P. Mancuso, Petra Fromme () and Nadia A. Zatsepin ()
Additional contact information
Chris Gisriel: Biodesign Center for Applied Structural Discovery, Arizona State University
Jesse Coe: Biodesign Center for Applied Structural Discovery, Arizona State University
Romain Letrun: European XFEL GmbH
Oleksandr M. Yefanov: Center for Free-Electron Laser Science, Deutsches Elektronen-Synchrotron
Cesar Luna-Chavez: Biodesign Center for Applied Structural Discovery, Arizona State University
Natasha E. Stander: Biodesign Center for Applied Structural Discovery, Arizona State University
Stella Lisova: Biodesign Center for Applied Structural Discovery, Arizona State University
Valerio Mariani: Center for Free-Electron Laser Science, Deutsches Elektronen-Synchrotron
Manuela Kuhn: Center for Free-Electron Laser Science, Deutsches Elektronen-Synchrotron
Steve Aplin: Center for Free-Electron Laser Science, Deutsches Elektronen-Synchrotron
Thomas D. Grant: Hauptman-Woodward Institute
Katerina Dörner: European XFEL GmbH
Tokushi Sato: European XFEL GmbH
Austin Echelmeier: Biodesign Center for Applied Structural Discovery, Arizona State University
Jorvani Cruz Villarreal: Biodesign Center for Applied Structural Discovery, Arizona State University
Mark S. Hunter: Linac Coherent Light Source, SLAC National Accelerator Laboratory
Max O. Wiedorn: Center for Free-Electron Laser Science, Deutsches Elektronen-Synchrotron
Juraj Knoska: Center for Free-Electron Laser Science, Deutsches Elektronen-Synchrotron
Victoria Mazalova: Center for Free-Electron Laser Science, Deutsches Elektronen-Synchrotron
Shatabdi Roy-Chowdhury: Biodesign Center for Applied Structural Discovery, Arizona State University
Jay-How Yang: Biodesign Center for Applied Structural Discovery, Arizona State University
Alex Jones: Biodesign Center for Applied Structural Discovery, Arizona State University
Richard Bean: European XFEL GmbH
Johan Bielecki: European XFEL GmbH
Yoonhee Kim: European XFEL GmbH
Grant Mills: European XFEL GmbH
Britta Weinhausen: European XFEL GmbH
Jose D. Meza: European XFEL GmbH
Nasser Al-Qudami: European XFEL GmbH
Saša Bajt: Deutsches Elektronen-Synchrotron
Gerrit Brehm: Biodesign Center for Applied Structural Discovery, Arizona State University
Sabine Botha: Department of Physics, Arizona State University
Djelloul Boukhelef: European XFEL GmbH
Sandor Brockhauser: European XFEL GmbH
Barry D. Bruce: Department of Biochemistry & Cellular and Molecular Biology, University of Tennessee at Knoxville
Matthew A. Coleman: Lawrence Livermore National Laboratory
Cyril Danilevski: European XFEL GmbH
Erin Discianno: Biodesign Center for Applied Structural Discovery, Arizona State University
Zachary Dobson: Biodesign Center for Applied Structural Discovery, Arizona State University
Hans Fangohr: European XFEL GmbH
Jose M. Martin-Garcia: Biodesign Center for Applied Structural Discovery, Arizona State University
Yaroslav Gevorkov: Center for Free-Electron Laser Science, Deutsches Elektronen-Synchrotron
Steffen Hauf: European XFEL GmbH
Ahmad Hosseinizadeh: Department of Physics, University of Wisconsin-Milwaukee
Friederike Januschek: European XFEL GmbH
Gihan K. Ketawala: Biodesign Center for Applied Structural Discovery, Arizona State University
Christopher Kupitz: Linac Coherent Light Source, SLAC National Accelerator Laboratory
Luis Maia: European XFEL GmbH
Maurizio Manetti: European XFEL GmbH
Marc Messerschmidt: Biodesign Center for Applied Structural Discovery, Arizona State University
Thomas Michelat: European XFEL GmbH
Jyotirmoy Mondal: Department of Biochemistry & Cellular and Molecular Biology, University of Tennessee at Knoxville
Abbas Ourmazd: Department of Physics, University of Wisconsin-Milwaukee
Gianpietro Previtali: European XFEL GmbH
Iosifina Sarrou: Center for Free-Electron Laser Science, Deutsches Elektronen-Synchrotron
Silvan Schön: Center for Free-Electron Laser Science, Deutsches Elektronen-Synchrotron
Peter Schwander: Department of Physics, University of Wisconsin-Milwaukee
Megan L. Shelby: Lawrence Livermore National Laboratory
Alessandro Silenzi: European XFEL GmbH
Jolanta Sztuk-Dambietz: European XFEL GmbH
Janusz Szuba: European XFEL GmbH
Monica Turcato: European XFEL GmbH
Thomas A. White: Center for Free-Electron Laser Science, Deutsches Elektronen-Synchrotron
Krzysztof Wrona: European XFEL GmbH
Chen Xu: European XFEL GmbH
Mohamed H. Abdellatif: Center for Free-Electron Laser Science, Deutsches Elektronen-Synchrotron
James D. Zook: Biodesign Center for Applied Structural Discovery, Arizona State University
John C. H. Spence: Biodesign Center for Applied Structural Discovery, Arizona State University
Henry N. Chapman: Center for Free-Electron Laser Science, Deutsches Elektronen-Synchrotron
Anton Barty: Center for Free-Electron Laser Science, Deutsches Elektronen-Synchrotron
Richard A. Kirian: Biodesign Center for Applied Structural Discovery, Arizona State University
Matthias Frank: Lawrence Livermore National Laboratory
Alexandra Ros: Biodesign Center for Applied Structural Discovery, Arizona State University
Marius Schmidt: Department of Physics, University of Wisconsin-Milwaukee
Raimund Fromme: Biodesign Center for Applied Structural Discovery, Arizona State University
Adrian P. Mancuso: European XFEL GmbH
Petra Fromme: Biodesign Center for Applied Structural Discovery, Arizona State University
Nadia A. Zatsepin: Biodesign Center for Applied Structural Discovery, Arizona State University

Nature Communications, 2019, vol. 10, issue 1, 1-11

Abstract: Abstract The world’s first superconducting megahertz repetition rate hard X-ray free-electron laser (XFEL), the European XFEL, began operation in 2017, featuring a unique pulse train structure with 886 ns between pulses. With its rapid pulse rate, the European XFEL may alleviate some of the increasing demand for XFEL beamtime, particularly for membrane protein serial femtosecond crystallography (SFX), leveraging orders-of-magnitude faster data collection. Here, we report the first membrane protein megahertz SFX experiment, where we determined a 2.9 Å-resolution SFX structure of the large membrane protein complex, Photosystem I, a > 1 MDa complex containing 36 protein subunits and 381 cofactors. We address challenges to megahertz SFX for membrane protein complexes, including growth of large quantities of crystals and the large molecular and unit cell size that influence data collection and analysis. The results imply that megahertz crystallography could have an important impact on structure determination of large protein complexes with XFELs.

Date: 2019
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DOI: 10.1038/s41467-019-12955-3

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