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Title: Membrane protein megahertz crystallography at the European XFEL

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.

Authors:
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Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States); Univ. of Wisconsin, Milwaukee, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); European Research Council (ERC); German Research Foundation (DFG); German Federal Ministry of Education and Research (BMBF); Australian Research Council (ARC)
Contributing Org.:
European XFEL Group
OSTI Identifier:
1596363
Alternate Identifier(s):
OSTI ID: 1598207
Grant/Contract Number:  
AC02-76SF00515; SC0002164; SC0010575; R01GM095583; 609920; DFG-EXC1074; 05K18CHA; AC52-07NA27344; R01GM117342; CE140100011
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
75 CONDENSED MATTER PHYSICS, SUPERCONDUCTIVITY AND SUPERFLUIDITY

Citation Formats

Gisriel, Chris, Coe, Jesse, Letrun, Romain, Yefanov, Oleksandr M., Luna-Chavez, Cesar, Stander, Natasha E., Lisova, Stella, Mariani, Valerio, Kuhn, Manuela, Aplin, Steve, Grant, Thomas D., Dörner, Katerina, Sato, Tokushi, Echelmeier, Austin, Cruz Villarreal, Jorvani, Hunter, Mark S., Wiedorn, Max O., Knoska, Juraj, Mazalova, Victoria, Roy-Chowdhury, Shatabdi, Yang, Jay-How, Jones, Alex, Bean, Richard, Bielecki, Johan, Kim, Yoonhee, Mills, Grant, Weinhausen, Britta, Meza, Jose D., Al-Qudami, Nasser, Bajt, Saša, Brehm, Gerrit, Botha, Sabine, Boukhelef, Djelloul, Brockhauser, Sandor, Bruce, Barry D., Coleman, Matthew A., Danilevski, Cyril, Discianno, Erin, Dobson, Zachary, Fangohr, Hans, Martin-Garcia, Jose M., Gevorkov, Yaroslav, Hauf, Steffen, Hosseinizadeh, Ahmad, Januschek, Friederike, Ketawala, Gihan K., Kupitz, Christopher, Maia, Luis, Manetti, Maurizio, Messerschmidt, Marc, Michelat, Thomas, Mondal, Jyotirmoy, Ourmazd, Abbas, Previtali, Gianpietro, Sarrou, Iosifina, Schön, Silvan, Schwander, Peter, Shelby, Megan L., Silenzi, Alessandro, Sztuk-Dambietz, Jolanta, Szuba, Janusz, Turcato, Monica, White, Thomas A., Wrona, Krzysztof, Xu, Chen, Abdellatif, Mohamed H., Zook, James D., Spence, John C. H., Chapman, Henry N., Barty, Anton, Kirian, Richard A., Frank, Matthias, Ros, Alexandra, Schmidt, Marius, Fromme, Raimund, Mancuso, Adrian P., Fromme, Petra, and Zatsepin, Nadia A. Membrane protein megahertz crystallography at the European XFEL. United States: N. p., 2019. Web. doi:10.1038/s41467-019-12955-3.
Gisriel, Chris, Coe, Jesse, Letrun, Romain, Yefanov, Oleksandr M., Luna-Chavez, Cesar, Stander, Natasha E., Lisova, Stella, Mariani, Valerio, Kuhn, Manuela, Aplin, Steve, Grant, Thomas D., Dörner, Katerina, Sato, Tokushi, Echelmeier, Austin, Cruz Villarreal, Jorvani, Hunter, Mark S., Wiedorn, Max O., Knoska, Juraj, Mazalova, Victoria, Roy-Chowdhury, Shatabdi, Yang, Jay-How, Jones, Alex, Bean, Richard, Bielecki, Johan, Kim, Yoonhee, Mills, Grant, Weinhausen, Britta, Meza, Jose D., Al-Qudami, Nasser, Bajt, Saša, Brehm, Gerrit, Botha, Sabine, Boukhelef, Djelloul, Brockhauser, Sandor, Bruce, Barry D., Coleman, Matthew A., Danilevski, Cyril, Discianno, Erin, Dobson, Zachary, Fangohr, Hans, Martin-Garcia, Jose M., Gevorkov, Yaroslav, Hauf, Steffen, Hosseinizadeh, Ahmad, Januschek, Friederike, Ketawala, Gihan K., Kupitz, Christopher, Maia, Luis, Manetti, Maurizio, Messerschmidt, Marc, Michelat, Thomas, Mondal, Jyotirmoy, Ourmazd, Abbas, Previtali, Gianpietro, Sarrou, Iosifina, Schön, Silvan, Schwander, Peter, Shelby, Megan L., Silenzi, Alessandro, Sztuk-Dambietz, Jolanta, Szuba, Janusz, Turcato, Monica, White, Thomas A., Wrona, Krzysztof, Xu, Chen, Abdellatif, Mohamed H., Zook, James D., Spence, John C. H., Chapman, Henry N., Barty, Anton, Kirian, Richard A., Frank, Matthias, Ros, Alexandra, Schmidt, Marius, Fromme, Raimund, Mancuso, Adrian P., Fromme, Petra, & Zatsepin, Nadia A. Membrane protein megahertz crystallography at the European XFEL. United States. doi:https://doi.org/10.1038/s41467-019-12955-3
Gisriel, Chris, Coe, Jesse, Letrun, Romain, Yefanov, Oleksandr M., Luna-Chavez, Cesar, Stander, Natasha E., Lisova, Stella, Mariani, Valerio, Kuhn, Manuela, Aplin, Steve, Grant, Thomas D., Dörner, Katerina, Sato, Tokushi, Echelmeier, Austin, Cruz Villarreal, Jorvani, Hunter, Mark S., Wiedorn, Max O., Knoska, Juraj, Mazalova, Victoria, Roy-Chowdhury, Shatabdi, Yang, Jay-How, Jones, Alex, Bean, Richard, Bielecki, Johan, Kim, Yoonhee, Mills, Grant, Weinhausen, Britta, Meza, Jose D., Al-Qudami, Nasser, Bajt, Saša, Brehm, Gerrit, Botha, Sabine, Boukhelef, Djelloul, Brockhauser, Sandor, Bruce, Barry D., Coleman, Matthew A., Danilevski, Cyril, Discianno, Erin, Dobson, Zachary, Fangohr, Hans, Martin-Garcia, Jose M., Gevorkov, Yaroslav, Hauf, Steffen, Hosseinizadeh, Ahmad, Januschek, Friederike, Ketawala, Gihan K., Kupitz, Christopher, Maia, Luis, Manetti, Maurizio, Messerschmidt, Marc, Michelat, Thomas, Mondal, Jyotirmoy, Ourmazd, Abbas, Previtali, Gianpietro, Sarrou, Iosifina, Schön, Silvan, Schwander, Peter, Shelby, Megan L., Silenzi, Alessandro, Sztuk-Dambietz, Jolanta, Szuba, Janusz, Turcato, Monica, White, Thomas A., Wrona, Krzysztof, Xu, Chen, Abdellatif, Mohamed H., Zook, James D., Spence, John C. H., Chapman, Henry N., Barty, Anton, Kirian, Richard A., Frank, Matthias, Ros, Alexandra, Schmidt, Marius, Fromme, Raimund, Mancuso, Adrian P., Fromme, Petra, and Zatsepin, Nadia A. Mon . "Membrane protein megahertz crystallography at the European XFEL". United States. doi:https://doi.org/10.1038/s41467-019-12955-3. https://www.osti.gov/servlets/purl/1596363.
@article{osti_1596363,
title = {Membrane protein megahertz crystallography at the European XFEL},
author = {Gisriel, Chris and Coe, Jesse and Letrun, Romain and Yefanov, Oleksandr M. and Luna-Chavez, Cesar and Stander, Natasha E. and Lisova, Stella and Mariani, Valerio and Kuhn, Manuela and Aplin, Steve and Grant, Thomas D. and Dörner, Katerina and Sato, Tokushi and Echelmeier, Austin and Cruz Villarreal, Jorvani and Hunter, Mark S. and Wiedorn, Max O. and Knoska, Juraj and Mazalova, Victoria and Roy-Chowdhury, Shatabdi and Yang, Jay-How and Jones, Alex and Bean, Richard and Bielecki, Johan and Kim, Yoonhee and Mills, Grant and Weinhausen, Britta and Meza, Jose D. and Al-Qudami, Nasser and Bajt, Saša and Brehm, Gerrit and Botha, Sabine and Boukhelef, Djelloul and Brockhauser, Sandor and Bruce, Barry D. and Coleman, Matthew A. and Danilevski, Cyril and Discianno, Erin and Dobson, Zachary and Fangohr, Hans and Martin-Garcia, Jose M. and Gevorkov, Yaroslav and Hauf, Steffen and Hosseinizadeh, Ahmad and Januschek, Friederike and Ketawala, Gihan K. and Kupitz, Christopher and Maia, Luis and Manetti, Maurizio and Messerschmidt, Marc and Michelat, Thomas and Mondal, Jyotirmoy and Ourmazd, Abbas and Previtali, Gianpietro and Sarrou, Iosifina and Schön, Silvan and Schwander, Peter and Shelby, Megan L. and Silenzi, Alessandro and Sztuk-Dambietz, Jolanta and Szuba, Janusz and Turcato, Monica and White, Thomas A. and Wrona, Krzysztof and Xu, Chen and Abdellatif, Mohamed H. and Zook, James D. and Spence, John C. H. and Chapman, Henry N. and Barty, Anton and Kirian, Richard A. and Frank, Matthias and Ros, Alexandra and Schmidt, Marius and Fromme, Raimund and Mancuso, Adrian P. and Fromme, Petra and Zatsepin, Nadia A.},
abstractNote = {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.},
doi = {10.1038/s41467-019-12955-3},
journal = {Nature Communications},
number = 1,
volume = 10,
place = {United States},
year = {2019},
month = {11}
}

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    Works referencing / citing this record:

    Electric Triggering for Enhanced Control of Droplet Generation
    journal, June 2019


    Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein
    journal, December 2014


    Structures of riboswitch RNA reaction states by mix-and-inject XFEL serial crystallography
    journal, November 2016

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    PHENIX: a comprehensive Python-based system for macromolecular structure solution
    journal, January 2010

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    • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
    • DOI: 10.1107/s0907444909052925

    Lipidic cubic phase injector facilitates membrane protein serial femtosecond crystallography
    journal, February 2014

    • Weierstall, Uwe; James, Daniel; Wang, Chong
    • Nature Communications, Vol. 5, Issue 1
    • DOI: 10.1038/ncomms4309

    The Adaptive Gain Integrating Pixel Detector at the European XFEL
    journal, January 2019

    • Allahgholi, Aschkan; Becker, Julian; Delfs, Annette
    • Journal of Synchrotron Radiation, Vol. 26, Issue 1
    • DOI: 10.1107/s1600577518016077

    The adaptive gain integrating pixel detector AGIPD a detector for the European XFEL
    journal, May 2011

    • Henrich, B.; Becker, J.; Dinapoli, R.
    • Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment, Vol. 633
    • DOI: 10.1016/j.nima.2010.06.107

    Toward structure determination using membrane–protein nanocrystals and microcrystals
    journal, December 2011


    High-Resolution Protein Structure Determination by Serial Femtosecond Crystallography
    journal, May 2012


    Megahertz serial crystallography
    journal, October 2018


    Molecular mechanism of photosystem I assembly in oxygenic organisms
    journal, September 2015

    • Yang, Huixia; Liu, Jun; Wen, Xiaogang
    • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 9
    • DOI: 10.1016/j.bbabio.2014.12.011

    Selective Detection of Protein Crystals by Second Harmonic Microscopy
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    • Wampler, Ronald D.; Kissick, David J.; Dehen, Christopher J.
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    • Krauss, Norbert; Hinrichs, Winfried; Witt, Ingrid
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    • DOI: 10.1038/361326a0

    Structural enzymology using X-ray free electron lasers
    journal, December 2016

    • Kupitz, Christopher; Olmos, Jose L.; Holl, Mark
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