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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); Univ. of Wisconsin, Milwaukee, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
Contributing Org.:
European XFEL Group
OSTI Identifier:
1596363
Alternate Identifier(s):
OSTI ID: 1598207; OSTI ID: 1598409
Grant/Contract Number:  
AC02-76SF00515; SC0002164
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

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: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: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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    • Yang, Huixia; Liu, Jun; Wen, Xiaogang
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    Electric Triggering for Enhanced Control of Droplet Generation
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    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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    Structures of riboswitch RNA reaction states by mix-and-inject XFEL serial crystallography
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    Lipidic cubic phase injector facilitates membrane protein serial femtosecond crystallography
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    Megahertz data collection from protein microcrystals at an X-ray free-electron laser
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    • Nature Communications, Vol. 9, Issue 1
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    Megahertz serial crystallography
    journal, October 2018


    Double-flow focused liquid injector for efficient serial femtosecond crystallography
    journal, March 2017

    • Oberthuer, Dominik; Knoška, Juraj; Wiedorn, Max O.
    • Scientific Reports, Vol. 7, Issue 1
    • DOI: 10.1038/srep44628

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

    • Kupitz, Christopher; Olmos, Jose L.; Holl, Mark
    • Structural Dynamics, Vol. 4, Issue 4
    • DOI: 10.1063/1.4972069

    Photosystem I, an Improved Model of the Stromal Subunits PsaC, PsaD, and PsaE
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    Localization of Two Phylloquinones, Q K and Q K ′, in an Improved Electron Density Map of Photosystem I at 4-Å Resolution
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    • Klukas, Olaf; Schubert, Wolf-Dieter; Jordan, Patrick
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    Gas dynamic virtual nozzle for generation of microscopic droplet streams
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    • Allahgholi, Aschkan; Becker, Julian; Delfs, Annette
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    High-Resolution Protein Structure Determination by Serial Femtosecond Crystallography
    journal, May 2012


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


    Direct observation of ultrafast collective motions in CO myoglobin upon ligand dissociation
    journal, September 2015


    Enzyme intermediates captured “on the fly” by mix-and-inject serial crystallography
    journal, May 2018


    Time-Resolved Macromolecular Crystallography at Pulsed X-ray Sources
    journal, March 2019

    • Schmidt, Marius
    • International Journal of Molecular Sciences, Vol. 20, Issue 6
    • DOI: 10.3390/ijms20061401