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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 Laboratory (SLAC), Menlo Park, CA (United States); Lawrence Livermore National Laboratory (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); USDOE National Nuclear Security Administration (NNSA)
Contributing Org.:
European XFEL Group
OSTI Identifier:
1596363
Alternate Identifier(s):
OSTI ID: 1598207; OSTI ID: 1959525
Report Number(s):
LLNL-JRNL-843428
Journal ID: ISSN 2041-1723; TRN: US2102069
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. 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. 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 = {Mon Nov 04 00:00:00 EST 2019},
month = {Mon Nov 04 00:00:00 EST 2019}
}

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Works referencing / citing this record:

Membrane protein megahertz crystallography at the European XFEL
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Phase Diversity Electro-optic Sampling: A new approach to single-shot terahertz waveform recording
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