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

doi:10.1038/s41467-019-12955-3

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-ChowdhuryJay 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

Research output: Contribution to journal › Article › peer-review

45 Scopus citations

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.

Original language	English (US)
Article number	5021
Journal	Nature communications
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-12955-3
State	Published - Dec 1 2019

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General Physics and Astronomy

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10.1038/s41467-019-12955-3

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Gisriel, C., Coe, J., Letrun, R., Yefanov, O. M., Luna-Chavez, C., Stander, N. E., Lisova, S., Mariani, V., Kuhn, M., Aplin, S., Grant, T. D., Dörner, K., Sato, T., Echelmeier, A., Cruz Villarreal, J., Hunter, M. S., Wiedorn, M. O., Knoska, J., Mazalova, V., ... Fromme, P. (2019). Membrane protein megahertz crystallography at the European XFEL. Nature communications, 10(1), Article 5021. https://doi.org/10.1038/s41467-019-12955-3

Gisriel, C, Coe, J, Letrun, R, Yefanov, OM, Luna-Chavez, C, Stander, NE, Lisova, S, Mariani, V, Kuhn, M, Aplin, S, Grant, TD, Dörner, K, Sato, T, Echelmeier, A, Cruz Villarreal, J, Hunter, MS, Wiedorn, MO, Knoska, J, Mazalova, V, Roy-Chowdhury, S, Yang, JH, Jones, A, Bean, R, Bielecki, J, Kim, Y, Mills, G, Weinhausen, B, Meza, JD, Al-Qudami, N, Bajt, S, Brehm, G, Botha, S, Boukhelef, D, Brockhauser, S, Bruce, BD, Coleman, MA, Danilevski, C, Discianno, E, Dobson, Z, Fangohr, H, Martin-Garcia, JM, Gevorkov, Y, Hauf, S, Hosseinizadeh, A, Januschek, F, Ketawala, GK, Kupitz, C, Maia, L, Manetti, M, Messerschmidt, M, Michelat, T, Mondal, J, Ourmazd, A, Previtali, G, Sarrou, I, Schön, S, Schwander, P, Shelby, ML, Silenzi, A, Sztuk-Dambietz, J, Szuba, J, Turcato, M, White, TA, Wrona, K, Xu, C, Abdellatif, MH, Zook, JD, Spence, JCH, Chapman, HN, Barty, A, Kirian, RA, Frank, M, Ros, A, Schmidt, M, Fromme, R, Mancuso, AP & Fromme, P 2019, 'Membrane protein megahertz crystallography at the European XFEL', Nature communications, vol. 10, no. 1, 5021. https://doi.org/10.1038/s41467-019-12955-3

@article{59f2063333534ee3aedfd71bc724be70,

title = "Membrane protein megahertz crystallography at the European XFEL",

abstract = "The world{\textquoteright}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 {\AA}-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.",

author = "Chris Gisriel and Jesse Coe and Romain Letrun and Yefanov, {Oleksandr M.} and Cesar Luna-Chavez and Stander, {Natasha E.} and Stella Lisova and Valerio Mariani and Manuela Kuhn and Steve Aplin and Grant, {Thomas D.} and Katerina D{\"o}rner and Tokushi Sato and Austin Echelmeier and {Cruz Villarreal}, Jorvani and Hunter, {Mark S.} and Wiedorn, {Max O.} and Juraj Knoska and Victoria Mazalova and Shatabdi Roy-Chowdhury and Yang, {Jay How} and Alex Jones and Richard Bean and Johan Bielecki and Yoonhee Kim and Grant Mills and Britta Weinhausen and Meza, {Jose D.} and Nasser Al-Qudami and Sa{\v s}a Bajt and Gerrit Brehm and Sabine Botha and Djelloul Boukhelef and Sandor Brockhauser and Bruce, {Barry D.} and Coleman, {Matthew A.} and Cyril Danilevski and Erin Discianno and Zachary Dobson and Hans Fangohr and Martin-Garcia, {Jose M.} and Yaroslav Gevorkov and Steffen Hauf and Ahmad Hosseinizadeh and Friederike Januschek and Ketawala, {Gihan K.} and Christopher Kupitz and Luis Maia and Maurizio Manetti and Marc Messerschmidt and Thomas Michelat and Jyotirmoy Mondal and Abbas Ourmazd and Gianpietro Previtali and Iosifina Sarrou and Silvan Sch{\"o}n and Peter Schwander and Shelby, {Megan L.} and Alessandro Silenzi and Jolanta Sztuk-Dambietz and Janusz Szuba and Monica Turcato and White, {Thomas A.} and Krzysztof Wrona and Chen Xu and Abdellatif, {Mohamed H.} and Zook, {James D.} and Spence, {John C.H.} and Chapman, {Henry N.} and Anton Barty and Kirian, {Richard A.} and Matthias Frank and Alexandra Ros and Marius Schmidt and Raimund Fromme and Mancuso, {Adrian P.} and Petra Fromme",

note = "Publisher Copyright: {\textcopyright} 2019, The Author(s).",

year = "2019",

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day = "1",

doi = "10.1038/s41467-019-12955-3",

language = "English (US)",

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journal = "Nature communications",

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T1 - Membrane protein megahertz crystallography at the European XFEL

AU - Gisriel, Chris

AU - Coe, Jesse

AU - Letrun, Romain

AU - Yefanov, Oleksandr M.

AU - Luna-Chavez, Cesar

AU - Stander, Natasha E.

AU - Lisova, Stella

AU - Mariani, Valerio

AU - Kuhn, Manuela

AU - Aplin, Steve

AU - Grant, Thomas D.

AU - Dörner, Katerina

AU - Sato, Tokushi

AU - Echelmeier, Austin

AU - Cruz Villarreal, Jorvani

AU - Hunter, Mark S.

AU - Wiedorn, Max O.

AU - Knoska, Juraj

AU - Mazalova, Victoria

AU - Roy-Chowdhury, Shatabdi

AU - Yang, Jay How

AU - Jones, Alex

AU - Bean, Richard

AU - Bielecki, Johan

AU - Kim, Yoonhee

AU - Mills, Grant

AU - Weinhausen, Britta

AU - Meza, Jose D.

AU - Al-Qudami, Nasser

AU - Bajt, Saša

AU - Brehm, Gerrit

AU - Botha, Sabine

AU - Boukhelef, Djelloul

AU - Brockhauser, Sandor

AU - Bruce, Barry D.

AU - Coleman, Matthew A.

AU - Danilevski, Cyril

AU - Discianno, Erin

AU - Dobson, Zachary

AU - Fangohr, Hans

AU - Martin-Garcia, Jose M.

AU - Gevorkov, Yaroslav

AU - Hauf, Steffen

AU - Hosseinizadeh, Ahmad

AU - Januschek, Friederike

AU - Ketawala, Gihan K.

AU - Kupitz, Christopher

AU - Maia, Luis

AU - Manetti, Maurizio

AU - Messerschmidt, Marc

AU - Michelat, Thomas

AU - Mondal, Jyotirmoy

AU - Ourmazd, Abbas

AU - Previtali, Gianpietro

AU - Sarrou, Iosifina

AU - Schön, Silvan

AU - Schwander, Peter

AU - Shelby, Megan L.

AU - Silenzi, Alessandro

AU - Sztuk-Dambietz, Jolanta

AU - Szuba, Janusz

AU - Turcato, Monica

AU - White, Thomas A.

AU - Wrona, Krzysztof

AU - Xu, Chen

AU - Abdellatif, Mohamed H.

AU - Zook, James D.

AU - Spence, John C.H.

AU - Chapman, Henry N.

AU - Barty, Anton

AU - Kirian, Richard A.

AU - Frank, Matthias

AU - Ros, Alexandra

AU - Schmidt, Marius

AU - Fromme, Raimund

AU - Mancuso, Adrian P.

AU - Fromme, Petra

PY - 2019/12/1

Y1 - 2019/12/1

N2 - 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.

AB - 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.

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VL - 10

JO - Nature communications

JF - Nature communications

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Membrane protein megahertz crystallography at the European XFEL

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Photosynthesis seen in a new light by rapid X-ray pulses

Photosynthesis Seen in a New Light by Rapid X-ray Pulses

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Membrane protein megahertz crystallography at the European XFEL

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Photosynthesis seen in a new light by rapid X-ray pulses

Photosynthesis Seen in a New Light by Rapid X-ray Pulses

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