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Title: Pink-beam serial crystallography

Abstract

Serial X-ray crystallography allows macromolecular structure determination at both X-ray free electron lasers (XFELs) and, more recently, synchrotron sources. The time resolution for serial synchrotron crystallography experiments has been limited to millisecond timescales with monochromatic beams. The polychromatic, “pink”, beam provides a more than two orders of magnitude increased photon flux and hence allows accessing much shorter timescales in diffraction experiments at synchrotron sources. Here we report the structure determination of two different protein samples by merging pink-beam diffraction patterns from many crystals, each collected with a single 100 ps X-ray pulse exposure per crystal using a setup optimized for very low scattering background. In contrast to experiments with monochromatic radiation, data from only 50 crystals were required to obtain complete datasets. The high quality of the diffraction data highlights the potential of this method for studying irreversible reactions at sub-microsecond timescales using high-brightness X-ray facilities.

Authors:
ORCiD logo [1]; ORCiD logo [2];  [3];  [4];  [5];  [5];  [5];  [6];  [5];  [7];  [8];  [9];  [10];  [10]; ORCiD logo [6];  [6];  [8];  [5]; ORCiD logo [10]; ORCiD logo [11]
  1. DESY, Hamburg (Germany). Center for Free Electron Laser Science and Photon Science
  2. DESY, Hamburg (Germany). Center for Free Electron Laser Science; University of Hamburg (Germany). Dept. of Physics
  3. Univ. of Chicago, IL (United States). Center for Advanced Radiation Sources
  4. Center for Advanced Radiation Sources
  5. DESY, Hamburg (Germany). Center for Free Electron Laser Science
  6. Institut für Biophysikalische Chemie, Hannover (Germany). Medizinische Hochschule Hannover (MHH)
  7. University of Hamburg (Germany). Dept. of Physics
  8. Deutsches Elektronen Synchrotron (DESY), Hamburg (Germany). Photon Science
  9. National Science Foundation BioXFEL Science and Technology Center, Buffalo, NY (United States)
  10. Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
  11. DESY, Hamburg (Germany). Center for Free Electron Laser Science; University of Hamburg (Germany). Dept. of Physics; Centre for Ultrafast Imaging, Hamburg (Germany)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Scientific User Facilities Division; European Union - Horizon 2020 Research and Innovation Programme; Helmholtz Association of German Research Centres - Virtual Institute; National Institutes of Health (NIH) - National Institute of General Medical Sciences
OSTI Identifier:
1422407
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
71 CLASSICAL AND QUANTUM MECHANICS, GENERAL PHYSICS; 46 INSTRUMENTATION RELATED TO NUCLEAR SCIENCE AND TECHNOLOGY; Techniques and instrumentation; X-ray crystallography

Citation Formats

Meents, A., Wiedorn, M. O., Srajer, V., Henning, R., Sarrou, I., Bergtholdt, J., Barthelmess, M., Reinke, P. Y. A., Dierksmeyer, D., Tolstikova, A., Schaible, S., Messerschmidt, M., Ogata, C. M., Kissick, D. J., Taft, M. H., Manstein, D. J., Lieske, J., Oberthuer, D., Fischetti, R. F., and Chapman, H. N. Pink-beam serial crystallography. United States: N. p., 2017. Web. doi:10.1038/s41467-017-01417-3.
Meents, A., Wiedorn, M. O., Srajer, V., Henning, R., Sarrou, I., Bergtholdt, J., Barthelmess, M., Reinke, P. Y. A., Dierksmeyer, D., Tolstikova, A., Schaible, S., Messerschmidt, M., Ogata, C. M., Kissick, D. J., Taft, M. H., Manstein, D. J., Lieske, J., Oberthuer, D., Fischetti, R. F., & Chapman, H. N. Pink-beam serial crystallography. United States. doi:10.1038/s41467-017-01417-3.
Meents, A., Wiedorn, M. O., Srajer, V., Henning, R., Sarrou, I., Bergtholdt, J., Barthelmess, M., Reinke, P. Y. A., Dierksmeyer, D., Tolstikova, A., Schaible, S., Messerschmidt, M., Ogata, C. M., Kissick, D. J., Taft, M. H., Manstein, D. J., Lieske, J., Oberthuer, D., Fischetti, R. F., and Chapman, H. N. Fri . "Pink-beam serial crystallography". United States. doi:10.1038/s41467-017-01417-3. https://www.osti.gov/servlets/purl/1422407.
@article{osti_1422407,
title = {Pink-beam serial crystallography},
author = {Meents, A. and Wiedorn, M. O. and Srajer, V. and Henning, R. and Sarrou, I. and Bergtholdt, J. and Barthelmess, M. and Reinke, P. Y. A. and Dierksmeyer, D. and Tolstikova, A. and Schaible, S. and Messerschmidt, M. and Ogata, C. M. and Kissick, D. J. and Taft, M. H. and Manstein, D. J. and Lieske, J. and Oberthuer, D. and Fischetti, R. F. and Chapman, H. N.},
abstractNote = {Serial X-ray crystallography allows macromolecular structure determination at both X-ray free electron lasers (XFELs) and, more recently, synchrotron sources. The time resolution for serial synchrotron crystallography experiments has been limited to millisecond timescales with monochromatic beams. The polychromatic, “pink”, beam provides a more than two orders of magnitude increased photon flux and hence allows accessing much shorter timescales in diffraction experiments at synchrotron sources. Here we report the structure determination of two different protein samples by merging pink-beam diffraction patterns from many crystals, each collected with a single 100 ps X-ray pulse exposure per crystal using a setup optimized for very low scattering background. In contrast to experiments with monochromatic radiation, data from only 50 crystals were required to obtain complete datasets. The high quality of the diffraction data highlights the potential of this method for studying irreversible reactions at sub-microsecond timescales using high-brightness X-ray facilities.},
doi = {10.1038/s41467-017-01417-3},
journal = {Nature Communications},
number = 1,
volume = 8,
place = {United States},
year = {2017},
month = {11}
}

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Cited by: 34 works
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    Works referencing / citing this record:

    Kinetic Modeling of the X-ray-Induced Damage to a Metalloprotein
    journal, July 2013

    • Davis, Katherine M.; Kosheleva, Irina; Henning, Robert W.
    • The Journal of Physical Chemistry B, Vol. 117, Issue 31
    • DOI: 10.1021/jp403654n

    Millisecond Laue structures of an enzyme–product complex using photocaged substrate analogs
    journal, October 1998

    • Stoddard, Barry L.; Cohen, Bruce E.; Brubaker, Michael
    • Nature Structural Biology, Vol. 5, Issue 10
    • DOI: 10.1038/2331

    Time-resolved X-ray crystallographic study of the conformational change in Ha-Ras p21 protein on GTP hydrolysis
    journal, May 1990

    • Schlichting, Ilme; Almo, Steven C.; Rapp, Gert
    • Nature, Vol. 345, Issue 6273
    • DOI: 10.1038/345309a0

    Femtosecond X-ray protein nanocrystallography
    journal, February 2011

    • Chapman, Henry N.; Fromme, Petra; Barty, Anton
    • Nature, Vol. 470, Issue 7332, p. 73-77
    • DOI: 10.1038/nature09750

    De novo phasing with X-ray laser reveals mosquito larvicide BinAB structure
    journal, September 2016

    • Colletier, Jacques-Philippe; Sawaya, Michael R.; Gingery, Mari
    • Nature, Vol. 539, Issue 7627
    • DOI: 10.1038/nature19825

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

    • Stagno, J. R.; Liu, Y.; Bhandari, Y. R.
    • Nature, Vol. 541, Issue 7636
    • DOI: 10.1038/nature20599

    Imaging live cell in micro-liquid enclosure by X-ray laser diffraction
    journal, January 2014

    • Kimura, Takashi; Joti, Yasumasa; Shibuya, Akemi
    • Nature Communications, Vol. 5, Issue 1
    • DOI: 10.1038/ncomms4052

    High-speed fixed-target serial virus crystallography
    journal, June 2017

    • Roedig, Philip; Ginn, Helen M.; Pakendorf, Tim
    • Nature Methods, Vol. 14, Issue 8
    • DOI: 10.1038/nmeth.4335

    A micro-patterned silicon chip as sample holder for macromolecular crystallography experiments with minimal background scattering
    journal, May 2015

    • Roedig, P.; Vartiainen, I.; Duman, R.
    • Scientific Reports, Vol. 5, Issue 1
    • DOI: 10.1038/srep10451

    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

    Protein kinetics: Structures of intermediates and reaction mechanism from time-resolved x-ray data
    journal, March 2004

    • Schmidt, M.; Pahl, R.; Srajer, V.
    • Proceedings of the National Academy of Sciences, Vol. 101, Issue 14
    • DOI: 10.1073/pnas.0305983101

    From The Cover: Visualizing reaction pathways in photoactive yellow protein from nanoseconds to seconds
    journal, May 2005

    • Ihee, H.; Rajagopal, S.; Srajer, V.
    • Proceedings of the National Academy of Sciences, Vol. 102, Issue 20
    • DOI: 10.1073/pnas.0409035102

    Ligand migration pathway and protein dynamics in myoglobin: A time-resolved crystallographic study on L29W MbCO
    journal, August 2005

    • Schmidt, M.; Nienhaus, K.; Pahl, R.
    • Proceedings of the National Academy of Sciences, Vol. 102, Issue 33
    • DOI: 10.1073/pnas.0504932102

    Allosteric action in real time: Time-resolved crystallographic studies of a cooperative dimeric hemoglobin
    journal, May 2006

    • Knapp, J. E.; Pahl, R.; Srajer, V.
    • Proceedings of the National Academy of Sciences, Vol. 103, Issue 20
    • DOI: 10.1073/pnas.0509411103

    Experimental determination of the radiation dose limit for cryocooled protein crystals
    journal, March 2006

    • Owen, R. L.; Rudino-Pinera, E.; Garman, E. F.
    • Proceedings of the National Academy of Sciences, Vol. 103, Issue 13
    • DOI: 10.1073/pnas.0600973103

    Origin and temperature dependence of radiation damage in biological samples at cryogenic temperatures
    journal, December 2009

    • Meents, A.; Gutmann, S.; Wagner, A.
    • Proceedings of the National Academy of Sciences, Vol. 107, Issue 3
    • DOI: 10.1073/pnas.0905481107

    Accessing protein conformational ensembles using room-temperature X-ray crystallography
    journal, September 2011

    • Fraser, J. S.; van den Bedem, H.; Samelson, A. J.
    • Proceedings of the National Academy of Sciences, Vol. 108, Issue 39
    • DOI: 10.1073/pnas.1111325108

    Protein crystal structure obtained at 2.9 A resolution from injecting bacterial cells into an X-ray free-electron laser beam
    journal, August 2014

    • Sawaya, M. R.; Cascio, D.; Gingery, M.
    • Proceedings of the National Academy of Sciences, Vol. 111, Issue 35
    • DOI: 10.1073/pnas.1413456111

    Atomic structure of granulin determined from native nanocrystalline granulovirus using an X-ray free-electron laser
    journal, February 2017

    • Gati, Cornelius; Oberthuer, Dominik; Yefanov, Oleksandr
    • Proceedings of the National Academy of Sciences, Vol. 114, Issue 9
    • DOI: 10.1073/pnas.1609243114

    The Protein Data Bank
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    Fixed-target serial oscillation crystallography at room temperature
    journal, February 2019


    Synchrotron microcrystal native-SAD phasing at a low energy
    journal, May 2019


    On-chip crystallization for serial crystallography experiments and on-chip ligand-binding studies
    journal, June 2019


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    journal, June 2003


    Light-Induced Structural Changes in a Photosynthetic Reaction Center Caught by Laue Diffraction
    journal, April 2010


    Photolysis of the Carbon Monoxide Complex of Myoglobin: Nanosecond Time-Resolved Crystallography
    journal, December 1996


    Biostructural Science Inspired by Next-Generation X-Ray Sources
    journal, June 2015


    Mix and Inject: Reaction Initiation by Diffusion for Time-Resolved Macromolecular Crystallography
    journal, January 2013


    Fixed-target serial oscillation crystallography at room temperature
    journal, February 2019


    Synchrotron microcrystal native-SAD phasing at a low energy
    journal, May 2019


    On-chip crystallization for serial crystallography experiments and on-chip ligand-binding studies
    journal, June 2019