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Complementarity of neutron, XFEL and synchrotron crystallography for defining the structures of metalloenzymes at room temperature

Complementarity of neutron, XFEL and synchrotron crystallography for defining the structures of metalloenzymes at room temperature
Complementarity of neutron, XFEL and synchrotron crystallography for defining the structures of metalloenzymes at room temperature
Room-temperature macromolecular crystallography allows protein structures to be determined under close-to-physiological conditions, permits dynamic freedom in protein motions and enables time-resolved studies. In the case of metalloenzymes that are highly sensitive to radiation damage, such room-temperature experiments can present challenges, including increased rates of X-ray reduction of metal centres and site-specific radiation-damage artefacts, as well as in devising appropriate sample-delivery and data-collection methods. It can also be problematic to compare structures measured using different crystal sizes and light sources. In this study, structures of a multifunctional globin, dehaloperoxidase B (DHP-B), obtained using several methods of room-temperature crystallographic structure determination are described and compared. Here, data were measured from large single crystals and multiple microcrystals using neutrons, X-ray free-electron laser pulses, monochromatic synchrotron radiation and polychromatic (Laue) radiation light sources. These approaches span a range of 18 orders of magnitude in measurement time per diffraction pattern and four orders of magnitude in crystal volume. The first room-temperature neutron structures of DHP-B are also presented, allowing the explicit identification of the hydrogen positions. The neutron data proved to be complementary to the serial femtosecond crystallography data, with both methods providing structures free of the effects of X-ray radiation damage when compared with standard cryo-crystallography. Comparison of these room-temperature methods demonstrated the large differences in sample requirements, data-collection time and the potential for radiation damage between them. With regard to the structure and function of DHP-B, despite the results being partly limited by differences in the underlying structures, new information was gained on the protonation states of active-site residues which may guide future studies of DHP-B.
XFEL, erial synchrotron crystallography, neutron crystallography, serial femtosecond crystallography, room temperature, XFELs, metalloenzymes, serial synchrotron crystallography
2052-2525
610-624
Moreno-Chicano, Tadeo
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Carey, Leiah M.
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Axford, Danny
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Beale, John H.
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Doak, R. Bruce
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Duyvesteyn, Helen M.E.
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Ebrahim, Ali
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Henning, Robert W.
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Monteiro, Diana C.F.
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Myles, Dean A.
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Owada, Shigeki
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Sherrell, Darren A.
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Straw, Megan L.
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Šrajjer, Vukica
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Sugimoto, Hiroshi
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Tono, Kensuke
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Tosha, Takehiko
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Tews, Ivo
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Trebbin, Martin
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Strange, Richard W.
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Weiss, Kelvin L.
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Worrall, Jonathan A.R.
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Meilleur, Flora
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Owen, Robin L.
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Ghiladi, Reza A.
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Hough, Michael A.
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Moreno-Chicano, Tadeo
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Carey, Leiah M.
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Axford, Danny
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Beale, John H.
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Doak, R. Bruce
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Duyvesteyn, Helen M.E.
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Ebrahim, Ali
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Henning, Robert W.
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Monteiro, Diana C.F.
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Myles, Dean A.
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Owada, Shigeki
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Sherrell, Darren A.
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Straw, Megan L.
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Šrajjer, Vukica
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Sugimoto, Hiroshi
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Tono, Kensuke
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Tosha, Takehiko
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Tews, Ivo
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Trebbin, Martin
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Strange, Richard W.
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Weiss, Kelvin L.
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Worrall, Jonathan A.R.
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Meilleur, Flora
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Owen, Robin L.
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Ghiladi, Reza A.
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Hough, Michael A.
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Moreno-Chicano, Tadeo, Carey, Leiah M., Axford, Danny, Beale, John H., Doak, R. Bruce, Duyvesteyn, Helen M.E., Ebrahim, Ali, Henning, Robert W., Monteiro, Diana C.F., Myles, Dean A., Owada, Shigeki, Sherrell, Darren A., Straw, Megan L., Šrajjer, Vukica, Sugimoto, Hiroshi, Tono, Kensuke, Tosha, Takehiko, Tews, Ivo, Trebbin, Martin, Strange, Richard W., Weiss, Kelvin L., Worrall, Jonathan A.R., Meilleur, Flora, Owen, Robin L., Ghiladi, Reza A. and Hough, Michael A. (2022) Complementarity of neutron, XFEL and synchrotron crystallography for defining the structures of metalloenzymes at room temperature. IUCrJ, 9 (Part 5), 610-624. (doi:10.1107/S2052252522006418).

Record type: Article

Abstract

Room-temperature macromolecular crystallography allows protein structures to be determined under close-to-physiological conditions, permits dynamic freedom in protein motions and enables time-resolved studies. In the case of metalloenzymes that are highly sensitive to radiation damage, such room-temperature experiments can present challenges, including increased rates of X-ray reduction of metal centres and site-specific radiation-damage artefacts, as well as in devising appropriate sample-delivery and data-collection methods. It can also be problematic to compare structures measured using different crystal sizes and light sources. In this study, structures of a multifunctional globin, dehaloperoxidase B (DHP-B), obtained using several methods of room-temperature crystallographic structure determination are described and compared. Here, data were measured from large single crystals and multiple microcrystals using neutrons, X-ray free-electron laser pulses, monochromatic synchrotron radiation and polychromatic (Laue) radiation light sources. These approaches span a range of 18 orders of magnitude in measurement time per diffraction pattern and four orders of magnitude in crystal volume. The first room-temperature neutron structures of DHP-B are also presented, allowing the explicit identification of the hydrogen positions. The neutron data proved to be complementary to the serial femtosecond crystallography data, with both methods providing structures free of the effects of X-ray radiation damage when compared with standard cryo-crystallography. Comparison of these room-temperature methods demonstrated the large differences in sample requirements, data-collection time and the potential for radiation damage between them. With regard to the structure and function of DHP-B, despite the results being partly limited by differences in the underlying structures, new information was gained on the protonation states of active-site residues which may guide future studies of DHP-B.

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Accepted/In Press date: 21 June 2022
e-pub ahead of print date: 25 July 2022
Published date: September 2022
Keywords: XFEL, erial synchrotron crystallography, neutron crystallography, serial femtosecond crystallography, room temperature, XFELs, metalloenzymes, serial synchrotron crystallography

Identifiers

Local EPrints ID: 469282
URI: http://eprints.soton.ac.uk/id/eprint/469282
ISSN: 2052-2525
PURE UUID: 16836c94-8f6e-4125-914c-ca7184f2e8e4
ORCID for Ivo Tews: ORCID iD orcid.org/0000-0002-4704-1139

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Date deposited: 12 Sep 2022 16:58
Last modified: 06 Jun 2024 01:48

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Contributors

Author: Tadeo Moreno-Chicano
Author: Leiah M. Carey
Author: Danny Axford
Author: John H. Beale
Author: R. Bruce Doak
Author: Helen M.E. Duyvesteyn
Author: Ali Ebrahim
Author: Robert W. Henning
Author: Diana C.F. Monteiro
Author: Dean A. Myles
Author: Shigeki Owada
Author: Darren A. Sherrell
Author: Megan L. Straw
Author: Vukica Šrajjer
Author: Hiroshi Sugimoto
Author: Kensuke Tono
Author: Takehiko Tosha
Author: Ivo Tews ORCID iD
Author: Martin Trebbin
Author: Richard W. Strange
Author: Kelvin L. Weiss
Author: Jonathan A.R. Worrall
Author: Flora Meilleur
Author: Robin L. Owen
Author: Reza A. Ghiladi
Author: Michael A. Hough

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