Structure-factor amplitude reconstruction from serial femtosecond crystallography of two-dimensional membrane-protein crystals
Abstract
Serial femtosecond crystallography of two-dimensional membrane-protein crystals at X-ray free-electron lasers has the potential to address the dynamics of functionally relevant large-scale motions, which can be sterically hindered in three-dimensional crystals and suppressed in cryocooled samples. In previous work, diffraction data limited to a two-dimensional reciprocal-space slice were evaluated and it was demonstrated that the low intensity of the diffraction signal can be overcome by collecting highly redundant data, thus enhancing the achievable resolution. Here, the application of a newly developed method to analyze diffraction data covering three reciprocal-space dimensions, extracting the reciprocal-space map of the structure-factor amplitudes, is presented. Despite the low resolution and completeness of the data set, it is shown by molecular replacement that the reconstructed amplitudes carry meaningful structural information. Therefore, it appears that these intrinsic limitations in resolution and completeness from two-dimensional crystal diffraction may be overcome by collecting highly redundant data along the three reciprocal-space axes, thus allowing the measurement of large-scale dynamics in pump–probe experiments.
- Authors:
- Publication Date:
- Research Org.:
- Brookhaven National Lab. (BNL), Upton, NY (United States); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE National Nuclear Security Administration (NNSA)
- OSTI Identifier:
- 1481810
- Alternate Identifier(s):
- OSTI ID: 1493572; OSTI ID: 1557942
- Report Number(s):
- BNL-211246-2019-JAAM; LLNL-JRNL-782404
Journal ID: ISSN 2052-2525; IUCRAJ; PII: S2052252518014641
- Grant/Contract Number:
- AC52-07NA27344; AC02-76SF00515; SC0012704
- Resource Type:
- Published Article
- Journal Name:
- IUCrJ
- Additional Journal Information:
- Journal Name: IUCrJ Journal Volume: 6 Journal Issue: 1; Journal ID: ISSN 2052-2525
- Publisher:
- International Union of Crystallography (IUCr)
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; free-electron lasers; serial femtosecond crystallography; membrane proteins; two-dimensional crystals; Biological and medical sciences
Citation Formats
Casadei, Cecilia M., Nass, Karol, Barty, Anton, Hunter, Mark S., Padeste, Celestino, Tsai, Ching-Ju, Boutet, Sébastien, Messerschmidt, Marc, Sala, Leonardo, Williams, Garth J., Ozerov, Dmitry, Coleman, Matthew, Li, Xiao-Dan, Frank, Matthias, and Pedrini, Bill. Structure-factor amplitude reconstruction from serial femtosecond crystallography of two-dimensional membrane-protein crystals. United Kingdom: N. p., 2019.
Web. doi:10.1107/S2052252518014641.
Casadei, Cecilia M., Nass, Karol, Barty, Anton, Hunter, Mark S., Padeste, Celestino, Tsai, Ching-Ju, Boutet, Sébastien, Messerschmidt, Marc, Sala, Leonardo, Williams, Garth J., Ozerov, Dmitry, Coleman, Matthew, Li, Xiao-Dan, Frank, Matthias, & Pedrini, Bill. Structure-factor amplitude reconstruction from serial femtosecond crystallography of two-dimensional membrane-protein crystals. United Kingdom. https://doi.org/10.1107/S2052252518014641
Casadei, Cecilia M., Nass, Karol, Barty, Anton, Hunter, Mark S., Padeste, Celestino, Tsai, Ching-Ju, Boutet, Sébastien, Messerschmidt, Marc, Sala, Leonardo, Williams, Garth J., Ozerov, Dmitry, Coleman, Matthew, Li, Xiao-Dan, Frank, Matthias, and Pedrini, Bill. Tue .
"Structure-factor amplitude reconstruction from serial femtosecond crystallography of two-dimensional membrane-protein crystals". United Kingdom. https://doi.org/10.1107/S2052252518014641.
@article{osti_1481810,
title = {Structure-factor amplitude reconstruction from serial femtosecond crystallography of two-dimensional membrane-protein crystals},
author = {Casadei, Cecilia M. and Nass, Karol and Barty, Anton and Hunter, Mark S. and Padeste, Celestino and Tsai, Ching-Ju and Boutet, Sébastien and Messerschmidt, Marc and Sala, Leonardo and Williams, Garth J. and Ozerov, Dmitry and Coleman, Matthew and Li, Xiao-Dan and Frank, Matthias and Pedrini, Bill},
abstractNote = {Serial femtosecond crystallography of two-dimensional membrane-protein crystals at X-ray free-electron lasers has the potential to address the dynamics of functionally relevant large-scale motions, which can be sterically hindered in three-dimensional crystals and suppressed in cryocooled samples. In previous work, diffraction data limited to a two-dimensional reciprocal-space slice were evaluated and it was demonstrated that the low intensity of the diffraction signal can be overcome by collecting highly redundant data, thus enhancing the achievable resolution. Here, the application of a newly developed method to analyze diffraction data covering three reciprocal-space dimensions, extracting the reciprocal-space map of the structure-factor amplitudes, is presented. Despite the low resolution and completeness of the data set, it is shown by molecular replacement that the reconstructed amplitudes carry meaningful structural information. Therefore, it appears that these intrinsic limitations in resolution and completeness from two-dimensional crystal diffraction may be overcome by collecting highly redundant data along the three reciprocal-space axes, thus allowing the measurement of large-scale dynamics in pump–probe experiments.},
doi = {10.1107/S2052252518014641},
journal = {IUCrJ},
number = 1,
volume = 6,
place = {United Kingdom},
year = {2019},
month = {1}
}
https://doi.org/10.1107/S2052252518014641
Web of Science
Works referenced in this record:
Goniometer-based femtosecond crystallography with X-ray free electron lasers
journal, October 2014
- Cohen, Aina E.; Soltis, S. Michael; González, Ana
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 48, p. 17122-17127
Cheetah : software for high-throughput reduction and analysis of serial femtosecond X-ray diffraction data
journal, May 2014
- Barty, Anton; Kirian, Richard A.; Maia, Filipe R. N. C.
- Journal of Applied Crystallography, Vol. 47, Issue 3
Linking Crystallographic Model and Data Quality
journal, May 2012
- Karplus, P. A.; Diederichs, K.
- Science, Vol. 336, Issue 6084
CrystFEL : a software suite for snapshot serial crystallography
journal, March 2012
- White, Thomas A.; Kirian, Richard A.; Martin, Andrew V.
- Journal of Applied Crystallography, Vol. 45, Issue 2
Overview of the CCP 4 suite and current developments
journal, March 2011
- Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
Membrane protein structural biology using X-ray free electron lasers
journal, August 2015
- Neutze, Richard; Brändén, Gisela; Schertler, Gebhard FX
- Current Opinion in Structural Biology, Vol. 33
Measurement and evaluation of electron diffraction patterns from two-dimensional crystals
journal, January 1984
- Baldwin, Joyce; Henderson, Richard
- Ultramicroscopy, Vol. 14, Issue 4
Announcing the worldwide Protein Data Bank
journal, December 2003
- Berman, Helen; Henrick, Kim; Nakamura, Haruki
- Nature Structural & Molecular Biology, Vol. 10, Issue 12
High-speed fixed-target serial virus crystallography
journal, June 2017
- Roedig, Philip; Ginn, Helen M.; Pakendorf, Tim
- Nature Methods, Vol. 14, Issue 8
Lipidic cubic phase injector is a viable crystal delivery system for time-resolved serial crystallography
journal, August 2016
- Nogly, Przemyslaw; Panneels, Valerie; Nelson, Garrett
- Nature Communications, Vol. 7, Issue 1
New Python-based methods for data processing
journal, June 2013
- Sauter, Nicholas K.; Hattne, Johan; Grosse-Kunstleve, Ralf W.
- Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7
High-Resolution Protein Structure Determination by Serial Femtosecond Crystallography
journal, May 2012
- Boutet, S.; Lomb, L.; Williams, G. J.
- Science, Vol. 337, Issue 6092
Femtosecond X-ray protein nanocrystallography
journal, February 2011
- Chapman, Henry N.; Fromme, Petra; Barty, Anton
- Nature, Vol. 470, Issue 7332, p. 73-77
Molecular mechanism of vectorial proton translocation by bacteriorhodopsin
journal, August 2000
- Subramaniam, Sriram; Henderson, Richard
- Nature, Vol. 406, Issue 6796
Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy
journal, July 2014
- Kern, Jan; Tran, Rosalie; Alonso-Mori, Roberto
- Nature Communications, Vol. 5, Issue 1
Serial crystallography at synchrotrons and X-ray lasers
journal, February 2017
- Standfuss, Jörg; Spence, John
- IUCrJ, Vol. 4, Issue 2
Enzyme intermediates captured “on the fly” by mix-and-inject serial crystallography
journal, May 2018
- Olmos, Jose L.; Pandey, Suraj; Martin-Garcia, Jose M.
- BMC Biology, Vol. 16, Issue 1
Serial femtosecond crystallography: the first five years
journal, February 2015
- Schlichting, Ilme
- IUCrJ, Vol. 2, Issue 2, p. 246-255
X-ray detectors at the Linac Coherent Light Source
journal, April 2015
- Blaj, Gabriel; Caragiulo, Pietro; Carini, Gabriella
- Journal of Synchrotron Radiation, Vol. 22, Issue 3
The Coherent X-ray Imaging instrument at the Linac Coherent Light Source
journal, April 2015
- Liang, Mengning; Williams, Garth J.; Messerschmidt, Marc
- Journal of Synchrotron Radiation, Vol. 22, Issue 3
Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein
journal, December 2014
- Tenboer, Jason; Basu, Shibom; Zatsepin, Nadia
- Science, Vol. 346, Issue 6214
Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser
journal, July 2014
- Kupitz, Christopher; Basu, Shibom; Grotjohann, Ingo
- Nature, Vol. 513, Issue 7517
Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy
journal, June 1990
- Henderson, R.; Baldwin, J. M.; Ceska, T. A.
- Journal of Molecular Biology, Vol. 213, Issue 4
Three-dimensional structure of orthorhombic purple membrane at 6.5 Å resolution
journal, January 1983
- Leifer, Dana; Henderson, Richard
- Journal of Molecular Biology, Vol. 163, Issue 3
Improved Fourier coefficients for maps using phases from partial structures with errors
journal, May 1986
- Read, R. J.
- Acta Crystallographica Section A Foundations of Crystallography, Vol. 42, Issue 3
Resolution extension by image summing in serial femtosecond crystallography of two-dimensional membrane-protein crystals
journal, January 2018
- Casadei, Cecilia M.; Tsai, Ching-Ju; Barty, Anton
- IUCrJ, Vol. 5, Issue 1
Self-terminating diffraction gates femtosecond X-ray nanocrystallography measurements
journal, December 2011
- Barty, Anton; Caleman, Carl; Aquila, Andrew
- Nature Photonics, Vol. 6, Issue 1
Structure of photosystem II and substrate binding at room temperature
journal, November 2016
- Young, Iris D.; Ibrahim, Mohamed; Chatterjee, Ruchira
- Nature, Vol. 540, Issue 7633
Radiation damage in protein serial femtosecond crystallography using an x-ray free-electron laser
journal, December 2011
- Lomb, Lukas; Barends, Thomas R. M.; Kassemeyer, Stephan
- Physical Review B, Vol. 84, Issue 21
Lipidic cubic phase injector facilitates membrane protein serial femtosecond crystallography
journal, February 2014
- Weierstall, Uwe; James, Daniel; Wang, Chong
- Nature Communications, Vol. 5, Issue 1
The Reconstruction of a Three-Dimensional Structure from Projections and its Application to Electron Microscopy
journal, June 1970
- Crowther, R. A.; DeRosier, D. J.; Klug, A.
- Proceedings of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 317, Issue 1530
Fixed-target protein serial microcrystallography with an x-ray free electron laser
journal, August 2014
- Hunter, Mark S.; Segelke, Brent; Messerschmidt, Marc
- Scientific Reports, Vol. 4, Issue 1
Three-dimensional model of purple membrane obtained by electron microscopy
journal, September 1975
- Henderson, R.; Unwin, P. N. T.
- Nature, Vol. 257, Issue 5521
7 Å resolution in protein two-dimensional-crystal X-ray diffraction at Linac Coherent Light Source
journal, July 2014
- Pedrini, Bill; Tsai, Ching-Ju; Capitani, Guido
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647
Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL
journal, February 2017
- Suga, Michihiro; Akita, Fusamichi; Sugahara, Michihiro
- Nature, Vol. 543, Issue 7643
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
PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
On the treatment of negative intensity observations
journal, July 1978
- French, S.; Wilson, K.
- Acta Crystallographica Section A, Vol. 34, Issue 4
Indications of radiation damage in ferredoxin microcrystals using high-intensity X-FEL beams
journal, February 2015
- Nass, Karol; Foucar, Lutz; Barends, Thomas R. M.
- Journal of Synchrotron Radiation, Vol. 22, Issue 2
Two-dimensional crystals: a powerful approach to assess structure, function and dynamics of membrane proteins
journal, August 2001
- Stahlberg, Henning; Fotiadis, Dimitrios; Scheuring, Simon
- FEBS Letters, Vol. 504, Issue 3
An efficient method for finding the minimum of a function of several variables without calculating derivatives
journal, February 1964
- Powell, M. J. D.
- The Computer Journal, Vol. 7, Issue 2
Femtosecond X-ray diffraction from two-dimensional protein crystals
journal, February 2014
- Frank, Matthias; Carlson, David B.; Hunter, Mark S.
- IUCrJ, Vol. 1, Issue 2
Iterative-build OMIT maps: map improvement by iterative model building and refinement without model bias
journal, April 2008
- Terwilliger, Thomas C.; Grosse-Kunstleve, Ralf W.; Afonine, Pavel V.
- Acta Crystallographica Section D Biological Crystallography, Vol. 64, Issue 5
A three-dimensional movie of structural changes in bacteriorhodopsin
journal, December 2016
- Nango, Eriko; Royant, Antoine; Kubo, Minoru
- Science, Vol. 354, Issue 6319, p. 1552-1557
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
Electron Crystallography of Bacteriorhodopsin with Millisecond Time Resolution
journal, December 1999
- Subramaniam, Sriram; Henderson, Richard
- Journal of Structural Biology, Vol. 128, Issue 1
Communication in the Presence of Noise
journal, January 1949
- Shannon, C. E.
- Proceedings of the IRE, Vol. 37, Issue 1
Phaser crystallographic software
journal, July 2007
- McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D.
- Journal of Applied Crystallography, Vol. 40, Issue 4
Direct observation of ultrafast collective motions in CO myoglobin upon ligand dissociation
journal, September 2015
- Barends, T. R. M.; Foucar, L.; Ardevol, A.
- Science, Vol. 350, Issue 6259
Lipidic cubic phase injector is a viable crystal delivery system for time-resolved serial crystallography
text, January 2016
- Nogly, Przemyslaw; Panneels, Valerie; Nelson, Garrett
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Structures of riboswitch RNA reaction states by mix-and-inject XFEL serial crystallography
text, January 2016
- Stagno, J. R.; Liu, Y.; Bhandari, Y. R.
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Works referencing / citing this record:
Structure-factor amplitude reconstruction from serial femtosecond crystallography of two-dimensional membrane-protein crystals
text, January 2019
- Casadei, Cecilia M.; Nass, Karol; Barty, Anton
- Deutsches Elektronen-Synchrotron, DESY, Hamburg