Single-particle structure determination by X-ray free-electron lasers: Possibilities and challenges
Abstract
Single-particle structure recovery without crystals or radiation damage is a revolutionary possibility offered by X-ray free-electron lasers, but it involves formidable experimental and data-analytical challenges. Many of these difficulties were encountered during the development of cryogenic electron microscopy of biological systems. Electron microscopy of biological entities has now reached a spatial resolution of about 0.3 nm, with a rapidly emerging capability to map discrete and continuous conformational changes and the energy landscapes of biomolecular machines. Nonetheless, single-particle imaging by X-ray freeelectron lasers remains important for a range of applications, including the study of large “electron-opaque” objects and time-resolved examination of key biological processes at physiological temperatures. After summarizing the state of the art in the study of structure and conformations by cryogenic electron microscopy, we identify the primary opportunities and challenges facing X-ray-based single-particle approaches, and possible means for circumventing them.
- Authors:
-
- Univ. of Wisconsin, Milwaukee, WI (United States)
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Milwaukee, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF)
- OSTI Identifier:
- 1598194
- Alternate Identifier(s):
- OSTI ID: 1421053
- Grant/Contract Number:
- FG02-09ER16114; SC0002164
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Structural Dynamics
- Additional Journal Information:
- Journal Volume: 2; Journal Issue: 4; Journal ID: ISSN 2329-7778
- Publisher:
- American Crystallographic Association/AIP
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 71 CLASSICAL AND QUANTUM MECHANICS, GENERAL PHYSICS
Citation Formats
Hosseinizadeh, A., Dashti, A., Schwander, P., Fung, R., and Ourmazd, A. Single-particle structure determination by X-ray free-electron lasers: Possibilities and challenges. United States: N. p., 2015.
Web. doi:10.1063/1.4919740.
Hosseinizadeh, A., Dashti, A., Schwander, P., Fung, R., & Ourmazd, A. Single-particle structure determination by X-ray free-electron lasers: Possibilities and challenges. United States. https://doi.org/10.1063/1.4919740
Hosseinizadeh, A., Dashti, A., Schwander, P., Fung, R., and Ourmazd, A. Thu .
"Single-particle structure determination by X-ray free-electron lasers: Possibilities and challenges". United States. https://doi.org/10.1063/1.4919740. https://www.osti.gov/servlets/purl/1598194.
@article{osti_1598194,
title = {Single-particle structure determination by X-ray free-electron lasers: Possibilities and challenges},
author = {Hosseinizadeh, A. and Dashti, A. and Schwander, P. and Fung, R. and Ourmazd, A.},
abstractNote = {Single-particle structure recovery without crystals or radiation damage is a revolutionary possibility offered by X-ray free-electron lasers, but it involves formidable experimental and data-analytical challenges. Many of these difficulties were encountered during the development of cryogenic electron microscopy of biological systems. Electron microscopy of biological entities has now reached a spatial resolution of about 0.3 nm, with a rapidly emerging capability to map discrete and continuous conformational changes and the energy landscapes of biomolecular machines. Nonetheless, single-particle imaging by X-ray freeelectron lasers remains important for a range of applications, including the study of large “electron-opaque” objects and time-resolved examination of key biological processes at physiological temperatures. After summarizing the state of the art in the study of structure and conformations by cryogenic electron microscopy, we identify the primary opportunities and challenges facing X-ray-based single-particle approaches, and possible means for circumventing them.},
doi = {10.1063/1.4919740},
journal = {Structural Dynamics},
number = 4,
volume = 2,
place = {United States},
year = {Thu Apr 30 00:00:00 EDT 2015},
month = {Thu Apr 30 00:00:00 EDT 2015}
}
Web of Science
Works referenced in this record:
Single-shot three-dimensional structure determination of nanocrystals with femtosecond X-ray free-electron laser pulses
journal, June 2014
- Xu, Rui; Jiang, Huaidong; Song, Changyong
- Nature Communications, Vol. 5, Issue 1
Bayesian algorithms for recovering structure from single-particle diffraction snapshots of unknown orientation: a comparison
journal, July 2011
- Moths, Brian; Ourmazd, Abbas
- Acta Crystallographica Section A Foundations of Crystallography, Vol. 67, Issue 5
A Bayesian View on Cryo-EM Structure Determination
journal, January 2012
- Scheres, Sjors H. W.
- Journal of Molecular Biology, Vol. 415, Issue 2
Crystallography without crystals. I. The common-line method for assembling a three-dimensional diffraction volume from single-particle scattering
journal, February 2008
- Shneerson, V. L.; Ourmazd, A.; Saldin, D. K.
- Acta Crystallographica Section A Foundations of Crystallography, Vol. 64, Issue 2
Three-Dimensional Reconstruction of the Giant Mimivirus Particle with an X-Ray Free-Electron Laser
journal, March 2015
- Ekeberg, Tomas; Svenda, Martin; Abergel, Chantal
- Physical Review Letters, Vol. 114, Issue 9
Conformations of macromolecules and their complexes from heterogeneous datasets
journal, July 2014
- Schwander, P.; Fung, R.; Ourmazd, A.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647
High-resolution structure of viruses from random diffraction snapshots
journal, July 2014
- Hosseinizadeh, A.; Schwander, P.; Dashti, A.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647
Solving structure with sparse, randomly-oriented x-ray data
journal, January 2012
- Philipp, Hugh T.; Ayyer, Kartik; Tate, Mark W.
- Optics Express, Vol. 20, Issue 12
The symmetries of image formation by scattering I Theoretical framework
journal, January 2012
- Giannakis, Dimitrios; Schwander, Peter; Ourmazd, Abbas
- Optics Express, Vol. 20, Issue 12
Disentangling conformational states of macromolecules in 3D-EM through likelihood optimization
journal, December 2006
- Scheres, Sjors H. W.; Gao, Haixiao; Valle, Mikel
- Nature Methods, Vol. 4, Issue 1
Microholography of Living Organisms
journal, October 1982
- Solem, J. C.; Baldwin, G. C.
- Science, Vol. 218, Issue 4569
How Should We Think About the Ribosome?
journal, June 2012
- Moore, Peter B.
- Annual Review of Biophysics, Vol. 41, Issue 1
Signal, noise, and resolution in correlated fluctuations from snapshot small-angle x-ray scattering
journal, July 2011
- Kirian, Richard A.; Schmidt, Kevin E.; Wang, Xiaoyu
- Physical Review E, Vol. 84, Issue 1
Structure of the human LAT1–4F2hc heteromeric amino acid transporter complex
journal, March 2019
- Yan, Renhong; Zhao, Xin; Lei, Jianlin
- Nature, Vol. 568, Issue 7750
Three-Dimensional Electron Microscopy of Macromolecular Assemblies
book, January 2006
- Frank, Joachim
- Oxford University Press
Flat-field correction technique for digital detectors
conference, July 1998
- Seibert, James A.; Boone, John M.; Lindfors, Karen K.
- Medical Imaging '98, SPIE Proceedings
Reconstruction algorithm for single-particle diffraction imaging experiments
journal, August 2009
- Loh, Ne-Te Duane; Elser, Veit
- Physical Review E, Vol. 80, Issue 2
The symmetries of image formation by scattering II Applications
journal, January 2012
- Schwander, Peter; Giannakis, Dimitrios; Yoon, Chun Hong
- Optics Express, Vol. 20, Issue 12
Structure from fleeting illumination of faint spinning objects in flight
journal, November 2008
- Fung, Russell; Shneerson, Valentin; Saldin, Dilano K.
- Nature Physics, Vol. 5, Issue 1
Atomic structure of a single large biomolecule from diffraction patterns of random orientations
journal, July 2012
- Tegze, Miklós; Bortel, Gábor
- Journal of Structural Biology, Vol. 179, Issue 1
Potential for biomolecular imaging with femtosecond X-ray pulses
journal, August 2000
- Neutze, Richard; Wouts, Remco; van der Spoel, David
- Nature, Vol. 406, Issue 6797
The linac coherent light source single particle imaging road map
journal, July 2015
- Aquila, A.; Barty, A.; Bostedt, C.
- Structural Dynamics, Vol. 2, Issue 4
Disentangling conformational states of macromolecules in 3D-EM through likelihood optimization
book, April 2018
- Scheres, Sjors H. W.; Gao, Haixiao; Valle, Mikel
- Series in Structural Biology
Structure of the Yeast Mitochondrial Large Ribosomal Subunit
journal, March 2014
- Amunts, A.; Brown, A.; Bai, X. -c.
- Science, Vol. 343, Issue 6178
Structure of isolated biomolecules obtained from ultrashort x-ray pulses: exploiting the symmetry of random orientations
journal, March 2009
- Saldin, D. K.; Shneerson, V. L.; Fung, R.
- Journal of Physics: Condensed Matter, Vol. 21, Issue 13
Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy
journal, July 2010
- Fischer, Niels; Konevega, Andrey L.; Wintermeyer, Wolfgang
- Nature, Vol. 466, Issue 7304
Trajectories of the ribosome as a Brownian nanomachine
journal, November 2014
- Dashti, Ali; Schwander, Peter; Langlois, Robert
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 49
Structure of the Yeast Mitochondrial Large Ribosomal Subunit
journal, August 2014
- Amunts, Alexey; Brown, Alan; Bai, Xiao-chen
- Microscopy and Microanalysis, Vol. 20, Issue S3
A reconstruction algorithm for single-particle diffraction imaging experiments
journal, August 2009
- Loh, Duane Ne-Te; Elser, Veit
- Acta Crystallographica Section A Foundations of Crystallography, Vol. 65, Issue a1
A Bayesian view on cryo-EM structure determination
conference, May 2012
- Scheres, Sjors H. W.
- 2012 IEEE 9th International Symposium on Biomedical Imaging (ISBI 2012), 2012 9th IEEE International Symposium on Biomedical Imaging (ISBI)
Bayesian algorithms for recovering structure from single-particle diffraction snapshots of unknown orientation: a comparison
preprint, January 2010
- Moths, Brian; Ourmazd, Abbas
- arXiv
Atomic structure of a single large biomolecule from diffraction patterns of random orientations
preprint, January 2012
- Tegze, Miklós; Bortel, Gábor
- arXiv
Conformations of Macromolecules and their Complexes from Heterogeneous Datasets
preprint, January 2014
- Schwander, P.; Fung, R.; Ourmazd, A.
- arXiv
High-resolution structure of viruses from random diffraction snapshots
preprint, January 2014
- Hosseinizadeh, A.; Schwander, P.; Dashti, A.
- arXiv
Atomic structure of a single large biomolecule from diffraction patterns of random orientations
journal, July 2012
- Tegze, Miklós; Bortel, Gábor
- Journal of Structural Biology, Vol. 179, Issue 1
Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy
journal, July 2010
- Fischer, Niels; Konevega, Andrey L.; Wintermeyer, Wolfgang
- Nature, Vol. 466, Issue 7304
Single-shot three-dimensional structure determination of nanocrystals with femtosecond X-ray free-electron laser pulses
journal, June 2014
- Xu, Rui; Jiang, Huaidong; Song, Changyong
- Nature Communications, Vol. 5, Issue 1
Disentangling conformational states of macromolecules in 3D-EM through likelihood optimization
journal, December 2006
- Scheres, Sjors H. W.; Gao, Haixiao; Valle, Mikel
- Nature Methods, Vol. 4, Issue 1
Cryo-EM, XFELs and the structure conundrum in structural biology
journal, September 2019
- Ourmazd, Abbas
- Nature Methods, Vol. 16, Issue 10
The linac coherent light source single particle imaging road map
journal, July 2015
- Aquila, A.; Barty, A.; Bostedt, C.
- Structural Dynamics, Vol. 2, Issue 4
High-resolution structure of viruses from random diffraction snapshots
journal, July 2014
- Hosseinizadeh, A.; Schwander, P.; Dashti, A.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647
A Bayesian view on cryo-EM structure determination
conference, May 2012
- Scheres, Sjors H. W.
- 2012 IEEE 9th International Symposium on Biomedical Imaging (ISBI 2012), 2012 9th IEEE International Symposium on Biomedical Imaging (ISBI)
Flat-field correction technique for digital detectors
conference, July 1998
- Seibert, James A.; Boone, John M.; Lindfors, Karen K.
- Medical Imaging '98, SPIE Proceedings
Bayesian algorithms for recovering structure from single-particle diffraction snapshots of unknown orientation: a comparison
preprint, January 2010
- Moths, Brian; Ourmazd, Abbas
- arXiv
Works referencing / citing this record:
Short-wavelength free-electron laser sources and science: a review
text, January 2017
- Seddon, E. A.; Clarke, J. A.; Dunning, D. J.
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Coherent diffraction of single Rice Dwarf virus particles using hard X-rays at the Linac Coherent Light Source
text, January 2016
- Munke, Anna; Andreasson, Jakob; Aquila, Andrew
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Conformational landscape of a virus by single-particle X-ray scattering
journal, August 2017
- Hosseinizadeh, Ahmad; Mashayekhi, Ghoncheh; Copperman, Jeremy
- Nature Methods, Vol. 14, Issue 9
Coherent diffraction of single Rice Dwarf virus particles using hard X-rays at the Linac Coherent Light Source
journal, August 2016
- Munke, Anna; Andreasson, Jakob; Aquila, Andrew
- Scientific Data, Vol. 3, Issue 1
Coherent soft X-ray diffraction imaging of coliphage PR772 at the Linac coherent light source
journal, June 2017
- Reddy, Hemanth K. N.; Yoon, Chun Hong; Aquila, Andrew
- Scientific Data, Vol. 4, Issue 1
Evaluation of the performance of classification algorithms for XFEL single-particle imaging data
journal, February 2019
- Shi, Yingchen; Yin, Ke; Tai, Xuecheng
- IUCrJ, Vol. 6, Issue 2
Evaluation of the performance of classification algorithms for XFEL single-particle imaging data
text, January 2019
- Shi, Yingchen; Yin, Ke; Tai, Xuecheng
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Evaluation of the performance of classification algorithms for XFEL single-particle imaging data
text, January 2019
- Shi, Yingchen; Yin, Ke; Tai, Xuecheng
- International Union of Crystallography (IUCr)
Short-wavelength free-electron laser sources and science: a review
journal, October 2017
- Seddon, E. A.; Clarke, J. A.; Dunning, D. J.
- Reports on Progress in Physics, Vol. 80, Issue 11
Single-particle imaging by x-ray free-electron lasers—How many snapshots are needed?
journal, March 2020
- Poudyal, I.; Schmidt, M.; Schwander, P.
- Structural Dynamics, Vol. 7, Issue 2
A Survey of the Use of Iterative Reconstruction Algorithms in Electron Microscopy
journal, January 2017
- Sorzano, C. O. S.; Vargas, J.; Otón, J.
- BioMed Research International, Vol. 2017