Ab initio structure determination from experimental fluctuation X-ray scattering data

Pande, Kanupriya; Donatelli, Jeffrey J.; Malmerberg, Erik; Foucar, Lutz; Bostedt, Christoph; Schlichting, Ilme; Zwart, Petrus H.

doi:10.1073/pnas.1812064115

Title: Ab initio structure determination from experimental fluctuation X-ray scattering data

Journal Article · Mon Oct 29 00:00:00 EDT 2018 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1812064115· OSTI ID:1479619

Pande, Kanupriya; Donatelli, Jeffrey J.; Malmerberg, Erik; Foucar, Lutz; Bostedt, Christoph; Schlichting, Ilme; Zwart, Petrus H.

Fluctuation X-ray scattering (FXS) is an emerging experimental technique in which X-ray solution scattering data are collected from particles in solution using ultrashort X-ray exposures generated by a free-electron laser (FEL). FXS experiments overcome the low data-to-parameter ratios associated with traditional solution scattering measurements by providing several orders of magnitude more information in the final processed data. Here we demonstrate the practical feasibility of FEL-based FXS on a biological multiple-particle system and describe data-processing techniques required to extract robust FXS data and significantly reduce the required number of snapshots needed by introducing an iterative noise-filtering technique. We showcase a successful ab initio electron density reconstruction from such an experiment, studying the Paramecium bursaria Chlorella virus (PBCV-1).

View Journal Article

Cite

Export

Save

Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-05CH11231; AC02-76SF00515; R01GM109019

OSTI ID:: 1479619

Alternate ID(s):: OSTI ID: 1490637; OSTI ID: 1493266

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 115 Journal Issue: 46; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 22 works

Citation information provided by
Web of Science

References (38)

Biological imaging by soft x-ray diffraction microscopy Shapiro, D.; Thibault, P.; Beetz, T. Proceedings of the National Academy of Sciences, Vol. 102, Issue 43 https://doi.org/10.1073/pnas.0503305102	journal	October 2005
Cheetah : software for high-throughput reduction and analysis of serial femtosecond X-ray diffraction data Barty, Anton; Kirian, Richard A.; Maia, Filipe R. N. C. Journal of Applied Crystallography, Vol. 47, Issue 3 https://doi.org/10.1107/S1600576714007626	journal	May 2014
Near-Optimal Parameters for Tikhonov and Other Regularization Methods O'Leary, Dianne P. SIAM Journal on Scientific Computing, Vol. 23, Issue 4 https://doi.org/10.1137/S1064827599354147	journal	January 2001
High-throughput imaging of heterogeneous cell organelles with an X-ray laser Hantke, Max F.; Hasse, Dirk; Maia, Filipe R. N. C. Nature Photonics, Vol. 8, Issue 12 https://doi.org/10.1038/nphoton.2014.270	journal	November 2014
Single Particle X-ray Diffractive Imaging Bogan, Michael J.; Benner, W. Henry; Boutet, Sébastien Nano Letters, Vol. 8, Issue 1, p. 310-316 https://doi.org/10.1021/nl072728k	journal	January 2008
First lasing and operation of an ångstrom-wavelength free-electron laser Emma, P.; Akre, R.; Arthur, J. Nature Photonics, Vol. 4, Issue 9 https://doi.org/10.1038/nphoton.2010.176	journal	August 2010
New Light on Disordered Ensembles: Ab Initio Structure Determination of One Particle from Scattering Fluctuations of Many Copies Saldin, D. K.; Poon, H. C.; Bogan, M. J. Physical Review Letters, Vol. 106, Issue 11 https://doi.org/10.1103/PhysRevLett.106.115501	journal	March 2011
Reconstruction from limited single-particle diffraction data via simultaneous determination of state, orientation, intensity, and phase Donatelli, Jeffrey J.; Sethian, James A.; Zwart, Peter H. Proceedings of the National Academy of Sciences, Vol. 114, Issue 28 https://doi.org/10.1073/pnas.1708217114	journal	June 2017
Free-electron laser data for multiple-particle fluctuation scattering analysis Pande, Kanupriya; Donatelli, Jeffrey J.; Malmerberg, Erik Scientific Data, Vol. 5, Issue 1 https://doi.org/10.1038/sdata.2018.201	journal	October 2018
Unsupervised classification of single-particle X-ray diffraction snapshots by spectral clustering Yoon, Chun Hong; Schwander, Peter; Abergel, Chantal Optics Express, Vol. 19, Issue 17 https://doi.org/10.1364/OE.19.016542	journal	January 2011
Three-Dimensional Reconstruction of the Giant Mimivirus Particle with an X-Ray Free-Electron Laser Ekeberg, Tomas; Svenda, Martin; Abergel, Chantal Physical Review Letters, Vol. 114, Issue 9 https://doi.org/10.1103/PhysRevLett.114.098102	journal	March 2015
The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus Nandhagopal, N.; Simpson, A. A.; Gurnon, J. R. Proceedings of the National Academy of Sciences, Vol. 99, Issue 23 https://doi.org/10.1073/pnas.232580699	journal	October 2002
Prevention of overfitting in cryo-EM structure determination Scheres, Sjors H. W.; Chen, Shaoxia Nature Methods, Vol. 9, Issue 9 https://doi.org/10.1038/nmeth.2115	journal	July 2012
A Generalized Sampling Theorem Kramer, H. P. Journal of Mathematics and Physics, Vol. 38, Issue 1-4 https://doi.org/10.1002/sapm195938168	journal	April 1959
Single-particle structure determination by correlations of snapshot X-ray diffraction patterns Starodub, D.; Aquila, A.; Bajt, S. Nature Communications, Vol. 3, Issue 1 https://doi.org/10.1038/ncomms2288	journal	January 2012
CASS—CFEL-ASG software suite Foucar, Lutz; Barty, Anton; Coppola, Nicola Computer Physics Communications, Vol. 183, Issue 10 https://doi.org/10.1016/j.cpc.2012.04.023	journal	October 2012
Signal, noise, and resolution in correlated fluctuations from snapshot small-angle x-ray scattering Kirian, Richard A.; Schmidt, Kevin E.; Wang, Xiaoyu Physical Review E, Vol. 84, Issue 1 https://doi.org/10.1103/PhysRevE.84.011921	journal	July 2011
Injector for scattering measurements on fully solvated biospecies Weierstall, U.; Spence, J. C. H.; Doak, R. B. Review of Scientific Instruments, Vol. 83, Issue 3 https://doi.org/10.1063/1.3693040	journal	March 2012
AMO instrumentation for the LCLS X-ray FEL Bozek, J. D. The European Physical Journal Special Topics, Vol. 169, Issue 1 https://doi.org/10.1140/epjst/e2009-00982-y	journal	March 2009
Large format imaging detectors for x-ray free-electron-lasers Hartmann, Robert; Epp, Sascha; Gorke, Hubert SPIE Optics + Optoelectronics, SPIE Proceedings https://doi.org/10.1117/12.887034	conference	May 2011
The Atomic, Molecular and Optical Science instrument at the Linac Coherent Light Source Ferguson, Ken R.; Bucher, Maximilian; Bozek, John D. Journal of Synchrotron Radiation, Vol. 22, Issue 3 https://doi.org/10.1107/S1600577515004646	journal	April 2015
Growth cycle of a virus, PBCV-1, that infects Chlorella-like algae Van Etten, James L.; Burbank, Dwight E.; Xia, Yuannan Virology, Vol. 126, Issue 1 https://doi.org/10.1016/0042-6822(83)90466-X	journal	April 1983
Correlations in Scattered X-Ray Laser Pulses Reveal Nanoscale Structural Features of Viruses Kurta, Ruslan P.; Donatelli, Jeffrey J.; Yoon, Chun Hong Physical Review Letters, Vol. 119, Issue 15, Article No. 158102 https://doi.org/10.1103/PhysRevLett.119.158102	journal	October 2017
Iterative phasing for fluctuation X-ray scattering Donatelli, Jeffrey J.; Zwart, Peter H.; Sethian, James A. Proceedings of the National Academy of Sciences, Vol. 112, Issue 33 https://doi.org/10.1073/pnas.1513738112	journal	August 2015
Three-dimensional structure and function of the Paramecium bursaria chlorella virus capsid Zhang, X.; Xiang, Y.; Dunigan, D. D. Proceedings of the National Academy of Sciences, Vol. 108, Issue 36 https://doi.org/10.1073/pnas.1107847108	journal	August 2011
Structure from fleeting illumination of faint spinning objects in flight Fung, Russell; Shneerson, Valentin; Saldin, Dilano K. Nature Physics, Vol. 5, Issue 1 https://doi.org/10.1038/nphys1129	journal	November 2008
Automated identification and classification of single particle serial femtosecond X-ray diffraction data Andreasson, Jakob; Martin, Andrew V.; Liang, Meng Optics Express, Vol. 22, Issue 3 https://doi.org/10.1364/OE.22.002497	journal	January 2014
Potential for biomolecular imaging with femtosecond X-ray pulses Neutze, Richard; Wouts, Remco; van der Spoel, David Nature, Vol. 406, Issue 6797 https://doi.org/10.1038/35021099	journal	August 2000
Three-dimensional single-particle imaging using angular correlations from X-ray laser data Liu, Haiguang; Poon, Billy K.; Saldin, Dilano K. Acta Crystallographica Section A Foundations of Crystallography, Vol. 69, Issue 4 https://doi.org/10.1107/S0108767313006016	journal	May 2013
Coherent soft X-ray diffraction imaging of coliphage PR772 at the Linac coherent light source Reddy, Hemanth K. N.; Yoon, Chun Hong; Aquila, Andrew Scientific Data, Vol. 4, Issue 1 https://doi.org/10.1038/sdata.2017.79	journal	June 2017
Observation of correlated X-ray scattering at atomic resolution Mendez, Derek; Lane, Thomas J.; Sung, Jongmin Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647 https://doi.org/10.1098/rstb.2013.0315	journal	July 2014
Fluctuation x-ray scattering from biological particles in frozen solution by using synchrotron radiation. Kam, Z.; Koch, M. H.; Bordas, J. Proceedings of the National Academy of Sciences, Vol. 78, Issue 6 https://doi.org/10.1073/pnas.78.6.3559	journal	June 1981
Structure determination of Pt-coated Au dumbbells via fluctuation X-ray scattering Chen, Gang; Modestino, Miguel A.; Poon, Billy K. Journal of Synchrotron Radiation, Vol. 19, Issue 5 https://doi.org/10.1107/S0909049512023801	journal	July 2012
Determination of Macromolecular Structure in Solution by Spatial Correlation of Scattering Fluctuations Kam, Zvi Macromolecules, Vol. 10, Issue 5, p. 927-934 https://doi.org/10.1021/ma60059a009	journal	September 1977
Gas dynamic virtual nozzle for generation of microscopic droplet streams DePonte, D. P.; Weierstall, U.; Schmidt, K. Journal of Physics D: Applied Physics, Vol. 41, Issue 19, Article No. 195505 https://doi.org/10.1088/0022-3727/41/19/195505	journal	September 2008
Calibration methods and performance evaluation for pnCCDs in experiments with FEL radiation Kimmel, N.; Andritschke, R.; Englert, L. SPIE Optics + Optoelectronics, SPIE Proceedings https://doi.org/10.1117/12.887026	conference	May 2011
Large-format, high-speed, X-ray pnCCDs combined with electron and ion imaging spectrometers in a multipurpose chamber for experiments at 4th generation light sources Strüder, Lothar; Epp, Sascha; Rolles, Daniel Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment, Vol. 614, Issue 3 https://doi.org/10.1016/j.nima.2009.12.053	journal	March 2010
Better models by discarding data? Diederichs, K.; Karplus, P. A. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444913001121	journal	June 2013