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Title: Conformational landscape of a virus by single-particle X-ray scattering

Abstract

Using a manifold-based analysis of experimental diffraction snapshots from an X-ray free electron laser, we determine the three-dimensional structure and conformational landscape of the PR772 virus to a detector-limited resolution of 9 nm. Our results indicate that a single conformational coordinate controls reorganization of the genome, growth of a tubular structure from a portal vertex and release of the genome. Furthermore, these results demonstrate that single-particle X-ray scattering has the potential to shed light on key biological processes.

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [2];  [3];  [4];  [2]; ORCiD logo [1]
  1. Univ. of Wisconsin, Milwaukee, WI (United States)
  2. SLAC National Accelerator Lab., Menlo Park, CA (United States)
  3. Arizona State Univ., Tempe, AZ (United States)
  4. Brookhaven National Lab. (BNL), Upton, NY (United States)
Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States); Univ. of Wisconsin, Milwaukee, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1394091
Alternate Identifier(s):
OSTI ID: 1598200
Grant/Contract Number:  
AC02-76SF00515; SC0002164
Resource Type:
Accepted Manuscript
Journal Name:
Nature Methods
Additional Journal Information:
Journal Volume: 14; Journal Issue: 9; Journal ID: ISSN 1548-7091
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; 97 MATHEMATICS AND COMPUTING

Citation Formats

Hosseinizadeh, Ahmad, Mashayekhi, Ghoncheh, Copperman, Jeremy, Schwander, Peter, Dashti, Ali, Sepehr, Reyhaneh, Fung, Russell, Schmidt, Marius, Yoon, Chun Hong, Hogue, Brenda G., Williams, Garth J., Aquila, Andrew, and Ourmazd, Abbas. Conformational landscape of a virus by single-particle X-ray scattering. United States: N. p., 2017. Web. doi:10.1038/NMETH.4395.
Hosseinizadeh, Ahmad, Mashayekhi, Ghoncheh, Copperman, Jeremy, Schwander, Peter, Dashti, Ali, Sepehr, Reyhaneh, Fung, Russell, Schmidt, Marius, Yoon, Chun Hong, Hogue, Brenda G., Williams, Garth J., Aquila, Andrew, & Ourmazd, Abbas. Conformational landscape of a virus by single-particle X-ray scattering. United States. doi:10.1038/NMETH.4395.
Hosseinizadeh, Ahmad, Mashayekhi, Ghoncheh, Copperman, Jeremy, Schwander, Peter, Dashti, Ali, Sepehr, Reyhaneh, Fung, Russell, Schmidt, Marius, Yoon, Chun Hong, Hogue, Brenda G., Williams, Garth J., Aquila, Andrew, and Ourmazd, Abbas. Mon . "Conformational landscape of a virus by single-particle X-ray scattering". United States. doi:10.1038/NMETH.4395. https://www.osti.gov/servlets/purl/1394091.
@article{osti_1394091,
title = {Conformational landscape of a virus by single-particle X-ray scattering},
author = {Hosseinizadeh, Ahmad and Mashayekhi, Ghoncheh and Copperman, Jeremy and Schwander, Peter and Dashti, Ali and Sepehr, Reyhaneh and Fung, Russell and Schmidt, Marius and Yoon, Chun Hong and Hogue, Brenda G. and Williams, Garth J. and Aquila, Andrew and Ourmazd, Abbas},
abstractNote = {Using a manifold-based analysis of experimental diffraction snapshots from an X-ray free electron laser, we determine the three-dimensional structure and conformational landscape of the PR772 virus to a detector-limited resolution of 9 nm. Our results indicate that a single conformational coordinate controls reorganization of the genome, growth of a tubular structure from a portal vertex and release of the genome. Furthermore, these results demonstrate that single-particle X-ray scattering has the potential to shed light on key biological processes.},
doi = {10.1038/NMETH.4395},
journal = {Nature Methods},
number = 9,
volume = 14,
place = {United States},
year = {2017},
month = {8}
}

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Cited by: 17 works
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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
  • DOI: 10.1038/ncomms5061

Single mimivirus particles intercepted and imaged with an X-ray laser
journal, February 2011

  • Seibert, M. Marvin; Ekeberg, Tomas; Maia, Filipe R. N. C.
  • Nature, Vol. 470, Issue 7332
  • DOI: 10.1038/nature09748

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
  • DOI: 10.1107/S0021889812002312

Graph Laplacian Tomography From Unknown Random Projections
journal, October 2008

  • Coifman, R. R.; Shkolnisky, Y.; Sigworth, F. J.
  • IEEE Transactions on Image Processing, Vol. 17, Issue 10
  • DOI: 10.1109/TIP.2008.2002305

High-throughput imaging of heterogeneous cell organelles with an X-ray laser
journal, November 2014


A pH-Induced Structural Change in Bromegrass Mosaic Virus
journal, January 1964


Extending the methodology of X-ray crystallography to allow imaging of micrometre-sized non-crystalline specimens
journal, July 1999

  • Miao, Jianwei; Charalambous, Pambos; Kirz, Janos
  • Nature, Vol. 400, Issue 6742
  • DOI: 10.1038/22498

Molecular Microscopy: Fundamental Limitations
journal, December 1970


Shake, rattle, and roll: Impact of the dynamics of flavivirus particles on their interactions with the host
journal, May 2015


Three-Dimensional Reconstruction of the Giant Mimivirus Particle with an X-Ray Free-Electron Laser
journal, March 2015


Activation of the A2A adenosine G-protein-coupled receptor by conformational selection
journal, May 2016


Efficient Computation of k-Nearest Neighbour Graphs for Large High-Dimensional Data Sets on GPU Clusters
journal, September 2013


Prevention of overfitting in cryo-EM structure determination
journal, July 2012

  • Scheres, Sjors H. W.; Chen, Shaoxia
  • Nature Methods, Vol. 9, Issue 9
  • DOI: 10.1038/nmeth.2115

The adaptive gain integrating pixel detector AGIPD a detector for the European XFEL
journal, May 2011

  • Henrich, B.; Becker, J.; Dinapoli, R.
  • Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment, Vol. 633
  • DOI: 10.1016/j.nima.2010.06.107

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
  • DOI: 10.1098/rstb.2013.0567

Dragonfly : an implementation of the expand–maximize–compress algorithm for single-particle imaging
journal, June 2016

  • Ayyer, Kartik; Lan, Ti-Yen; Elser, Veit
  • Journal of Applied Crystallography, Vol. 49, Issue 4
  • DOI: 10.1107/S1600576716008165

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
  • DOI: 10.1098/rstb.2013.0326

Membrane-assisted viral DNA ejection
journal, March 2017

  • Santos-Pérez, Isaac; Oksanen, Hanna M.; Bamford, Dennis H.
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1861, Issue 3
  • DOI: 10.1016/j.bbagen.2016.12.013

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
  • DOI: 10.1364/OE.20.012799

Microholography of Living Organisms
journal, October 1982


Phase retrieval algorithms: a comparison
journal, January 1982


How Should We Think About the Ribosome?
journal, June 2012


Nonequilibrium Equality for Free Energy Differences
journal, April 1997


Conformational selection or induced-fit? 50 years of debate resolved
journal, September 2011

  • Changeux, Jean-Pierre; Edelstein, Stuart
  • F1000 Biology Reports, Vol. 3
  • DOI: 10.3410/B3-19

Structure of the Immature Dengue Virus at Low pH Primes Proteolytic Maturation
journal, March 2008


Principles of maximum entropy and maximum caliber in statistical physics
journal, July 2013


Equilibrium free-energy differences from nonequilibrium measurements: A master-equation approach
journal, November 1997


Nonlinear Laplacian spectral analysis for time series with intermittency and low-frequency variability
journal, January 2012

  • Giannakis, D.; Majda, A. J.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 7
  • DOI: 10.1073/pnas.1118984109

Reconstruction algorithm for single-particle diffraction imaging experiments
journal, August 2009


Single-particle structure determination by X-ray free-electron lasers: Possibilities and challenges
journal, July 2015

  • Hosseinizadeh, A.; Dashti, A.; Schwander, P.
  • Structural Dynamics, Vol. 2, Issue 4
  • DOI: 10.1063/1.4919740

Path-ensemble averages in systems driven far from equilibrium
journal, March 2000


Mechanism of Membranous Tunnelling Nanotube Formation in Viral Genome Delivery
journal, September 2013


Cryptotomography: Reconstructing 3D Fourier Intensities from Randomly Oriented Single-Shot Diffraction Patterns
journal, June 2010


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
  • DOI: 10.1364/OE.20.012827

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
  • DOI: 10.1038/nphys1129

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
  • DOI: 10.1038/35021099

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
  • DOI: 10.1038/sdata.2017.79

Assembly, stability and dynamics of virus capsids
journal, March 2013


Geometric diffusions as a tool for harmonic analysis and structure definition of data: Diffusion maps
journal, May 2005

  • Coifman, R. R.; Lafon, S.; Lee, A. B.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 21
  • DOI: 10.1073/pnas.0500334102

X-ray image reconstruction from a diffraction pattern alone
journal, October 2003


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
  • DOI: 10.1073/pnas.1419276111

    Works referencing / citing this record:

    A statistical approach to detect protein complexes at X-ray free electron laser facilities
    journal, December 2018

    • Pietrini, Alberto; Bielecki, Johan; Timneanu, Nicusor
    • Communications Physics, Vol. 1, Issue 1
    • DOI: 10.1038/s42005-018-0092-6

    A statistical approach to detect protein complexes at X-ray free electron laser facilities
    journal, December 2018

    • Pietrini, Alberto; Bielecki, Johan; Timneanu, Nicusor
    • Communications Physics, Vol. 1, Issue 1
    • DOI: 10.1038/s42005-018-0092-6