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Title: Correlations in Scattered X-Ray Laser Pulses Reveal Nanoscale Structural Features of Viruses

Abstract

We use extremely bright and ultrashort pulses from an x-ray free-electron laser (XFEL) to measure correlations in x rays scattered from individual bioparticles. This allows us to go beyond the traditional crystallography and single-particle imaging approaches for structure investigations. We employ angular correlations to recover the three-dimensional (3D) structure of nanoscale viruses from x-ray diffraction data measured at the Linac Coherent Light Source. Correlations provide us with a comprehensive structural fingerprint of a 3D virus, which we use both for model-based and ab initio structure recovery. The analyses reveal a clear indication that the structure of the viruses deviates from the expected perfect icosahedral symmetry. Lastly, our results anticipate exciting opportunities for XFEL studies of the structure and dynamics of nanoscale objects by means of angular correlations.

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [3];  [7];  [6];  [8];  [6];  [6];  [9];  [6];  [10];  [3];  [6];  [6];  [11];  [12] more »;  [13];  [3];  [2];  [1] « less
  1. European XFEL GmbH, Schenefeld (Germany)
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Center for Advanced Mathematics for Energy Research Applications, Berkeley, CA (United States)
  3. SLAC National Accelerator Lab., Menlo Park, CA (United States)
  4. La Trobe Univ., Melbourne (Australia)
  5. Uppsala Univ., Uppsala (Sweden); European XFEL GmbH, Schenefeld (Germany)
  6. Uppsala Univ., Uppsala (Sweden)
  7. Arizona State Univ., Tempe, AZ (United States)
  8. Uppsala Univ., Uppsala (Sweden); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  9. Center for Advanced Mathematics for Energy Research Applications, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  10. KTH Royal Institute of Technology, Stockholm (Sweden); Uppsala Univ., Uppsala (Sweden)
  11. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany); National Research Nuclear Univ. MePhl (Moscow Engineering Physics Institute), Moscow (Russia)
  12. Brookhaven National Lab. (BNL), Upton, NY (United States)
  13. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany); Max-Planck Institute for the Structure and Dynamics of Matter, Hamburg (Germany)
Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Brookhaven National Lab. (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1408102
Alternate Identifier(s):
OSTI ID: 1399167; OSTI ID: 1421825; OSTI ID: 1436269
Report Number(s):
[BNL-203624-2018-JAAM]
[Journal ID: ISSN 0031-9007; PRLTAO; TRN: US1702931]
Grant/Contract Number:  
[AC02-05CH11231; ERC-2013-SyG 609920; NSF-1231306; R01GM095583; R01GM109019; SC0012704; AC02-76SF00515]
Resource Type:
Accepted Manuscript
Journal Name:
Physical Review Letters
Additional Journal Information:
[ Journal Volume: 119; Journal Issue: 15]; Journal ID: ISSN 0031-9007
Publisher:
American Physical Society (APS)
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; 43 PARTICLE ACCELERATORS; 36 MATERIALS SCIENCE

Citation Formats

Kurta, Ruslan P., Donatelli, Jeffrey J., Yoon, Chun Hong, Berntsen, Peter, Bielecki, Johan, Daurer, Benedikt J., DeMirci, Hasan, Fromme, Petra, Hantke, Max Felix, Maia, Filipe R. N. C., Munke, Anna, Nettelblad, Carl, Pande, Kanupriya, Reddy, Hemanth K. N., Sellberg, Jonas A., Sierra, Raymond G., Svenda, Martin, van der Schot, Gijs, Vartanyants, Ivan A., Williams, Garth J., Xavier, P. Lourdu, Aquila, Andrew, Zwart, Peter H., and Mancuso, Adrian P. Correlations in Scattered X-Ray Laser Pulses Reveal Nanoscale Structural Features of Viruses. United States: N. p., 2017. Web. doi:10.1103/PhysRevLett.119.158102.
Kurta, Ruslan P., Donatelli, Jeffrey J., Yoon, Chun Hong, Berntsen, Peter, Bielecki, Johan, Daurer, Benedikt J., DeMirci, Hasan, Fromme, Petra, Hantke, Max Felix, Maia, Filipe R. N. C., Munke, Anna, Nettelblad, Carl, Pande, Kanupriya, Reddy, Hemanth K. N., Sellberg, Jonas A., Sierra, Raymond G., Svenda, Martin, van der Schot, Gijs, Vartanyants, Ivan A., Williams, Garth J., Xavier, P. Lourdu, Aquila, Andrew, Zwart, Peter H., & Mancuso, Adrian P. Correlations in Scattered X-Ray Laser Pulses Reveal Nanoscale Structural Features of Viruses. United States. doi:10.1103/PhysRevLett.119.158102.
Kurta, Ruslan P., Donatelli, Jeffrey J., Yoon, Chun Hong, Berntsen, Peter, Bielecki, Johan, Daurer, Benedikt J., DeMirci, Hasan, Fromme, Petra, Hantke, Max Felix, Maia, Filipe R. N. C., Munke, Anna, Nettelblad, Carl, Pande, Kanupriya, Reddy, Hemanth K. N., Sellberg, Jonas A., Sierra, Raymond G., Svenda, Martin, van der Schot, Gijs, Vartanyants, Ivan A., Williams, Garth J., Xavier, P. Lourdu, Aquila, Andrew, Zwart, Peter H., and Mancuso, Adrian P. Thu . "Correlations in Scattered X-Ray Laser Pulses Reveal Nanoscale Structural Features of Viruses". United States. doi:10.1103/PhysRevLett.119.158102. https://www.osti.gov/servlets/purl/1408102.
@article{osti_1408102,
title = {Correlations in Scattered X-Ray Laser Pulses Reveal Nanoscale Structural Features of Viruses},
author = {Kurta, Ruslan P. and Donatelli, Jeffrey J. and Yoon, Chun Hong and Berntsen, Peter and Bielecki, Johan and Daurer, Benedikt J. and DeMirci, Hasan and Fromme, Petra and Hantke, Max Felix and Maia, Filipe R. N. C. and Munke, Anna and Nettelblad, Carl and Pande, Kanupriya and Reddy, Hemanth K. N. and Sellberg, Jonas A. and Sierra, Raymond G. and Svenda, Martin and van der Schot, Gijs and Vartanyants, Ivan A. and Williams, Garth J. and Xavier, P. Lourdu and Aquila, Andrew and Zwart, Peter H. and Mancuso, Adrian P.},
abstractNote = {We use extremely bright and ultrashort pulses from an x-ray free-electron laser (XFEL) to measure correlations in x rays scattered from individual bioparticles. This allows us to go beyond the traditional crystallography and single-particle imaging approaches for structure investigations. We employ angular correlations to recover the three-dimensional (3D) structure of nanoscale viruses from x-ray diffraction data measured at the Linac Coherent Light Source. Correlations provide us with a comprehensive structural fingerprint of a 3D virus, which we use both for model-based and ab initio structure recovery. The analyses reveal a clear indication that the structure of the viruses deviates from the expected perfect icosahedral symmetry. Lastly, our results anticipate exciting opportunities for XFEL studies of the structure and dynamics of nanoscale objects by means of angular correlations.},
doi = {10.1103/PhysRevLett.119.158102},
journal = {Physical Review Letters},
number = [15],
volume = [119],
place = {United States},
year = {2017},
month = {10}
}

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Cited by: 20 works
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Figures / Tables:

FIG. 1 FIG. 1: (a),(b) Experimental SAXS profiles $\langle{I}_{i}(q, φ)\rangle$φ,i (log scale) determined for (a) RDVand (b) PR772 viruses. The insets in (a) and (b) display randomly chosen high-intensity singleparticle diffraction patterns for corresponding particles. (c)–(f) Amplitudes of the FCs $\tilde{C}$n(q1, q2) for $n$ = 1,…, 12 determined for (c),(e) RDVand (d,f)more » PR772 viruses at (c,d) q1 = q2 = q and (e,f) at fixed q2 = 0.3 nm−1 as a function of q1.« less

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    Works referencing / citing this record:

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    • Kurta, Ruslan P.; Donatelli, Jeffrey J.; Yoon, Chun Hong
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    • DOI: 10.1063/1.4918726

    Biological imaging by soft x-ray diffraction microscopy
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    • Shapiro, D.; Thibault, P.; Beetz, T.
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    • DOI: 10.1073/pnas.0503305102

    X-ray cross correlation analysis uncovers hidden local symmetries in disordered matter
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    • Wochner, Peter; Gutt, Christian; Autenrieth, Tina
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    Iterative phasing for fluctuation X-ray scattering
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    • Donatelli, Jeffrey J.; Zwart, Peter H.; Sethian, James A.
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    • DOI: 10.1073/pnas.1513738112

    Reconstruction from limited single-particle diffraction data via simultaneous determination of state, orientation, intensity, and phase
    journal, June 2017

    • Donatelli, Jeffrey J.; Sethian, James A.; Zwart, Peter H.
    • Proceedings of the National Academy of Sciences, Vol. 114, Issue 28
    • DOI: 10.1073/pnas.1708217114

    Fluctuation x-ray scattering from biological particles in frozen solution by using synchrotron radiation.
    journal, June 1981

    • Kam, Z.; Koch, M. H.; Bordas, J.
    • Proceedings of the National Academy of Sciences, Vol. 78, Issue 6
    • DOI: 10.1073/pnas.78.6.3559

    Gas dynamic virtual nozzle for generation of microscopic droplet streams
    journal, September 2008

    • DePonte, D. P.; Weierstall, U.; Schmidt, K.
    • Journal of Physics D: Applied Physics, Vol. 41, Issue 19, Article No. 195505
    • DOI: 10.1088/0022-3727/41/19/195505

    Structure determination through correlated fluctuations in x-ray scattering
    journal, November 2012


    Orientation determination in single-particle x-ray coherent diffraction imaging experiments
    journal, August 2013

    • Yefanov, O. M.; Vartanyants, I. A.
    • Journal of Physics B: Atomic, Molecular and Optical Physics, Vol. 46, Issue 16
    • DOI: 10.1088/0953-4075/46/16/164013

    Multiple-wavelength resonant fluctuation x-ray scattering
    journal, July 2016


    Structure of isolated biomolecules obtained from ultrashort x-ray pulses: exploiting the symmetry of random orientations
    journal, March 2009


    Coherent imaging of biological samples with femtosecond pulses at the free-electron laser FLASH
    journal, March 2010


    Limitations of coherent diffractive imaging of single objects due to their damage by intense x-ray radiation
    journal, November 2012


    Solution of the phase problem for coherent scattering from a disordered system of identical particles
    journal, January 2013


    Structural properties of π-π conjugated network in polymer thin films studied by x-ray cross-correlation analysis
    journal, April 2014


    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

    Deducing fast electron density changes in randomly orientated uncrystallized biomolecules in a pump–probe experiment
    journal, July 2014

    • Pande, K.; Schwander, P.; Schmidt, M.
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647
    • DOI: 10.1098/rstb.2013.0332

    Fluctuation X-ray scattering from nanorods in solution reveals weak temperature-dependent orientational ordering
    journal, May 2019


    The correlation averaging of a regularly arranged bacterial cell envelope protein
    journal, August 1982


    Imaging Atomic Structure and Dynamics with Ultrafast X-ray Scattering
    journal, June 2007


    High-Resolution Protein Structure Determination by Serial Femtosecond Crystallography
    journal, May 2012


    Microholography of Living Organisms
    journal, October 1982


    Software Platform for European XFEL: Towards Online Experimental Data Analysis
    journal, November 2018

    • Bobkov, S. A.; Teslyuk, A. B.; Zolotarev, S. I.
    • Lobachevskii Journal of Mathematics, Vol. 39, Issue 9
    • DOI: 10.1134/s1995080218090093

    AMO instrumentation for the LCLS X-ray FEL
    journal, March 2009


    X-Ray Cross-Correlation Analysis of Disordered Ensembles of Particles: Potentials and Limitations
    journal, January 2013

    • Kurta, R. P.; Altarelli, M.; Vartanyants, I. A.
    • Advances in Condensed Matter Physics, Vol. 2013
    • DOI: 10.1155/2013/959835

      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.