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Title: Atomic structure of granulin determined from native nanocrystalline granulovirus using an X-ray free-electron laser

Abstract

To understand how molecules function in biological systems, new methods are required to obtain atomic resolution structures from biological material under physiological conditions. Intense femtosecond-duration pulses from X-ray free-electron lasers (XFELs) can outrun most damage processes, vastly increasing the tolerable dose before the specimen is destroyed. This in turn allows structure determination from crystals much smaller and more radiation sensitive than previously considered possible, allowing data collection from room temperature structures and avoiding structural changes due to cooling. Regardless, high-resolution structures obtained from XFEL data mostly use crystals far larger than 1 μm3 in volume, whereas the X-ray beam is often attenuated to protect the detector from damage caused by intense Bragg spots. Here, we describe the 2 Å resolution structure of native nanocrystalline granulovirus occlusion bodies (OBs) that are less than 0.016 μm3 in volume using the full power of the Linac Coherent Light Source (LCLS) and a dose up to 1.3 GGy per crystal. The crystalline shell of granulovirus OBs consists, on average, of about 9,000 unit cells, representing the smallest protein crystals to yield a high-resolution structure by X-ray crystallography to date. The XFEL structure shows little to no evidence of radiation damage and is more completemore » than a model determined using synchrotron data from recombinantly produced, much larger, cryocooled granulovirus granulin microcrystals. Furthermore, our measurements suggest that it should be possible, under ideal experimental conditions, to obtain data from protein crystals with only 100 unit cells in volume using currently available XFELs and suggest that single-molecule imaging of individual biomolecules could almost be within reach.« less

Authors:
 [1];  [2];  [2]; ORCiD logo [3];  [2];  [4];  [4];  [5];  [6];  [5];  [2];  [7];  [8];  [9];  [10];  [11];  [2];  [11];  [11];  [12] more »;  [13];  [14];  [15];  [11];  [13];  [16];  [11];  [2];  [17];  [11];  [11];  [11];  [18];  [19];  [4];  [2]; ORCiD logo [20] « less
+ Show Author Affiliations
  1. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany); MRC Lab. of Molecular Biology, Cambridge (United Kingdom)
  2. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany)
  3. The Univ. of Auckland, Auckland (New Zealand); Friedrich Miescher Institute for Biomedical Research, Basel (Switzerland)
  4. The Univ. of Auckland, Auckland (New Zealand)
  5. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany); European XFEL GmbH, Hamburg (Germany)
  6. Arizona State Univ., Tempe, AZ (United States); Paul Scherrer Inst. (PSI), Villigen (Switzerland)
  7. Max Planck Institute for Medical Research, Heidelberg (Germany); Univ. of Hamburg, Hamburg (Germany)
  8. SLAC National Accelerator Lab., Menlo Park, CA (United States)
  9. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany); SLAC National Accelerator Lab., Menlo Park, CA (United States)
  10. Arizona State Univ., Tempe, AZ (United States); Max Planck Institute for Medical Research, Heidelberg (Germany)
  11. Arizona State Univ., Tempe, AZ (United States)
  12. Arizona State Univ., Tempe, AZ (United States); Univ. of Wisconsin-Milwaukee, Milwaukee, WI (United States)
  13. Max Planck Institute for Medical Research, Heidelberg (Germany)
  14. SLAC National Accelerator Lab., Menlo Park, CA (United States); National Science Foundation BioXFEL Science and Technology Center, Buffalo, NY (United States)
  15. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany); Paul Scherrer Inst. (PSI), Villigen (Switzerland)
  16. Arizona State Univ., Tempe, AZ (United States); ShanghaiTech Univ., Shanghai (China)
  17. SLAC National Accelerator Lab., Menlo Park, CA (United States); Brookhaven National Lab. (BNL), Upton, NY (United States)
  18. Univ. Basel, Basel (Switzerland)
  19. Julius Kuehn Institute (JKI), Darmstadt (Germany)
  20. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany); Univ. of Hamburg, Hamburg (Germany)
Publication Date:
Research Org.:
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1353189
Grant/Contract Number:  
617095583; UOA1221; AC02-76SF00515
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 114; Journal Issue: 9; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
36 MATERIALS SCIENCE; 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; XFEL; nanocrystals; structural biology; bioimaging; SFX

Citation Formats

Gati, Cornelius, Oberthuer, Dominik, Yefanov, Oleksandr, Bunker, Richard D., Stellato, Francesco, Chiu, Elaine, Yeh, Shin -Mei, Aquila, Andrew, Basu, Shibom, Bean, Richard, Beyerlein, Kenneth R., Botha, Sabine, Boutet, Sebastien, DePonte, Daniel P., Doak, R. Bruce, Fromme, Raimund, Galli, Lorenzo, Grotjohann, Ingo, James, Daniel R., Kupitz, Christopher, Lomb, Lukas, Messerschmidt, Marc, Nass, Karol, Rendek, Kimberly, Shoeman, Robert L., Wang, Dingjie, Weierstall, Uwe, White, Thomas A., Williams, Garth J., Zatsepin, Nadia A., Fromme, Petra, Spence, John C. H., Goldie, Kenneth N., Jehle, Johannes A., Metcalf, Peter, Barty, Anton, and Chapman, Henry N. Atomic structure of granulin determined from native nanocrystalline granulovirus using an X-ray free-electron laser. United States: N. p., 2017. Web. doi:10.1073/pnas.1609243114.
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Gati, Cornelius, Oberthuer, Dominik, Yefanov, Oleksandr, Bunker, Richard D., Stellato, Francesco, Chiu, Elaine, Yeh, Shin -Mei, Aquila, Andrew, Basu, Shibom, Bean, Richard, Beyerlein, Kenneth R., Botha, Sabine, Boutet, Sebastien, DePonte, Daniel P., Doak, R. Bruce, Fromme, Raimund, Galli, Lorenzo, Grotjohann, Ingo, James, Daniel R., Kupitz, Christopher, Lomb, Lukas, Messerschmidt, Marc, Nass, Karol, Rendek, Kimberly, Shoeman, Robert L., Wang, Dingjie, Weierstall, Uwe, White, Thomas A., Williams, Garth J., Zatsepin, Nadia A., Fromme, Petra, Spence, John C. H., Goldie, Kenneth N., Jehle, Johannes A., Metcalf, Peter, Barty, Anton, & Chapman, Henry N. Atomic structure of granulin determined from native nanocrystalline granulovirus using an X-ray free-electron laser. United States. https://doi.org/10.1073/pnas.1609243114
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Gati, Cornelius, Oberthuer, Dominik, Yefanov, Oleksandr, Bunker, Richard D., Stellato, Francesco, Chiu, Elaine, Yeh, Shin -Mei, Aquila, Andrew, Basu, Shibom, Bean, Richard, Beyerlein, Kenneth R., Botha, Sabine, Boutet, Sebastien, DePonte, Daniel P., Doak, R. Bruce, Fromme, Raimund, Galli, Lorenzo, Grotjohann, Ingo, James, Daniel R., Kupitz, Christopher, Lomb, Lukas, Messerschmidt, Marc, Nass, Karol, Rendek, Kimberly, Shoeman, Robert L., Wang, Dingjie, Weierstall, Uwe, White, Thomas A., Williams, Garth J., Zatsepin, Nadia A., Fromme, Petra, Spence, John C. H., Goldie, Kenneth N., Jehle, Johannes A., Metcalf, Peter, Barty, Anton, and Chapman, Henry N. Wed . "Atomic structure of granulin determined from native nanocrystalline granulovirus using an X-ray free-electron laser". United States. https://doi.org/10.1073/pnas.1609243114. https://www.osti.gov/servlets/purl/1353189.
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@article{osti_1353189,
title = {Atomic structure of granulin determined from native nanocrystalline granulovirus using an X-ray free-electron laser},
author = {Gati, Cornelius and Oberthuer, Dominik and Yefanov, Oleksandr and Bunker, Richard D. and Stellato, Francesco and Chiu, Elaine and Yeh, Shin -Mei and Aquila, Andrew and Basu, Shibom and Bean, Richard and Beyerlein, Kenneth R. and Botha, Sabine and Boutet, Sebastien and DePonte, Daniel P. and Doak, R. Bruce and Fromme, Raimund and Galli, Lorenzo and Grotjohann, Ingo and James, Daniel R. and Kupitz, Christopher and Lomb, Lukas and Messerschmidt, Marc and Nass, Karol and Rendek, Kimberly and Shoeman, Robert L. and Wang, Dingjie and Weierstall, Uwe and White, Thomas A. and Williams, Garth J. and Zatsepin, Nadia A. and Fromme, Petra and Spence, John C. H. and Goldie, Kenneth N. and Jehle, Johannes A. and Metcalf, Peter and Barty, Anton and Chapman, Henry N.},
abstractNote = {To understand how molecules function in biological systems, new methods are required to obtain atomic resolution structures from biological material under physiological conditions. Intense femtosecond-duration pulses from X-ray free-electron lasers (XFELs) can outrun most damage processes, vastly increasing the tolerable dose before the specimen is destroyed. This in turn allows structure determination from crystals much smaller and more radiation sensitive than previously considered possible, allowing data collection from room temperature structures and avoiding structural changes due to cooling. Regardless, high-resolution structures obtained from XFEL data mostly use crystals far larger than 1 μm3 in volume, whereas the X-ray beam is often attenuated to protect the detector from damage caused by intense Bragg spots. Here, we describe the 2 Å resolution structure of native nanocrystalline granulovirus occlusion bodies (OBs) that are less than 0.016 μm3 in volume using the full power of the Linac Coherent Light Source (LCLS) and a dose up to 1.3 GGy per crystal. The crystalline shell of granulovirus OBs consists, on average, of about 9,000 unit cells, representing the smallest protein crystals to yield a high-resolution structure by X-ray crystallography to date. The XFEL structure shows little to no evidence of radiation damage and is more complete than a model determined using synchrotron data from recombinantly produced, much larger, cryocooled granulovirus granulin microcrystals. Furthermore, our measurements suggest that it should be possible, under ideal experimental conditions, to obtain data from protein crystals with only 100 unit cells in volume using currently available XFELs and suggest that single-molecule imaging of individual biomolecules could almost be within reach.},
doi = {10.1073/pnas.1609243114},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 9,
volume = 114,
place = {United States},
year = {Wed Feb 15 00:00:00 EST 2017},
month = {Wed Feb 15 00:00:00 EST 2017}
}
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Journal Article:
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https://doi.org/10.1073/pnas.1609243114
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Cited by: 57 works
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Figures / Tables:

Figure 1 Figure 1: Granulovirus OBs contain a single virion surrounded by a crystalline protein layer that diffracts to high resolution. (A) Powder X-ray diffraction from a pellet of granulovirus OBs at 100 K (Materials and Methods). Protein diffraction rings extend to a resolution between 3 and 3.5 Å. The detector panelsmore » on the left with enhanced contrast show evidence of diffraction at even higher resolution. Resolution rings are shown at 4, 3.5, and 3 Å. (B) Freeze etch electron micrograph showing the uniform size distribution of the particles (Materials and Methods). (C) Cryo-EM. The sequence of four 20 e/Å2 exposures shows the effects of radiation damage on granulovirus OBs. The crystalline lattice is visible only in the first image and hydrogen gas bubbles produced by radiolysis eventually reveal the virion. (Scale bar, 100 nm.)« less
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    Ultracompact 3D microfluidics for time-resolved structural biology
    text, January 2020

    • Knoska, Juraj; Adriano, Luigi; Awel, Salah
    • Deutsches Elektronen-Synchrotron, DESY, Hamburg
    • DOI: 10.3204/pubdb-2020-00623

    Megahertz serial crystallography
    text, January 2018

    • Wiedorn, Max Oliver; Oberthür, Dominik; Bean, Richard
    • Nature Publishing Group UK
    • DOI: 10.15480/882.2175

    Ultracompact 3D microfluidics for time-resolved structural biology
    journal, January 2020

    Evaluation of serial crystallographic structure determination within megahertz pulse trains
    text, January 2019

    • Yefanov, Oleksandr; Oberthür, Dominik; Bean, Richard
    • Deutsches Elektronen-Synchrotron, DESY, Hamburg
    • DOI: 10.3204/pubdb-2019-04763

    Controlled beams of shock-frozen, isolated, biological and artificial nanoparticles
    text, January 2020

    • Amin, Muhamed; Estillore, Armando; Roth, Nils
    • Deutsches Elektronen-Synchrotron, DESY, Hamburg
    • DOI: 10.3204/pubdb-2020-01398

    Macromolecular Nanocrystal Structural Analysis with Electron and X-Rays: A Comparative Review
    journal, September 2019

    Controlled beams of shockfrozen, isolated, biological and artificial nanoparticles
    preprint, January 2019

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