Structure of CPV17 polyhedrin determined by the improved analysis of serial femtosecond crystallographic data
Abstract
The X-ray free-electron laser (XFEL) allows the analysis of small weakly diffracting protein crystals, but has required very many crystals to obtain good data. Here we use an XFEL to determine the room temperature atomic structure for the smallest cytoplasmic polyhedrosis virus polyhedra yet characterized, which we failed to solve at a synchrotron. These protein microcrystals, roughly a micron across, accrue within infected cells. We use a new physical model for XFEL diffraction, which better estimates the experimental signal, delivering a high-resolution XFEL structure (1.75 Å), using fewer crystals than previously required for this resolution. The crystal lattice and protein core are conserved compared with a polyhedrin with less than 10% sequence identity. We explain how the conserved biological phenotype, the crystal lattice, is maintained in the face of extreme environmental challenge and massive evolutionary divergence. Our improved methods should open up more challenging biological samples to XFEL analysis.
- Authors:
-
- Univ. of Oxford (United Kingdom). Division of Structural Biology, The Wellcome Trust Centre for Human Genetics.
- SLAC National Accelerator Lab., Menlo Park, CA (United States)
- Univ. of Oxford (United Kingdom). Division of Structural Biology, The Wellcome Trust Centre for Human Genetics; Yale School of Medicine, New Haven, CT (United States). Molecular Biophysics and Biochemistry
- Harwell Science and Innovation Campus, Didcot, Oxfordshire (United Kingdom). Diamond House.
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division.
- Univ. of Oxford (United Kingdom). Division of Structural Biology, The Wellcome Trust Centre for Human Genetics; Harwell Science and Innovation Campus, Didcot, Oxfordshire (United Kingdom). Diamond House.
- Publication Date:
- Research Org.:
- SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1190163
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Volume: 6; Related Information: Portions of this research were carried out at the Linac Coherent Light Source (LCLS) at the SLAC National Accelerator Laboratory. LCLS is an Office of Science User Facility operated for the U.S. Department of Energy Office of Science by Stanford University.; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 74 ATOMIC AND MOLECULAR PHYSICS; biological sciences; biophysics; virology
Citation Formats
Ginn, Helen M., Messerschmidt, Marc, Ji, Xiaoyun, Zhang, Hanwen, Axford, Danny, Gildea, Richard J., Winter, Graeme, Brewster, Aaron S., Hattne, Johan, Wagner, Armin, Grimes, Jonathan M., Evans, Gwyndaf, Sauter, Nicholas K., Sutton, Geoff, and Stuart, David I. Structure of CPV17 polyhedrin determined by the improved analysis of serial femtosecond crystallographic data. United States: N. p., 2015.
Web. doi:10.1038/ncomms7435.
Ginn, Helen M., Messerschmidt, Marc, Ji, Xiaoyun, Zhang, Hanwen, Axford, Danny, Gildea, Richard J., Winter, Graeme, Brewster, Aaron S., Hattne, Johan, Wagner, Armin, Grimes, Jonathan M., Evans, Gwyndaf, Sauter, Nicholas K., Sutton, Geoff, & Stuart, David I. Structure of CPV17 polyhedrin determined by the improved analysis of serial femtosecond crystallographic data. United States. https://doi.org/10.1038/ncomms7435
Ginn, Helen M., Messerschmidt, Marc, Ji, Xiaoyun, Zhang, Hanwen, Axford, Danny, Gildea, Richard J., Winter, Graeme, Brewster, Aaron S., Hattne, Johan, Wagner, Armin, Grimes, Jonathan M., Evans, Gwyndaf, Sauter, Nicholas K., Sutton, Geoff, and Stuart, David I. Mon .
"Structure of CPV17 polyhedrin determined by the improved analysis of serial femtosecond crystallographic data". United States. https://doi.org/10.1038/ncomms7435. https://www.osti.gov/servlets/purl/1190163.
@article{osti_1190163,
title = {Structure of CPV17 polyhedrin determined by the improved analysis of serial femtosecond crystallographic data},
author = {Ginn, Helen M. and Messerschmidt, Marc and Ji, Xiaoyun and Zhang, Hanwen and Axford, Danny and Gildea, Richard J. and Winter, Graeme and Brewster, Aaron S. and Hattne, Johan and Wagner, Armin and Grimes, Jonathan M. and Evans, Gwyndaf and Sauter, Nicholas K. and Sutton, Geoff and Stuart, David I.},
abstractNote = {The X-ray free-electron laser (XFEL) allows the analysis of small weakly diffracting protein crystals, but has required very many crystals to obtain good data. Here we use an XFEL to determine the room temperature atomic structure for the smallest cytoplasmic polyhedrosis virus polyhedra yet characterized, which we failed to solve at a synchrotron. These protein microcrystals, roughly a micron across, accrue within infected cells. We use a new physical model for XFEL diffraction, which better estimates the experimental signal, delivering a high-resolution XFEL structure (1.75 Å), using fewer crystals than previously required for this resolution. The crystal lattice and protein core are conserved compared with a polyhedrin with less than 10% sequence identity. We explain how the conserved biological phenotype, the crystal lattice, is maintained in the face of extreme environmental challenge and massive evolutionary divergence. Our improved methods should open up more challenging biological samples to XFEL analysis.},
doi = {10.1038/ncomms7435},
journal = {Nature Communications},
number = ,
volume = 6,
place = {United States},
year = {Mon Mar 09 00:00:00 EDT 2015},
month = {Mon Mar 09 00:00:00 EDT 2015}
}
Web of Science
Works referenced in this record:
Oscillation camera data processing: reflecting range and prediction of partiality. 2. Monochromatized synchrotron X-radiation from a singly bent triangular monochromator
journal, October 1982
- Greenhough, T. J.; Helliwell, J. R.
- Journal of Applied Crystallography, Vol. 15, Issue 5
Linking Crystallographic Model and Data Quality
journal, May 2012
- Karplus, P. A.; Diederichs, K.
- Science, Vol. 336, Issue 6084
Reversible lattice repacking illustrates the temperature dependence of macromolecular interactions
journal, August 2001
- Juers, Douglas H.; Matthews, Brian W.
- Journal of Molecular Biology, Vol. 311, Issue 4
The Buccaneer software for automated model building. 1. Tracing protein chains
journal, August 2006
- Cowtan, Kevin
- Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 9
On the limited memory BFGS method for large scale optimization
journal, August 1989
- Liu, Dong C.; Nocedal, Jorge
- Mathematical Programming, Vol. 45, Issue 1-3
The molecular organization of cypovirus polyhedra
journal, March 2007
- Coulibaly, Fasséli; Chiu, Elaine; Ikeda, Keiko
- Nature, Vol. 446, Issue 7131
Crystal structure of cat muscle pyruvate kinase at a resolution of 2.6 Å
journal, October 1979
- Stuart, David I.; Levine, Michael; Muirhead, Hilary
- Journal of Molecular Biology, Vol. 134, Issue 1
A simplified description of X-ray free-electron lasers
journal, January 2011
- Margaritondo, G.; Rebernik Ribic, Primoz
- Journal of Synchrotron Radiation, Vol. 18, Issue 2
Processing and post-refinement of oscillation camera data
journal, December 1979
- Rossmann, M. G.; Leslie, A. G. W.; Abdel-Meguid, S. S.
- Journal of Applied Crystallography, Vol. 12, Issue 6
THE GENETICS AND GENOMICS OF THE SILKWORM, BOMBYX MORI
journal, January 2005
- Goldsmith, Marian R.; Shimada, Toru; Abe, Hiroaki
- Annual Review of Entomology, Vol. 50, Issue 1
De novo protein crystal structure determination from X-ray free-electron laser data
journal, November 2013
- Barends, Thomas R. M.; Foucar, Lutz; Botha, Sabine
- Nature, Vol. 505, Issue 7482
First lasing and operation of an ångstrom-wavelength free-electron laser
journal, August 2010
- Emma, P.; Akre, R.; Arthur, J.
- Nature Photonics, Vol. 4, Issue 9
Lipidic cubic phase injector facilitates membrane protein serial femtosecond crystallography
journal, February 2014
- Weierstall, Uwe; James, Daniel; Wang, Chong
- Nature Communications, Vol. 5, Issue 1
Coot model-building tools for molecular graphics
journal, November 2004
- Emsley, Paul; Cowtan, Kevin
- Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
The Coherent X-ray Imaging Data Bank
journal, August 2012
- Maia, Filipe R. N. C.
- Nature Methods, Vol. 9, Issue 9
New Python-based methods for data processing
journal, June 2013
- Sauter, Nicholas K.; Hattne, Johan; Grosse-Kunstleve, Ralf W.
- Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7
High-Resolution Protein Structure Determination by Serial Femtosecond Crystallography
journal, May 2012
- Boutet, S.; Lomb, L.; Williams, G. J.
- Science, Vol. 337, Issue 6092
Processing of X-ray snapshots from crystals in random orientations
journal, July 2014
- Kabsch, Wolfgang
- Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 8
REFMAC 5 for the refinement of macromolecular crystal structures
journal, March 2011
- Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A.
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
Femtosecond X-ray protein nanocrystallography
journal, February 2011
- Chapman, Henry N.; Fromme, Petra; Barty, Anton
- Nature, Vol. 470, Issue 7332, p. 73-77
Current status and prospects on microbial control in Japan
journal, July 2007
- Kunimi, Yasuhisa
- Journal of Invertebrate Pathology, Vol. 95, Issue 3
PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
Alkaline hydrolysis of the disulfide bonds of ovomucoid and of low molecular weight aliphatic and aromatic disulfides
journal, January 1971
- Donovan, John W.; White, Thomas M.
- Biochemistry, Vol. 10, Issue 1
Polyhedrin Structure
journal, August 1986
- Rohrmann, G. F.
- Journal of General Virology, Vol. 67, Issue 8
Breaking the indexing ambiguity in serial crystallography
journal, December 2013
- Brehm, Wolfgang; Diederichs, Kay
- Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 1
Improving baculovirus recombination
journal, January 2003
- Zhao, Y.
- Nucleic Acids Research, Vol. 31, Issue 2
Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein
journal, December 2014
- Tenboer, Jason; Basu, Shibom; Zatsepin, Nadia
- Science, Vol. 346, Issue 6214
Three-dimensional Fourier Synthesis of Tosyl-elastase at 3.5 Å Resolution
journal, February 1970
- Watson, H. C.; Shotton, D. M.; Cox, Joyce M.
- Nature, Vol. 225, Issue 5235
Crystal lattice as biological phenotype for insect viruses
journal, October 2005
- Anduleit, Karin; Sutton, Geoff; Diprose, Jonathan M.
- Protein Science, Vol. 14, Issue 10
Integration, scaling, space-group assignment and post-refinement
journal, January 2010
- Kabsch, Wolfgang
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 133-144
Morphological and Molecular Characterization of a Cypovirus (Reoviridae) from the Mosquito Uranotaenia sapphirina (Diptera: Culicidae)
journal, July 2005
- Shapiro, A.; Green, T.; Rao, S.
- Journal of Virology, Vol. 79, Issue 15
How baculovirus polyhedra fit square pegs into round holes to robustly package viruses
journal, December 2009
- Ji, Xiaoyun; Sutton, Geoff; Evans, Gwyndaf
- The EMBO Journal, Vol. 29, Issue 2
Post-refinement method for snapshot serial crystallography
journal, July 2014
- White, Thomas A.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647
Serial Femtosecond Crystallography of G Protein-Coupled Receptors
journal, December 2013
- Liu, W.; Wacker, D.; Gati, C.
- Science, Vol. 342, Issue 6165
An anti-settling sample delivery instrument for serial femtosecond crystallography
journal, July 2012
- Lomb, Lukas; Steinbrener, Jan; Bari, Sadia
- Journal of Applied Crystallography, Vol. 45, Issue 4
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
Phaser crystallographic software
journal, July 2007
- McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D.
- Journal of Applied Crystallography, Vol. 40, Issue 4
Accurate macromolecular structures using minimal measurements from X-ray free-electron lasers
journal, March 2014
- Hattne, Johan; Echols, Nathaniel; Tran, Rosalie
- Nature Methods, Vol. 11, Issue 5
Fossil evidence of insect pathogens
journal, July 2005
- Poinar, George; Poinar, Roberta
- Journal of Invertebrate Pathology, Vol. 89, Issue 3
Natively Inhibited Trypanosoma brucei Cathepsin B Structure Determined by Using an X-ray Laser
journal, November 2012
- Redecke, L.; Nass, K.; DePonte, D. P.
- Science, Vol. 339, Issue 6116
New methods for indexing multi-lattice diffraction data
journal, September 2014
- Gildea, Richard J.; Waterman, David G.; Parkhurst, James M.
- Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 10
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation
journal, February 2021
- Tillu, Vikas A.; Rae, James; Gao, Ya
- Nature Communications, Vol. 12, Issue 1
PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Apollo - University of Cambridge Repository
Works referencing / citing this record:
Climbing the Data Mountain: Processing of SFX Data
book, January 2018
- Yoon, Chun Hong; White, Thomas A.
- X-ray Free Electron Lasers
Cell-line-dependent crystal morphology and sublocalization of the Thyrinteina arnobia cypovirus polyhedrin expressed from a recombinant baculovirus
journal, April 2019
- Silva, Leonardo A.; Ardisson-Araújo, Daniel M. P.; Morgado, Fabricio S.
- Archives of Virology, Vol. 164, Issue 6
High-speed fixed-target serial virus crystallography
journal, June 2017
- Roedig, Philip; Ginn, Helen M.; Pakendorf, Tim
- Nature Methods, Vol. 14, Issue 8
Atomic structure of granulin determined from native nanocrystalline granulovirus using an X-ray free-electron laser
journal, February 2017
- Gati, Cornelius; Oberthuer, Dominik; Yefanov, Oleksandr
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 9
X-ray free-electron laser: opportunities for drug discovery
journal, July 2018
- Cheng, Robert; Abela, Rafael; Hennig, Michael
- Acta Crystallographica Section A Foundations and Advances, Vol. 74, Issue a1
In cellulo serial crystallography of alcohol oxidase crystals inside yeast cells
journal, January 2016
- Jakobi, Arjen J.; Passon, Daniel M.; Knoops, Kèvin
- IUCrJ, Vol. 3, Issue 2
Processing serial crystallography data with CrystFEL : a step-by-step guide
journal, January 2019
- White, Thomas A.
- Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2
Serial Femtosecond Crystallography
text, January 2015
- Chapman, Henry N.
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Megahertz Data Collection from Protein Microcrystals at an X-Ray Free-Electron Laser
text, January 2018
- Grünbein, Marie Luise; Bielecki, Johan; Gorel, Alexander
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Demonstration of femtosecond X-ray pump X-ray probe diffraction on protein crystals
text, January 2018
- Opara, Nadia L.; Mohacsi, Istvan; Makita, Mikako
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Megahertz data collection from protein microcrystals at an X-ray free-electron laser
journal, August 2018
- Grünbein, Marie Luise; Bielecki, Johan; Gorel, Alexander
- Nature Communications, Vol. 9, Issue 1
X-ray free electron laser: opportunities for drug discovery
journal, November 2017
- Cheng, Robert K. Y.; Abela, Rafael; Hennig, Michael
- Essays in Biochemistry, Vol. 61, Issue 5
Demonstration of femtosecond X-ray pump X-ray probe diffraction on protein crystals
journal, September 2018
- Opara, Nadia L.; Mohacsi, Istvan; Makita, Mikako
- Structural Dynamics, Vol. 5, Issue 5
Processing serial crystallography data with CrystFEL : a step-by-step guide
text, January 2019
- White, Thomas A.
- International Union of Crystallography (IUCr)
Climbing the Data Mountain: Processing of SFX Data
text, January 2018
- Yoon, Chun Hong; White, Thomas A.
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Serial Femtosecond Crystallography
journal, November 2015
- Chapman, Henry N.
- Synchrotron Radiation News, Vol. 28, Issue 6
Processing serial crystallography data with CrystFEL : a step-by-step guide
text, January 2019
- White, Thomas A.
- International Union of Crystallography (IUCr)
Processing serial crystallography data with CrystFEL : a step-by-step guide
text, January 2019
- White, Thomas
- Deutsches Elektronen-Synchrotron, DESY, Hamburg