Protein structure determination by single-wavelength anomalous diffraction phasing of X-ray free-electron laser data

Nass, Karol; Meinhart, Anton; Barends, Thomas R. M.; Foucar, Lutz; Gorel, Alexander; Aquila, Andrew; Botha, Sabine; Doak, R. Bruce; Koglin, Jason; Liang, Mengning; Shoeman, Robert L.; Williams, Garth; Boutet, Sebastien; Schlichting, Ilme

doi:10.1107/S2052252516002980

Title: Protein structure determination by single-wavelength anomalous diffraction phasing of X-ray free-electron laser data

Journal Article · Wed Mar 09 00:00:00 EST 2016 · IUCrJ

DOI:https://doi.org/10.1107/S2052252516002980· OSTI ID:1307373

Nass, Karol ^[1]; Meinhart, Anton ^[1]; Barends, Thomas R. M. ^[1]; Foucar, Lutz ^[1]; Gorel, Alexander ^[1]; Aquila, Andrew ^[2]; Botha, Sabine ^[3]; Doak, R. Bruce ^[1]; Koglin, Jason ^[4]; Liang, Mengning ^[4]; Shoeman, Robert L. ^[1]; Williams, Garth ^[5]; Boutet, Sebastien ^[4]; Schlichting, Ilme ^[1]

Max Planck Institute for Medical Research, Heidelberg (Germany)
European XFEL GmbH, Hamburg (Germany); SLAC National Accelerator Lab., Menlo Park, CA (United States)
Max Planck Institute for Medical Research, Heidelberg (Germany); Univ. of Hamburg, Hamburg (Germany)
SLAC National Accelerator Lab., Menlo Park, CA (United States)
SLAC National Accelerator Lab., Menlo Park, CA (United States); Brookhaven National Lab. (BNL), Upton, NY (United States)

Serial femtosecond crystallography (SFX) at X-ray free-electron lasers (XFELs) offers unprecedented possibilities for macromolecular structure determination of systems that are prone to radiation damage. However, phasing XFEL data de novo is complicated by the inherent inaccuracy of SFX data, and only a few successful examples, mostly based on exceedingly strong anomalous or isomorphous difference signals, have been reported. Here, it is shown that SFX data from thaumatin microcrystals can be successfully phased using only the weak anomalous scattering from the endogenous S atoms. Furthermore, a step-by-step investigation is presented of the particular problems of SAD phasing of SFX data, analysing data from a derivative with a strong anomalous signal as well as the weak signal from endogenous S atoms.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE

OSTI ID:: 1307373

Report Number(s):: AC02-76SF00515; IUCRAJ; PII: S2052252516002980

Journal Information:: IUCrJ, Vol. 3, Issue 3; ISSN 2052-2525

Publisher:: International Union of CrystallographyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 58 works

Citation information provided by
Web of Science

References (53)

PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Use of massively multiple merged data for low-resolution S-SAD phasing and refinement of flavivirus NS1 Akey, David L.; Brown, W. Clay; Konwerski, Jamie R. Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 10 https://doi.org/10.1107/S1399004714017556	journal	September 2014
De novo protein crystal structure determination from X-ray free-electron laser data Barends, Thomas R. M.; Foucar, Lutz; Botha, Sabine Nature, Vol. 505, Issue 7482 https://doi.org/10.1038/nature12773	journal	November 2013
Few-femtosecond time-resolved measurements of X-ray free-electron lasers Behrens, C.; Decker, F. -J.; Ding, Y. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4762	journal	April 2014
High-Resolution Protein Structure Determination by Serial Femtosecond Crystallography Boutet, S.; Lomb, L.; Williams, G. J. Science, Vol. 337, Issue 6092 https://doi.org/10.1126/science.1217737	journal	May 2012
Macromolecular X-ray structure determination using weak, single-wavelength anomalous data Bunkóczi, Gábor; McCoy, Airlie J.; Echols, Nathaniel Nature Methods, Vol. 12, Issue 2 https://doi.org/10.1038/nmeth.3212	journal	December 2014
Femtosecond X-ray protein nanocrystallography Chapman, Henry N.; Fromme, Petra; Barty, Anton Nature, Vol. 470, Issue 7332, p. 73-77 https://doi.org/10.1038/nature09750	journal	February 2011
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
Crystal structure of the pristine peroxidase ferryl center and its relevance to proton-coupled electron transfer Chreifi, Georges; Baxter, Elizabeth L.; Doukov, Tzanko Proceedings of the National Academy of Sciences, Vol. 113, Issue 5 https://doi.org/10.1073/pnas.1521664113	journal	January 2016
Can anomalous signal of sulfur become a tool for solving protein crystal structures? 1 1Edited by I. A. Wilson Dauter, Zbigniew; Dauter, Miroslawa; de La Fortelle, Eric Journal of Molecular Biology, Vol. 289, Issue 1 https://doi.org/10.1006/jmbi.1999.2743	journal	May 1999
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
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
Structure of CPV17 polyhedrin determined by the improved analysis of serial femtosecond crystallographic data Ginn, Helen M.; Messerschmidt, Marc; Ji, Xiaoyun Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7435	journal	March 2015
The CSPAD megapixel x-ray camera at LCLS Hart, Philip; Boutet, Sébastien; Carini, Gabriella SPIE Optical Engineering + Applications, SPIE Proceedings https://doi.org/10.1117/12.930924	conference	October 2012
Accurate macromolecular structures using minimal measurements from X-ray free-electron lasers Hattne, Johan; Echols, Nathaniel; Tran, Rosalie Nature Methods, Vol. 11, Issue 5 https://doi.org/10.1038/nmeth.2887	journal	March 2014
Structure of the hydrophobic protein crambin determined directly from the anomalous scattering of sulphur Hendrickson, Wayne A.; Teeter, Martha M. Nature, Vol. 290, Issue 5802 https://doi.org/10.1038/290107a0	journal	March 1981
Determination of damage-free crystal structure of an X-ray–sensitive protein using an XFEL Hirata, Kunio; Shinzawa-Itoh, Kyoko; Yano, Naomine Nature Methods, Vol. 11, Issue 7 https://doi.org/10.1038/nmeth.2962	journal	May 2014
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Processing of X-ray snapshots from crystals in random orientations Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 8 https://doi.org/10.1107/S1399004714013534	journal	July 2014
Crystal structure of rhodopsin bound to arrestin by femtosecond X-ray laser Kang, Yanyong; Zhou, X. Edward; Gao, Xiang Nature, Vol. 523, Issue 7562 https://doi.org/10.1038/nature14656	journal	July 2015
Femtosecond protein nanocrystallography—data analysis methods Kirian, Richard A.; Wang, Xiaoyu; Weierstall, Uwe Optics Express, Vol. 18, Issue 6 https://doi.org/10.1364/OE.18.005713	journal	January 2010
Structure-factor analysis of femtosecond microdiffraction patterns from protein nanocrystals Kirian, Richard A.; White, Thomas A.; Holton, James M. Acta Crystallographica Section A Foundations of Crystallography, Vol. 67, Issue 2 https://doi.org/10.1107/S0108767310050981	journal	February 2011
PROCHECK: a program to check the stereochemical quality of protein structures Laskowski, R. A.; MacArthur, M. W.; Moss, D. S. Journal of Applied Crystallography, Vol. 26, Issue 2 https://doi.org/10.1107/S0021889892009944	journal	April 1993
The Coherent X-ray Imaging instrument at the Linac Coherent Light Source Liang, Mengning; Williams, Garth J.; Messerschmidt, Marc Journal of Synchrotron Radiation, Vol. 22, Issue 3 https://doi.org/10.1107/S160057751500449X	journal	April 2015
Structures from Anomalous Diffraction of Native Biological Macromolecules Liu, Q.; Dahmane, T.; Zhang, Z. Science, Vol. 336, Issue 6084 https://doi.org/10.1126/science.1218753	journal	May 2012
Multi-crystal native SAD analysis at 6 keV Liu, Qun; Guo, Youzhong; Chang, Yanqi Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 10 https://doi.org/10.1107/S1399004714013376	journal	September 2014
Crystallographic phasing from weak anomalous signals Liu, Qun; Hendrickson, Wayne A. Current Opinion in Structural Biology, Vol. 34 https://doi.org/10.1016/j.sbi.2015.08.003	journal	October 2015
Serial Femtosecond Crystallography of G Protein-Coupled Receptors Liu, W.; Wacker, D.; Gati, C. Science, Vol. 342, Issue 6165 https://doi.org/10.1126/science.1244142	journal	December 2013
An anti-settling sample delivery instrument for serial femtosecond crystallography Lomb, Lukas; Steinbrener, Jan; Bari, Sadia Journal of Applied Crystallography, Vol. 45, Issue 4 https://doi.org/10.1107/S0021889812024557	journal	July 2012
The Coherent X-ray Imaging Data Bank Maia, Filipe R. N. C. Nature Methods, Vol. 9, Issue 9 https://doi.org/10.1038/nmeth.2110	journal	August 2012
On the routine use of soft X-rays in macromolecular crystallography. Part III. The optimal data-collection wavelength Mueller-Dieckmann, Christoph; Panjikar, Santosh; Tucker, Paul A. Acta Crystallographica Section D Biological Crystallography, Vol. 61, Issue 9 https://doi.org/10.1107/S0907444905021475	journal	August 2005
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
HKL2MAP : a graphical user interface for macromolecular phasing with SHELX programs Pape, Thomas; Schneider, Thomas R. Journal of Applied Crystallography, Vol. 37, Issue 5 https://doi.org/10.1107/S0021889804018047	journal	September 2004
Natively Inhibited Trypanosoma brucei Cathepsin B Structure Determined by Using an X-ray Laser Redecke, L.; Nass, K.; DePonte, D. P. Science, Vol. 339, Issue 6116 https://doi.org/10.1126/science.1229663	journal	November 2012
Native SAD is maturing Rose, John P.; Wang, Bi-Cheng; Weiss, Manfred S. IUCrJ, Vol. 2, Issue 4 https://doi.org/10.1107/S2052252515008337	journal	May 2015
New Python-based methods for data processing Sauter, Nicholas K.; Hattne, Johan; Grosse-Kunstleve, Ralf W. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444913000863	journal	June 2013
Protein crystal structure obtained at 2.9 A resolution from injecting bacterial cells into an X-ray free-electron laser beam Sawaya, M. R.; Cascio, D.; Gingery, M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 35 https://doi.org/10.1073/pnas.1413456111	journal	August 2014
Substructure solution with SHELXD Schneider, Thomas R.; Sheldrick, George M. Acta Crystallographica Section D Biological Crystallography, Vol. 58, Issue 10 https://doi.org/10.1107/S0907444902011678	journal	September 2002
Experimental phasing with SHELXC / D / E : combining chain tracing with density modification Sheldrick, George M. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444909038360	journal	March 2010
Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses Suga, Michihiro; Akita, Fusamichi; Hirata, Kunio Nature, Vol. 517, Issue 7532 https://doi.org/10.1038/nature13991	journal	November 2014
Enabling X-ray free electron laser crystallography for challenging biological systems from a limited number of crystals Uervirojnangkoorn, Monarin; Zeldin, Oliver B.; Lyubimov, Artem Y. eLife, Vol. 4 https://doi.org/10.7554/eLife.05421	journal	March 2015
Comparison of phasing methods for sulfur-SAD using in-house chromium radiation: case studies for standard proteins and a 69 kDa protein Watanabe, Nobuhisa; Kitago, Yu; Tanaka, Isao Acta Crystallographica Section D Biological Crystallography, Vol. 61, Issue 11 https://doi.org/10.1107/S0907444905028416	journal	October 2005
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
Fast native-SAD phasing for routine macromolecular structure determination Weinert, Tobias; Olieric, Vincent; Waltersperger, Sandro Nature Methods, Vol. 12, Issue 2 https://doi.org/10.1038/nmeth.3211	journal	December 2014
CrystFEL : a software suite for snapshot serial crystallography White, Thomas A.; Kirian, Richard A.; Martin, Andrew V. Journal of Applied Crystallography, Vol. 45, Issue 2 https://doi.org/10.1107/S0021889812002312	journal	March 2012
An isomorphous replacement method for efficient de novo phasing for serial femtosecond crystallography Yamashita, Keitaro; Pan, Dongqing; Okuda, Tomohiko Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep14017	journal	September 2015
Accurate determination of segmented X-ray detector geometry Yefanov, Oleksandr; Mariani, Valerio; Gati, Cornelius Optics Express, Vol. 23, Issue 22 https://doi.org/10.1364/OE.23.028459	journal	January 2015
Structure of the Angiotensin Receptor Revealed by Serial Femtosecond Crystallography Zhang, Haitao; Unal, Hamiyet; Gati, Cornelius Cell, Vol. 161, Issue 4 https://doi.org/10.1016/j.cell.2015.04.011	journal	May 2015
Exploring the gas access routes in a [NiFeSe] hydrogenase using crystals pressurized with krypton and oxygen Zacarias, Sónia; Temporão, Adriana; Carpentier, Philippe JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 6 https://doi.org/10.1007/s00775-020-01814-y	journal	August 2020
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
Macromolecular X-ray structure determination using weak, single-wavelength anomalous data. Bunkóczi, Gábor; McCoy, Airlie; Echols, Nathaniel Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.52310	text	January 2015
Accurate determination of segmented X-ray detector geometry Yefanov, Oleksandr; Mariani, Valerio; Gati, Cornelius Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2015-04830	text	January 2015
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010

Cited By (22)

Climbing the Data Mountain: Processing of SFX Data Yoon, Chun Hong; White, Thomas A. X-ray Free Electron Lasers https://doi.org/10.1007/978-3-030-00551-1_7	book	January 2018
Serial millisecond crystallography for routine room-temperature structure determination at synchrotrons Weinert, Tobias; Olieric, Natacha; Cheng, Robert Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00630-4	journal	September 2017
Multi-wavelength anomalous diffraction de novo phasing using a two-colour X-ray free-electron laser with wide tunability Gorel, Alexander; Motomura, Koji; Fukuzawa, Hironobu Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00754-7	journal	October 2017
Photoswitching mechanism of a fluorescent protein revealed by time-resolved crystallography and transient absorption spectroscopy Woodhouse, Joyce; Nass Kovacs, Gabriela; Coquelle, Nicolas Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14537-0	journal	February 2020
Hydroxyethyl cellulose matrix applied to serial crystallography Sugahara, Michihiro; Nakane, Takanori; Masuda, Tetsuya Scientific Reports, Vol. 7, Article No. 703 https://doi.org/10.1038/s41598-017-00761-0	journal	April 2017
An inverse free electron laser acceleration-driven Compton scattering X-ray source Gadjev, I.; Sudar, N.; Babzien, M. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-018-36423-y	journal	January 2019
Viscosity-adjustable grease matrices for serial nanocrystallography Sugahara, Michihiro; Motomura, Koji; Suzuki, Mamoru Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-57675-7	journal	January 2020
Unsupervised determination of protein crystal structures Ufimtsev, Ivan S.; Levitt, Michael Proceedings of the National Academy of Sciences, Vol. 116, Issue 22 https://doi.org/10.1073/pnas.1821512116	journal	May 2019
Processing serial crystallography data with CrystFEL : a step-by-step guide White, Thomas A. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2 https://doi.org/10.1107/s205979831801238x	journal	January 2019
Sample delivery for serial crystallography at free-electron lasers and synchrotrons Grünbein, Marie Luise; Nass Kovacs, Gabriela Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2 https://doi.org/10.1107/s205979831801567x	journal	January 2019
Short-wavelength free-electron laser sources and science: a review Seddon, E. A.; Clarke, J. A.; Dunning, D. J. Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2018-00596	text	January 2017
Rapid Sample Delivery for Megahertz Serial Crystallography at X-ray FELs Wiedorn, Max O.; Awel, Salah; Morgan, Andrew J. Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2018-02209	text	January 2018
Rapid sample delivery for megahertz serial crystallography at X-ray FELs Wiedorn, Max O.; Awel, Salah; Morgan, Andrew J. IUCrJ, Vol. 5, Issue 5 https://doi.org/10.1107/S2052252518008369	journal	July 2018
Processing serial crystallography data with CrystFEL : a step-by-step guide White, Thomas A. International Union of Crystallography (IUCr) https://doi.org/10.1107/s205979831801238x/ba5291sup2.txt	text	January 2019
Serial millisecond crystallography for routine room-temperature structure determination at synchrotrons Weinert, Tobias; Olieric, Natacha; Cheng, Robert ETH Zurich https://doi.org/10.3929/ethz-b-000191628	text	January 2017
Rapid sample delivery for megahertz serial crystallography at X-ray FELs Wiedorn, Max Oliver; Awel, Salah; Morgan, Andrew J. TUHH Universitätsbibliothek https://doi.org/10.15480/882.2221	text	January 2018
Climbing the Data Mountain: Processing of SFX Data Yoon, Chun Hong; White, Thomas A. Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2019-00970	text	January 2018
Processing serial crystallography data with CrystFEL : a step-by-step guide White, Thomas A. International Union of Crystallography (IUCr) https://doi.org/10.1107/s205979831801238x/ba5291sup1.pdf	text	January 2019
Short-wavelength free-electron laser sources and science: a review Seddon, E. A.; Clarke, J. A.; Dunning, D. J. Reports on Progress in Physics, Vol. 80, Issue 11 https://doi.org/10.1088/1361-6633/aa7cca	journal	October 2017
De novo protein structure determination by heavy-atom soaking in lipidic cubic phase and SIRAS phasing using serial synchrotron crystallography Botha, S.; Baitan, D.; Jungnickel, K. E. J. Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2018-05499	text	January 2018
Processing serial crystallography data with CrystFEL : a step-by-step guide White, Thomas Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2019-00931	text	January 2019
An inverse free electron laser acceleration-driven Compton scattering X-ray source Gadjev, I.; Sudar, N.; Babzien, M. arXiv https://doi.org/10.48550/arxiv.1711.00974	preprint	January 2017

Similar Records

Serial millisecond crystallography of membrane and soluble protein microcrystals using synchrotron radiation

Journal Article · Wed May 24 00:00:00 EDT 2017 · IUCrJ · OSTI ID:1307373

Martin-Garcia, Jose M.; Conrad, Chelsie E.; Nelson, Garrett; +27 more

Native phasing of x-ray free-electron laser data for a G protein–coupled receptor

Journal Article · Fri Sep 23 00:00:00 EDT 2016 · Science Advances · OSTI ID:1307373

Batyuk, Alexander; Galli, Lorenzo; Ishchenko, Andrii; +24 more

Multi-crystal native-SAD phasing at 5 keV with a helium environment

Journal Article · Fri Oct 21 00:00:00 EDT 2022 · IUCrJ · OSTI ID:1307373

Karasawa, Akira; Andi, Babak; Fuchs, Martin R.; +4 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
serial femtosecond crystallography
SFX
X-ray free-electron lasers
XFELs
SAD phasing
single-wavelength anomalous diffraction

Title: Protein structure determination by single-wavelength anomalous diffraction phasing of X-ray free-electron laser data

Citation Formats

References (53)

Cited By (22)

Similar Records

Related Subjects