Megahertz pulse trains enable multi-hit serial femtosecond crystallography experiments at X-ray free electron lasers

Holmes, Susannah; Kirkwood, Henry J.; Bean, Richard; Giewekemeyer, Klaus; Martin, Andrew V.; Hadian-Jazi, Marjan; Wiedorn, Max O.; Oberthür, Dominik; Marman, Hugh; Adriano, Luigi; Al-Qudami, Nasser; Bajt, Saša; Barák, Imrich; Bari, Sadia; Bielecki, Johan; Brockhauser, Sandor; Coleman, Mathew A.; Cruz-Mazo, Francisco; Danilevski, Cyril; Dörner, Katerina; Gañán-Calvo, Alfonso M.; Graceffa, Rita; Fanghor, Hans; Heymann, Michael; Frank, Matthias; Kaukher, Alexander; Kim, Yoonhee; Kobe, Bostjan; Knoška, Juraj; Laurus, Torsten; Letrun, Romain; Maia, Luis; Messerschmidt, Marc; Metz, Markus; Michelat, Thomas; Mills, Grant; Molodtsov, Serguei; Monteiro, Diana F.; Morgan, Andrew J.; Münnich, Astrid; Peña Murillo, Gisel E.; Previtali, Gianpietro; Round, Adam; Sato, Tokushi; Schubert, Robin; Schulz, Joachim; Shelby, Megan; Seuring, Carolin; Sellberg, Jonas A.; Sikorski, Marcin; Silenzi, Alessandro; Stern, Stephan; Sztuk-Dambietz, Jola; Szuba, Janusz; Trebbin, Martin; Vagovic, Patrick; Ve, Thomas; Weinhausen, Britta; Wrona, Krzysztof; Xavier, Paul Lourdu; Xu, Chen; Yefanov, Oleksandr; Nugent, Keith A.; Chapman, Henry N.; Mancuso, Adrian P.; Barty, Anton; Abbey, Brian; Darmanin, Connie

doi:10.1038/s41467-022-32434-6

Title: Megahertz pulse trains enable multi-hit serial femtosecond crystallography experiments at X-ray free electron lasers

Journal Article · Thu Aug 11 00:00:00 UTC 2022 · Nature Communications

DOI: https://doi.org/10.1038/s41467-022-32434-6 · OSTI ID:1959536

Holmes, Susannah;

; Bean, Richard; Giewekemeyer, Klaus;

; Hadian-Jazi, Marjan; Wiedorn, Max O.; Oberthür, Dominik; Marman, Hugh; Adriano, Luigi; Al-Qudami, Nasser;

;

; Bielecki, Johan;

; Coleman, Mathew A.;

; Danilevski, Cyril; Dörner, Katerina more »

The European X-ray Free Electron Laser (XFEL) and Linac Coherent Light Source (LCLS) II are extremely intense sources of X-rays capable of generating Serial Femtosecond Crystallography (SFX) data at megahertz (MHz) repetition rates. Previous work has shown that it is possible to use consecutive X-ray pulses to collect diffraction patterns from individual crystals. Here, we exploit the MHz pulse structure of the European XFEL to obtain two complete datasets from the same lysozyme crystal, first hit and the second hit, before it exits the beam. The two datasets, separated by <1 µs, yield up to 2.1 Å resolution structures. Comparisons between the two structures reveal no indications of radiation damage or significant changes within the active site, consistent with the calculated dose estimates. This demonstrates MHz SFX can be used as a tool for tracking sub-microsecond structural changes in individual single crystals, a technique we refer to as multi-hit SFX.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: AC52-07NA27344

OSTI ID:: 1959536

Report Number(s):: LLNL-JRNL-844538; 1067757

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 13; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (81)

Estimate your dose: RADDOSE-3D: RADDOSE-3D Bury, Charles S.; Brooks-Bartlett, Jonathan C.; Walsh, Steven P. Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3302	journal	November 2017
The primary and secondary acceptors in bacterial photosynthesis: II. The structure of the Fe2+-Q− complex Feher, G.; Okamura, M. Y. Applied Magnetic Resonance, Vol. 16, Issue 1 https://doi.org/10.1007/BF03161915	journal	January 1999
Quantifying millisecond time-scale exchange in proteins by CPMG relaxation dispersion NMR spectroscopy of side-chain carbonyl groups Hansen, Alexandar L.; Kay, Lewis E. Journal of Biomolecular NMR, Vol. 50, Issue 4 https://doi.org/10.1007/s10858-011-9520-6	journal	June 2011
Membrane protein dynamics studied by X-ray lasers – or why only time will tell Standfuss, Jörg Current Opinion in Structural Biology, Vol. 57 https://doi.org/10.1016/j.sbi.2019.02.001	journal	August 2019
Recent results in time resolved serial femtosecond crystallography at XFELs Orville, Allen M. Current Opinion in Structural Biology, Vol. 65 https://doi.org/10.1016/j.sbi.2020.08.011	journal	December 2020
Assignments, Secondary Structure, Global Fold, and Dynamics of Chemotaxis Y Protein Using Three- and Four-Dimensional Heteronuclear (13C,15N) NMR Spectroscopy Moy, Franklin J.; Lowry, David F.; Matsumura, Philip Biochemistry, Vol. 33, Issue 35 https://doi.org/10.1021/bi00201a022	journal	September 1994
Millisecond-timescale motions contribute to the function of the bacterial response regulator protein Spo0F Feher, Victoria A.; Cavanagh, John Nature, Vol. 400, Issue 6741 https://doi.org/10.1038/22357	journal	July 1999
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
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
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
Lipidic cubic phase injector facilitates membrane protein serial femtosecond crystallography Weierstall, Uwe; James, Daniel; Wang, Chong Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4309	journal	February 2014
Liquid explosions induced by X-ray laser pulses Stan, Claudiu A.; Milathianaki, Despina; Laksmono, Hartawan Nature Physics, Vol. 12, Issue 10 https://doi.org/10.1038/nphys3779	journal	May 2016
Megahertz data collection from protein microcrystals at an X-ray free-electron laser Grünbein, Marie Luise; Bielecki, Johan; Gorel, Alexander Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05953-4	journal	August 2018
Megahertz serial crystallography Wiedorn, Max O.; Oberthür, Dominik; Bean, Richard Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-06156-7	journal	October 2018
Membrane protein megahertz crystallography at the European XFEL Gisriel, Chris; Coe, Jesse; Letrun, Romain Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12955-3	journal	November 2019
Ultracompact 3D microfluidics for time-resolved structural biology Knoška, Juraj; Adriano, Luigi; Awel, Salah Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14434-6	journal	January 2020
Author Correction: Membrane protein megahertz crystallography at the European XFEL Gisriel, Chris; Coe, Jesse; Letrun, Romain Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14436-4	journal	January 2020
Structural dynamics in proteins induced by and probed with X-ray free-electron laser pulses Nass, Karol; Gorel, Alexander; Abdullah, Malik M. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-15610-4	journal	April 2020
Segmented flow generator for serial crystallography at the European X-ray free electron laser Echelmeier, Austin; Cruz Villarreal, Jorvani; Messerschmidt, Marc Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-18156-7	journal	September 2020
MyD88 TIR domain higher-order assembly interactions revealed by microcrystal electron diffraction and serial femtosecond crystallography Clabbers, Max T. B.; Holmes, Susannah; Muusse, Timothy W. Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-22590-6	journal	May 2021
Time-resolved serial femtosecond crystallography at the European XFEL Pandey, Suraj; Bean, Richard; Sato, Tokushi Nature Methods https://doi.org/10.1038/s41592-019-0628-z	journal	November 2019
MHz data collection of a microcrystalline mixture of different jack bean proteins Grünbein, Marie Luise; Bielecki, Johan; Gorel, Alexander Scientific Data, Vol. 6, Issue 1 https://doi.org/10.1038/s41597-019-0010-0	journal	April 2019
Radiation Damage in XFEL: Case study from the oxygen-evolving complex of Photosystem II Amin, Muhamed; Badawi, Ashraf; Obayya, S. S. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep36492	journal	November 2016
Evaluation of serial crystallographic structure determination within megahertz pulse trains Yefanov, Oleksandr; Oberthür, Dominik; Bean, Richard Structural Dynamics, Vol. 6, Issue 6 https://doi.org/10.1063/1.5124387	journal	November 2019
Experimental determination of the radiation dose limit for cryocooled protein crystals Owen, R. L.; Rudino-Pinera, E.; Garman, E. F. Proceedings of the National Academy of Sciences, Vol. 103, Issue 13 https://doi.org/10.1073/pnas.0600973103	journal	March 2006
Atomic structure of granulin determined from native nanocrystalline granulovirus using an X-ray free-electron laser Gati, Cornelius; Oberthuer, Dominik; Yefanov, Oleksandr Proceedings of the National Academy of Sciences, Vol. 114, Issue 9 https://doi.org/10.1073/pnas.1609243114	journal	February 2017
Radiation damage and dose limits in serial synchrotron crystallography at cryo- and room temperatures de la Mora, Eugenio; Coquelle, Nicolas; Bury, Charles S. Proceedings of the National Academy of Sciences, Vol. 117, Issue 8 https://doi.org/10.1073/pnas.1821522117	journal	February 2020
Gas dynamic virtual nozzle for generation of microscopic droplet streams DePonte, D. P.; Weierstall, U.; Schmidt, K. Journal of Physics D: Applied Physics, Vol. 41, Issue 19, Article No. 195505 https://doi.org/10.1088/0022-3727/41/19/195505	journal	September 2008
Femtosecond crystallography of membrane proteins in the lipidic cubic phase Liu, Wei; Wacker, Daniel; Wang, Chong Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647 https://doi.org/10.1098/rstb.2013.0314	journal	July 2014
Radiation damage in protein serial femtosecond crystallography using an x-ray free-electron laser Lomb, Lukas; Barends, Thomas R. M.; Kassemeyer, Stephan Physical Review B, Vol. 84, Issue 21 https://doi.org/10.1103/PhysRevB.84.214111	journal	December 2011
Scaling Laws of an Exploding Liquid Column under an Intense Ultrashort X-Ray Pulse Gañán-Calvo, Alfonso M. Physical Review Letters, Vol. 123, Issue 6 https://doi.org/10.1103/PhysRevLett.123.064501	journal	August 2019
Generation of Steady Liquid Microthreads and Micron-Sized Monodisperse Sprays in Gas Streams Gañán-Calvo, Alfonso M. Physical Review Letters, Vol. 80, Issue 2 https://doi.org/10.1103/PhysRevLett.80.285	journal	January 1998
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
phenix.model_vs_data : a high-level tool for the calculation of crystallographic model and data statistics Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Chen, Vincent B. Journal of Applied Crystallography, Vol. 43, Issue 4 https://doi.org/10.1107/S0021889810015608	journal	May 2010
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
Low-resolution refinement in the program REFMAC Murshudov, G. N. Acta Crystallographica Section A Foundations of Crystallography, Vol. 67, Issue a1 https://doi.org/10.1107/S0108767311096711	journal	August 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
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Outrunning free radicals in room-temperature macromolecular crystallography Owen, Robin L.; Axford, Danny; Nettleship, Joanne E. Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 7 https://doi.org/10.1107/S0907444912012553	journal	June 2012
Crystallographic data processing for free-electron laser sources White, Thomas A.; Barty, Anton; Stellato, Francesco Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444913013620	journal	June 2013
The Rossmann Fourier autoindexing algorithm in MOSFLM Powell, Harold R. Acta Crystallographica Section D Biological Crystallography, Vol. 55, Issue 10 https://doi.org/10.1107/S0907444999009506	journal	October 1999
A beginner's guide to radiation damage Holton, James M. Journal of Synchrotron Radiation, Vol. 16, Issue 2 https://doi.org/10.1107/S0909049509004361	journal	February 2009
New methods for indexing multi-lattice diffraction data Gildea, Richard J.; Waterman, David G.; Parkhurst, James M. Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 10 https://doi.org/10.1107/S1399004714017039	journal	September 2014
Cheetah : software for high-throughput reduction and analysis of serial femtosecond X-ray diffraction data Barty, Anton; Kirian, Richard A.; Maia, Filipe R. N. C. Journal of Applied Crystallography, Vol. 47, Issue 3 https://doi.org/10.1107/S1600576714007626	journal	May 2014
Recent developments in CrystFEL White, Thomas A.; Mariani, Valerio; Brehm, Wolfgang Journal of Applied Crystallography, Vol. 49, Issue 2 https://doi.org/10.1107/S1600576716004751	journal	March 2016
OnDA : online data analysis and feedback for serial X-ray imaging Mariani, Valerio; Morgan, Andrew; Yoon, Chun Hong Journal of Applied Crystallography, Vol. 49, Issue 3 https://doi.org/10.1107/S1600576716007469	journal	May 2016
FELIX: an algorithm for indexing multiple crystallites in X-ray free-electron laser snapshot diffraction images Beyerlein, Kenneth R.; White, Thomas A.; Yefanov, Oleksandr Journal of Applied Crystallography, Vol. 50, Issue 4 https://doi.org/10.1107/S1600576717007506	journal	July 2017
Nanocrystallography measurements of early stage synthetic malaria pigment Dilanian, Ruben A.; Streltsov, Victor; Coughlan, Hannah D. Journal of Applied Crystallography, Vol. 50, Issue 5 https://doi.org/10.1107/S1600576717012663	journal	September 2017
RADDOSE-XFEL : femtosecond time-resolved dose estimates for macromolecular X-ray free-electron laser experiments Dickerson, Joshua L.; McCubbin, Patrick T. N.; Garman, Elspeth F. Journal of Applied Crystallography, Vol. 53, Issue 2 https://doi.org/10.1107/S1600576720000643	journal	February 2020
Bragg coherent diffraction imaging and metrics for radiation damage in protein micro-crystallography Coughlan, H. D.; Darmanin, C.; Kirkwood, H. J. Journal of Synchrotron Radiation, Vol. 24, Issue 1 https://doi.org/10.1107/S1600577516017525	journal	January 2017
The Karabo distributed control system Hauf, Steffen; Heisen, Burkhard; Aplin, Steve Journal of Synchrotron Radiation, Vol. 26, Issue 5 https://doi.org/10.1107/S1600577519006696	journal	August 2019
Lipidic cubic phase serial millisecond crystallography using synchrotron radiation Nogly, Przemyslaw; James, Daniel; Wang, Dingjie IUCrJ, Vol. 2, Issue 2, p. 168-176 https://doi.org/10.1107/S2052252514026487	journal	March 2015
Dose-resolved serial synchrotron and XFEL structures of radiation-sensitive metalloproteins Ebrahim, Ali; Moreno-Chicano, Tadeo; Appleby, Martin V. IUCrJ, Vol. 6, Issue 4 https://doi.org/10.1107/S2052252519003956	journal	May 2019
Specific radiation damage is a lesser concern at room temperature Gotthard, Guillaume; Aumonier, Sylvain; De Sanctis, Daniele IUCrJ, Vol. 6, Issue 4 https://doi.org/10.1107/S205225251900616X	journal	June 2019
TakeTwo: an indexing algorithm suited to still images with known crystal parameters Ginn, Helen Mary; Roedig, Philip; Kuo, Anling Acta Crystallographica Section D Structural Biology, Vol. 72, Issue 8, p. 956-965 https://doi.org/10.1107/S2059798316010706	journal	July 2016
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
Radiation damage in protein crystallography at X-ray free-electron lasers Nass, Karol Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2 https://doi.org/10.1107/S2059798319000317	journal	January 2019
Microfluidic mixing and jetting devices based on SU8 and glass for time-resolved molecular imaging experiments Hejazian, Majid; Balaur, Eugeniu; Flueckiger, Leonie Microfluidics, BioMEMS, and Medical Microsystems XVII https://doi.org/10.1117/12.2508437	conference	March 2019
X-ray laser–induced electron dynamics observed by femtosecond diffraction from nanocrystals of Buckminsterfullerene Abbey, Brian; Dilanian, Ruben A.; Darmanin, Connie Science Advances, Vol. 2, Issue 9 https://doi.org/10.1126/sciadv.1601186	journal	September 2016
Functional protein dynamics on uncharted time scales detected by nanoparticle-assisted NMR spin relaxation Xie, Mouzhe; Yu, Lei; Bruschweiler-Li, Lei Science Advances, Vol. 5, Issue 8 https://doi.org/10.1126/sciadv.aax5560	journal	August 2019
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
Linking Crystallographic Model and Data Quality Karplus, P. A.; Diederichs, K. Science, Vol. 336, Issue 6084 https://doi.org/10.1126/science.1218231	journal	May 2012
Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein Tenboer, Jason; Basu, Shibom; Zatsepin, Nadia Science, Vol. 346, Issue 6214 https://doi.org/10.1126/science.1259357	journal	December 2014
Two-State Allosteric Behavior in a Single-Domain Signaling Protein Volkman, B. F. Science, Vol. 291, Issue 5512 https://doi.org/10.1126/science.291.5512.2429	journal	March 2001
Segmented Flow Generator for Serial Crystallography at the European X-Ray Free Electron Laser Echelmeier, Echelmeier Coherent X-ray Imaging Data Bank (Lawrence Berkeley National Laboratory); ASU, European XFEL https://doi.org/10.11577/1660970	dataset	January 2020
Membrane protein megahertz crystallography at the European XFEL Gisriel, Chris Coherent X-ray Imaging Data Bank (Lawrence Berkeley National Laboratory); CFEL, European XFEL, DESY, Uppsala University, Heidelberg University https://doi.org/10.11577/1721364	dataset	January 2020
MyD88 TIR domain higher-order assembly interactions revealed by microcrystal electron diffraction and serial femtosecond crystallography Clabbers, Max; Holmes, Susannah Coherent X-ray Imaging Data Bank (Lawrence Berkeley National Laboratory); La Trobe University, Stockholm University SLAC https://doi.org/10.11577/1767965	dataset	January 2021
Enzyme intermediates captured “on the fly” by mix-and-inject serial crystallography Olmos, Jose L.; Pandey, Suraj; Martin-Garcia, Jose M. BMC Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12915-018-0524-5	journal	May 2018
Entering an era of dynamic structural biology… Orville, Allen M. BMC Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12915-018-0533-4	journal	May 2018
X-ray imaging with submicrometer resolution employing transparent luminescent screens Koch, Andreas; Raven, Carsten; Spanne, Per Journal of the Optical Society of America A, Vol. 15, Issue 7 https://doi.org/10.1364/JOSAA.15.001940	journal	January 1998
Time-resolved protein nanocrystallography using an X-ray free-electron laser Aquila, Andrew; Hunter, Mark S.; Doak, R. Bruce Optics Express, Vol. 20, Issue 3 https://doi.org/10.1364/OE.20.002706	journal	January 2012
Initial observations of the femtosecond timing jitter at the European XFEL Kirkwood, Henry J.; Letrun, Romain; Tanikawa, Takanori Optics Letters, Vol. 44, Issue 7 https://doi.org/10.1364/OL.44.001650	journal	January 2019
Decipher the Mechanisms of Protein Conformational Changes Induced by Nucleotide Binding through Free-Energy Landscape Analysis: ATP Binding to Hsp70 Nicolaï, Adrien; Delarue, Patrice; Senet, Patrick PLoS Computational Biology, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pcbi.1003379	journal	December 2013
First Experiments in Structural Biology at the European X-ray Free-Electron Laser Mills, Grant; Bean, Richard; Mancuso, Adrian P. Applied Sciences, Vol. 10, Issue 10 https://doi.org/10.3390/app10103642	journal	May 2020
Bacterial Colonization and Proliferation in Furcal Perforations Repaired by Different Materials: A Confocal Laser Scanning Microscopy Study Elbahary, Shlomo; Haj Yahya, Sohad; Koç, Cemre Applied Sciences, Vol. 11, Issue 8 https://doi.org/10.3390/app11083403	journal	April 2021
Analysis of Multi-Hit Crystals in Serial Synchrotron Crystallography Experiments Using High-Viscosity Injectors Hadian-Jazi, Marjan; Berntsen, Peter; Marman, Hugh Crystals, Vol. 11, Issue 1 https://doi.org/10.3390/cryst11010049	journal	January 2021
The Influence of Photoelectron Escape in Radiation Damage Simulations of Protein Micro-Crystallography Marman, Hugh; Darmanin, Connie; Abbey, Brian Crystals, Vol. 8, Issue 7 https://doi.org/10.3390/cryst8070267	journal	June 2018
Time-Resolved Macromolecular Crystallography at Pulsed X-ray Sources Schmidt, Marius International Journal of Molecular Sciences, Vol. 20, Issue 6 https://doi.org/10.3390/ijms20061401	journal	March 2019
The XFEL Protein Crystallography: Developments and Perspectives Liu, Haiguang; Lee, Weontae International Journal of Molecular Sciences, Vol. 20, Issue 14 https://doi.org/10.3390/ijms20143421	journal	July 2019
The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser Claesson, Elin; Wahlgren, Weixiao Yuan; Takala, Heikki eLife, Vol. 9 https://doi.org/10.7554/eLife.53514	journal	March 2020

Similar Records

Membrane protein megahertz crystallography at the European XFEL

Journal Article · Mon Nov 04 00:00:00 UTC 2019 · Nature Communications · OSTI ID:1596363

Gisriel, Chris; Coe, Jesse; Letrun, Romain; +75 more

Megahertz serial crystallography

Journal Article · Tue Oct 02 00:00:00 UTC 2018 · Nature Communications · OSTI ID:1490639

Wiedorn, Max O.; Oberthür, Dominik; Bean, Richard; +123 more

Cascaded hard X-ray self-seeded free-electron laser at megahertz repetition rate

Journal Article · Mon Oct 16 00:00:00 UTC 2023 · Nature Photonics · OSTI ID:2294087

Liu, Shan; Grech, Christian; Guetg, Marc; +37 more

Related Subjects

38 RADIATION CHEMISTRY, RADIOCHEMISTRY, AND NUCLEAR CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES

Title: Megahertz pulse trains enable multi-hit serial femtosecond crystallography experiments at X-ray free electron lasers

Citation Formats

References (81)

Similar Records

Related Subjects