Radiation damage and dose limits in serial synchrotron crystallography at cryo- and room temperatures

de la Mora, Eugenio; Coquelle, Nicolas; Bury, Charles S.; Rosenthal, Martin; Holton, James M.; Carmichael, Ian; Garman, Elspeth F.; Burghammer, Manfred; Colletier, Jacques-Philippe; Weik, Martin

doi:10.1073/pnas.1821522117

Title: Radiation damage and dose limits in serial synchrotron crystallography at cryo- and room temperatures

Journal Article · Tue Feb 11 00:00:00 EST 2020 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1821522117· OSTI ID:1608636

^[1]; Coquelle, Nicolas ^[2]; Bury, Charles S. ^[3]; Rosenthal, Martin ^[4];

^[5]; Carmichael, Ian ^[6]; Garman, Elspeth F. ^[3]; Burghammer, Manfred ^[4]; Colletier, Jacques-Philippe ^[1];

^[1]

Commissariat a l'Energie Atomique et aux Energies Alternatives (CEA), Grenoble (France); Univ. of Grenoble (France); Centre National de la Recherche Scientifique (CNRS), Grenoble (France). Inst. de Biologie Structurale (IBS)
Commissariat a l'Energie Atomique et aux Energies Alternatives (CEA), Grenoble (France); Univ. of Grenoble (France); Centre National de la Recherche Scientifique (CNRS), Grenoble (France). Inst. de Biologie Structurale (IBS); Inst. Laue-Langevin (ILL), Grenoble (France)
Univ. of Oxford (United Kingdom)
European Synchrotron Radiation Facility (ESRF), Grenoble (France)
Univ. of California, San Francisco, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
Univ. of Notre Dame, IN (United States). Notre Dame Radiation Lab. (NDRL)

Radiation damage limits the accuracy of macromolecular structures in X-ray crystallography. Cryogenic (cryo-) cooling reduces the global radiation damage rate and, therefore, became the method of choice over the past decades. The recent advent of serial crystallography, which spreads the absorbed energy over many crystals, thereby reducing damage, has rendered room temperature (RT) data collection more practical and also extendable to microcrystals, both enabling and requiring the study of specific and global radiation damage at RT. Here, we performed sequential serial raster-scanning crystallography using a microfocused synchrotron beam that allowed for the collection of two series of 40 and 90 full datasets at 2- and 1.9-Å resolution at a dose rate of 40.3 MGy/s on hen egg white lysozyme (HEWL) crystals at RT and cryotemperature, respectively. The diffraction intensity halved its initial value at average doses (D_1/2) of 0.57 and 15.3 MGy at RT and 100 K, respectively. Specific radiation damage at RT was observed at disulfide bonds but not at acidic residues, increasing and then apparently reversing, a peculiar behavior that can be modeled by accounting for differential diffraction intensity decay due to the nonuniform illumination by the X-ray beam. Specific damage to disulfide bonds is evident early on at RT and proceeds at a fivefold higher rate than global damage. The decay modeling suggests it is advisable not to exceed a dose of 0.38 MGy per dataset in static and time-resolved synchrotron crystallography experiments at RT. This rough yardstick might change for proteins other than HEWL and at resolutions other than 2 Å.

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

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); National Science Foundation (NSF)

Grant/Contract Number:: AC02-76SF00515; FC02-04ER15533; AC02-05CH11231; ANR-15-CE18-0005-02; ANR-17-CE11-0018-01; FA-AAP-2013-65-101349; GM124149; GM124169; GM103393; GM082250; DBI‐1625906

OSTI ID:: 1608636

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 117, Issue 8; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 65 works

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References (77)

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
Lifetimes and spatio-temporal response of protein crystals in intense X-ray microbeams Warkentin, Matthew A.; Atakisi, Hakan; Hopkins, Jesse B. IUCrJ, Vol. 4, Issue 6 https://doi.org/10.1107/S2052252517013495	journal	October 2017
Conformational variation of proteins at room temperature is not dominated by radiation damage Russi, Silvia; González, Ana; Kenner, Lillian R. Journal of Synchrotron Radiation, Vol. 24, Issue 1 https://doi.org/10.1107/S1600577516017343	journal	January 2017
The hit-and-return system enables efficient time-resolved serial synchrotron crystallography Schulz, Eike C.; Mehrabi, Pedram; Müller-Werkmeister, Henrike M. Nature Methods, Vol. 15, Issue 11 https://doi.org/10.1038/s41592-018-0180-2	journal	October 2018
Mounting of crystals for macromolecular crystallography in a free-standing thin film Teng, T.-Y. Journal of Applied Crystallography, Vol. 23, Issue 5, p. 387-391 https://doi.org/10.1107/S0021889890005568	journal	October 1990
Serial crystallography on in vivo grown microcrystals using synchrotron radiation Gati, Cornelius; Bourenkov, Gleb; Klinge, Marco IUCrJ, Vol. 1, Issue 2 https://doi.org/10.1107/S2052252513033939	journal	February 2014
Room-temperature macromolecular serial crystallography using synchrotron radiation Stellato, Francesco; Oberthür, Dominik; Liang, Mengning IUCrJ, Vol. 1, Issue 4, p. 204-212 https://doi.org/10.1107/S2052252514010070	journal	May 2014
Proton uptake mechanism in bacteriorhodopsin captured by serial synchrotron crystallography Weinert, Tobias; Skopintsev, Petr; James, Daniel Science, Vol. 365, Issue 6448 https://doi.org/10.1126/science.aaw8634	journal	July 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
Exploiting fast detectors to enter a new dimension in room-temperature crystallography Owen, Robin L.; Paterson, Neil; Axford, Danny Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 5 https://doi.org/10.1107/S1399004714005379	journal	April 2014
Liquid application method for time-resolved analyses by serial synchrotron crystallography Mehrabi, Pedram; Schulz, Eike C.; Agthe, Michael Nature Methods, Vol. 16, Issue 10 https://doi.org/10.1038/s41592-019-0553-1	journal	September 2019
Effective scavenging at cryotemperatures: further increasing the dose tolerance of protein crystals De la Mora, Eugenio; Carmichael, Ian; Garman, Elspeth F. Journal of Synchrotron Radiation, Vol. 18, Issue 3 https://doi.org/10.1107/S0909049511007163	journal	April 2011
Towards an understanding of radiation damage in cryocooled macromolecular crystals Nave, Colin; Garman, Elspeth F. Journal of Synchrotron Radiation, Vol. 12, Issue 3 https://doi.org/10.1107/S0909049505007132	journal	April 2005
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
The oscillation method for crystals with very large unit cells Winkler, F. K.; Schutt, C. E.; Harrison, S. C. Acta Crystallographica Section A, Vol. 35, Issue 6 https://doi.org/10.1107/S0567739479002035	journal	November 1979
Evidence for β Scission in the Oxidation of Amino Acids Wisniowski, Pawel; Carmichael, Ian; Fessenden, Richard W. The Journal of Physical Chemistry A, Vol. 106, Issue 18 https://doi.org/10.1021/jp0139383	journal	May 2002
Radiation damage in protein crystals is reduced with a micron-sized X-ray beam Sanishvili, R.; Yoder, D. W.; Pothineni, S. B. Proceedings of the National Academy of Sciences, Vol. 108, Issue 15 https://doi.org/10.1073/pnas.1017701108	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
Mix-and-diffuse serial synchrotron crystallography Beyerlein, Kenneth R.; Dierksmeyer, Dennis; Mariani, Valerio IUCrJ, Vol. 4, Issue 6 https://doi.org/10.1107/S2052252517013124	journal	October 2017
Radiation Damage in Macromolecular Crystallography Garman, Elspeth F.; Weik, Martin Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-7000-1_20	book	January 2017
Primary radiation damage of protein crystals by an intense synchrotron X-ray beam Teng, Tsu-yi; Moffat, Keith Journal of Synchrotron Radiation, Vol. 7, Issue 5 https://doi.org/10.1107/S0909049500008694	journal	September 2000
Glass transition in thaumatin crystals revealed through temperature-dependent radiation-sensitivity measurements Warkentin, Matthew; Thorne, Robert E. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 10 https://doi.org/10.1107/S0907444910035523	journal	September 2010
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
Autoindexing diffraction images with iMosflm Powell, Harold R.; Johnson, Owen; Leslie, Andrew G. W. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444912048524	journal	June 2013
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Indexing in single-crystal diffractometry with an obstinate list of reflections Duisenberg, A. J. M. Journal of Applied Crystallography, Vol. 25, Issue 2 https://doi.org/10.1107/S0021889891010634	journal	April 1992
Specific chemical and structural damage to proteins produced by synchrotron radiation Weik, M.; Ravelli, R. B. G.; Kryger, G. Proceedings of the National Academy of Sciences, Vol. 97, Issue 2 https://doi.org/10.1073/pnas.97.2.623	journal	January 2000
Cryo-protection of protein crystals against radiation damage in electron and X-ray diffraction Henderson, Richard Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 241, Issue 1300, p. 6-8 https://doi.org/10.1098/rspb.1990.0057	journal	July 1990
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
Protein crystal perfection and the nature of radiation damage Helliwell, J. R. Journal of Crystal Growth, Vol. 90, Issue 1-3 https://doi.org/10.1016/0022-0248(88)90322-3	journal	July 1988
Photoreduction of the active site of the metalloprotein putidaredoxin by synchrotron radiation Corbett, Mary C.; Latimer, Matthew J.; Poulos, Thomas L. Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 9 https://doi.org/10.1107/S0907444907035160	journal	August 2007
Low-dose fixed-target serial synchrotron crystallography Owen, Robin L.; Axford, Danny; Sherrell, Darren A. Acta Crystallographica Section D Structural Biology, Vol. 73, Issue 4, p. 373-378 https://doi.org/10.1107/S2059798317002996	journal	March 2017
Observation of Decreased Radiation Damage at Higher Dose Rates in Room Temperature Protein Crystallography Southworth-Davies, Robert J.; Medina, Melissa A.; Carmichael, Ian Structure, Vol. 15, Issue 12 https://doi.org/10.1016/j.str.2007.10.013	journal	December 2007
Room-temperature serial crystallography at synchrotron X-ray sources using slowly flowing free-standing high-viscosity microstreams Botha, Sabine; Nass, Karol; Barends, Thomas R. M. Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 2 https://doi.org/10.1107/S1399004714026327	journal	January 2015
Radiation damage in protein crystallography Hendrickson, Wayne A. Journal of Molecular Biology, Vol. 106, Issue 3 https://doi.org/10.1016/0022-2836(76)90271-0	journal	September 1976
EIGER detector: application in macromolecular crystallography Casanas, Arnau; Warshamanage, Rangana; Finke, Aaron D. Acta Crystallographica Section D Structural Biology, Vol. 72, Issue 9 https://doi.org/10.1107/S2059798316012304	journal	August 2016
RADDOSE-3D : time- and space-resolved modelling of dose in macromolecular crystallography Zeldin, Oliver B.; Gerstel, Markus; Garman, Elspeth F. Journal of Applied Crystallography, Vol. 46, Issue 4 https://doi.org/10.1107/S0021889813011461	journal	June 2013
Structural Basis of X-ray-Induced Transient Photobleaching in a Photoactivatable Green Fluorescent Protein Adam, Virgile; Carpentier, Philippe; Violot, Sebastien Journal of the American Chemical Society, Vol. 131, Issue 50 https://doi.org/10.1021/ja907296v	journal	December 2009
Insights into the mechanism of X-ray-induced disulfide-bond cleavage in lysozyme crystals based on EPR, optical absorption and X-ray diffraction studies Sutton, Kristin A.; Black, Paul J.; Mercer, Kermit R. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 12 https://doi.org/10.1107/S0907444913022117	journal	November 2013
Acoustic methods for high-throughput protein crystal mounting at next-generation macromolecular crystallographic beamlines Roessler, Christian G.; Kuczewski, Anthony; Stearns, Richard Journal of Synchrotron Radiation, Vol. 20, Issue 5 https://doi.org/10.1107/S0909049513020372	journal	August 2013
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
The ‘fingerprint’ that X-rays can leave on structures Ravelli, Raimond BG; McSweeney, Sean M. Structure, Vol. 8, Issue 3 https://doi.org/10.1016/S0969-2126(00)00109-X	journal	March 2000
X-ray damage to the Mn4Ca complex in single crystals of photosystem II: A case study for metalloprotein crystallography Yano, J.; Kern, J.; Irrgang, K. -D. Proceedings of the National Academy of Sciences, Vol. 102, Issue 34 https://doi.org/10.1073/pnas.0505207102	journal	August 2005
Time-resolved crystallography reveals allosteric communication aligned with molecular breathing Mehrabi, Pedram; Schulz, Eike C.; Dsouza, Raison Science, Vol. 365, Issue 6458 https://doi.org/10.1126/science.aaw9904	journal	September 2019
Cryocooling and radiation damage in macromolecular crystallography Garman, Elspeth F.; Owen, Robin Leslie Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1 https://doi.org/10.1107/S0907444905034207	journal	December 2005
An assessment of the resolution limitation due to radiation-damage in X-ray diffraction microscopy Howells, M. R.; Beetz, T.; Chapman, H. N. Journal of Electron Spectroscopy and Related Phenomena, Vol. 170, Issue 1-3 https://doi.org/10.1016/j.elspec.2008.10.008	journal	March 2009
How does Radiation Damage in Protein Crystals Depend on X-Ray Dose? Sliz, Piotr; Harrison, Stephen C.; Rosenbaum, Gerd Structure, Vol. 11, Issue 1 https://doi.org/10.1016/S0969-2126(02)00910-3	journal	January 2003
Raster-scanning serial protein crystallography using micro- and nano-focused synchrotron beams Coquelle, Nicolas; Brewster, Aaron S.; Kapp, Ulrike Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 5 https://doi.org/10.1107/S1399004715004514	journal	April 2015
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
Room-temperature macromolecular crystallography using a micro-patterned silicon chip with minimal background scattering Roedig, Philip; Duman, Ramona; Sanchez-Weatherby, Juan Journal of Applied Crystallography, Vol. 49, Issue 3 https://doi.org/10.1107/S1600576716006348	journal	May 2016
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
Structural changes in a cryo-cooled protein crystal owing to radiation damage Burmeister, Wilhelm Pascal Acta Crystallographica Section D Biological Crystallography, Vol. 56, Issue 3 https://doi.org/10.1107/S0907444999016261	journal	March 2000
Resolution and dose dependence of radiation damage in biomolecular systems Atakisi, Hakan; Conger, Lauren; Moreau, David W. IUCrJ, Vol. 6, Issue 6 https://doi.org/10.1107/S2052252519008777	journal	September 2019
Version 1.2 of the Crystallography and NMR system Brunger, Axel T. Nature Protocols, Vol. 2, Issue 11 https://doi.org/10.1038/nprot.2007.406	journal	October 2007
Cryocrystallography of biological macromolecules: a generally applicable method Hope, H. Acta Crystallographica Section B Structural Science, Vol. 44, Issue 1 https://doi.org/10.1107/S0108768187008632	journal	February 1988
Translational diffusion of hydration water correlates with functional motions in folded and intrinsically disordered proteins Schirò, Giorgio; Fichou, Yann; Gallat, Francois-Xavier Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7490	journal	March 2015
Pink-beam serial crystallography Meents, A.; Wiedorn, M. O.; Srajer, V. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01417-3	journal	November 2017
Will reduced radiation damage occur with very small crystals? Nave, Colin; Hill, Mark A. Journal of Synchrotron Radiation, Vol. 12, Issue 3 https://doi.org/10.1107/S0909049505003274	journal	April 2005
A micro-patterned silicon chip as sample holder for macromolecular crystallography experiments with minimal background scattering Roedig, P.; Vartiainen, I.; Duman, R. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep10451	journal	May 2015
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
Crystallography on a chip – without the chip: sheet-on-sheet sandwich Doak, R. Bruce; Nass Kovacs, Gabriela; Gorel, Alexander Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 10 https://doi.org/10.1107/S2059798318011634	journal	October 2018
Generation of Size-Controlled, Submicrometer Protein Crystals Falkner, Joshua C.; Al-Somali, Ali M.; Jamison, Jennifer A. Chemistry of Materials, Vol. 17, Issue 10 https://doi.org/10.1021/cm047924w	journal	May 2005
A microfluidic flow-focusing device for low sample consumption serial synchrotron crystallography experiments in liquid flow Monteiro, Diana C. F.; Vakili, Mohammad; Harich, Jessica Journal of Synchrotron Radiation, Vol. 26, Issue 2 https://doi.org/10.1107/S1600577519000304	journal	February 2019
Accessing protein conformational ensembles using room-temperature X-ray crystallography Fraser, J. S.; van den Bedem, H.; Samelson, A. J. Proceedings of the National Academy of Sciences, Vol. 108, Issue 39 https://doi.org/10.1073/pnas.1111325108	journal	September 2011
Improved Estimation of Structure-Factor Difference Amplitudesfrom Poorly Accurate Data Ursby, T.; Bourgeois, D. Acta Crystallographica Section A Foundations of Crystallography, Vol. 53, Issue 5 https://doi.org/10.1107/S0108767397004522	journal	September 1997
A multicrystal diffraction data-collection approach for studying structural dynamics with millisecond temporal resolution Schubert, Robin; Kapis, Svetlana; Gicquel, Yannig IUCrJ, Vol. 3, Issue 6 https://doi.org/10.1107/S2052252516016304	journal	October 2016
Raman-Assisted Crystallography Suggests a Mechanism of X-Ray-Induced Disulfide Radical Formation and Reparation Carpentier, Philippe; Royant, Antoine; Weik, Martin Structure, Vol. 18, Issue 11 https://doi.org/10.1016/j.str.2010.09.010	journal	November 2010
Some simple, highly reactive, inorganic chlorine derivatives in aqueous solution. Their formation using pulses of radiation and their role in the mechanism of the Fricke dosimeter Jayson, G. G.; Parsons, B. J.; Swallow, A. J. Journal of the Chemical Society, Faraday Transactions 1: Physical Chemistry in Condensed Phases, Vol. 69, Issue 0 https://doi.org/10.1039/f19736901597	journal	January 1973
Resolution and dose dependence of radiation damage in biomolecular systems Atakisi, Hakan; Conger, Lauren; Moreau, David Acta Crystallographica Section A Foundations and Advances, Vol. 75, Issue a1 https://doi.org/10.1107/s0108767319096521	journal	July 2019
Sequential radiation damage in protein crystallography Sygusch, J.; Allaire, M. Acta Crystallographica Section A Foundations of Crystallography, Vol. 44, Issue 4 https://doi.org/10.1107/s0108767388001394	journal	July 1988
Use of a `caged' analogue to study the traffic of choline within acetylcholinesterase by kinetic crystallography Colletier, Jacques-Philippe; Royant, Antoine; Specht, Alexandre Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 11 https://doi.org/10.1107/s0907444907044472	journal	October 2007
Global radiation damage at 300 and 260 K with dose rates approaching 1 MGy s ⁻¹ Warkentin, Matthew; Badeau, Ryan; Hopkins, Jesse B. Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 2 https://doi.org/10.1107/s0907444911052085	journal	January 2012
XANES measurements of the rate of radiation damage to selenomethionine side chains Holton, James M. Journal of Synchrotron Radiation, Vol. 14, Issue 1 https://doi.org/10.1107/s0909049506048898	journal	December 2006
Temperature-dependent radiation sensitivity and order of 70S ribosome crystals Warkentin, Matthew; Hopkins, Jesse B.; Haber, Jonah B. Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 11 https://doi.org/10.1107/s1399004714017672	journal	October 2014
RIDL : a tool to investigate radiation-induced density loss Bury, Charles Simon; Garman, Elspeth Frances Journal of Applied Crystallography, Vol. 51, Issue 3 https://doi.org/10.1107/s1600576718005241	journal	May 2018
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
Room-Temperature Macromolecular Crystallography Using a Micro-Patterned Silicon Chip with Minimal Background Scattering Roedig, Philip; Duman, Ramona; Sanchez-Weatherby, Juan Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2016-02690	text	January 2016

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Title: Radiation damage and dose limits in serial synchrotron crystallography at cryo- and room temperatures

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