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

Abstract

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 (D1/2) 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 onmore » 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.« less

Authors:
ORCiD logo [1];  [2];  [3];  [4]; ORCiD logo [5];  [6];  [3];  [4];  [1]; ORCiD logo [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)
  2. 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)
  3. Univ. of Oxford (United Kingdom)
  4. European Synchrotron Radiation Facility (ESRF), Grenoble (France)
  5. 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)
  6. Univ. of Notre Dame, IN (United States). Notre Dame Radiation Lab. (NDRL)
Publication Date:
Research Org.:
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); National Science Foundation (NSF)
OSTI Identifier:
1608636
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
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 117; Journal Issue: 8; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
36 MATERIALS SCIENCE; X-ray radiation damage; serial crystallography; room temperature synchrotron data collection

Citation Formats

de la Mora, Eugenio, Coquelle, Nicolas, Bury, Charles S., Rosenthal, Martin, Holton, James M., Carmichael, Ian, Garman, Elspeth F., Burghammer, Manfred, Colletier, Jacques-Philippe, and Weik, Martin. Radiation damage and dose limits in serial synchrotron crystallography at cryo- and room temperatures. United States: N. p., 2020. Web. doi:10.1073/pnas.1821522117.
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. Radiation damage and dose limits in serial synchrotron crystallography at cryo- and room temperatures. United States. https://doi.org/10.1073/pnas.1821522117
de la Mora, Eugenio, Coquelle, Nicolas, Bury, Charles S., Rosenthal, Martin, Holton, James M., Carmichael, Ian, Garman, Elspeth F., Burghammer, Manfred, Colletier, Jacques-Philippe, and Weik, Martin. Tue . "Radiation damage and dose limits in serial synchrotron crystallography at cryo- and room temperatures". United States. https://doi.org/10.1073/pnas.1821522117. https://www.osti.gov/servlets/purl/1608636.
@article{osti_1608636,
title = {Radiation damage and dose limits in serial synchrotron crystallography at cryo- and room temperatures},
author = {de la Mora, Eugenio and Coquelle, Nicolas and Bury, Charles S. and Rosenthal, Martin and Holton, James M. and Carmichael, Ian and Garman, Elspeth F. and Burghammer, Manfred and Colletier, Jacques-Philippe and Weik, Martin},
abstractNote = {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 (D1/2) 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.},
doi = {10.1073/pnas.1821522117},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 8,
volume = 117,
place = {United States},
year = {Tue Feb 11 00:00:00 EST 2020},
month = {Tue Feb 11 00:00:00 EST 2020}
}

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