Towards the spatial resolution of metalloprotein charge states by detailed modeling of XFEL crystallographic diffraction

Sauter, Nicholas K.; Kern, Jan; Yano, Junko; Holton, James M.

doi:10.1107/S2059798320000418

Title: Towards the spatial resolution of metalloprotein charge states by detailed modeling of XFEL crystallographic diffraction

Journal Article · Tue Feb 04 00:00:00 EST 2020 · Acta Crystallographica. Section D. Structural Biology

DOI:https://doi.org/10.1107/S2059798320000418· OSTI ID:1617958

Sauter, Nicholas K.;

;

; Holton, James M.

Oxidation states of individual metal atoms within a metalloprotein can be assigned by examining X-ray absorption edges, which shift to higher energy for progressively more positive valence numbers. Indeed, X-ray crystallography is well suited for such a measurement, owing to its ability to spatially resolve the scattering contributions of individual metal atoms that have distinct electronic environments contributing to protein function. However, as the magnitude of the shift is quite small, about +2 eV per valence state for iron, it has only been possible to measure the effect when performed with monochromated X-ray sources at synchrotron facilities with energy resolutions in the range 2–3 × 10^-4 (ΔE/E). This paper tests whether X-ray free-electron laser (XFEL) pulses, which have a broader bandpass (ΔE/E = 3 × 10^-3) when used without a monochromator, might also be useful for such studies. The program nanoBragg is used to simulate serial femtosecond crystallography (SFX) diffraction images with sufficient granularity to model the XFEL spectrum, the crystal mosaicity and the wavelength-dependent anomalous scattering factors contributed by two differently charged iron centers in the 110-amino-acid protein, ferredoxin. Bayesian methods are then used to deduce, from the simulated data, the most likely X-ray absorption curves for each metal atom in the protein, which agree well with the curves chosen for the simulation. The data analysis relies critically on the ability to measure the incident spectrum for each pulse, and also on the nanoBragg simulator to predict the size, shape and intensity profile of Bragg spots based on an underlying physical model that includes the absorption curves, which are then modified to produce the best agreement with the simulated data. This inference methodology potentially enables the use of SFX diffraction for the study of metalloenzyme mechanisms and, in general, offers a more detailed approach to Bragg spot data reduction.

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Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); National Institute of General Medical Sciences

Grant/Contract Number:: AC02-05CH11231; AC02-76SF00515; GM117126; GM124149; GM124169; GM126289; GM103393; GM082250; GM110501; DBI 1625906; 17-SC-20-SC

OSTI ID:: 1617958

Alternate ID(s):: OSTI ID: 1615300; OSTI ID: 1638258

Journal Information:: Acta Crystallographica. Section D. Structural Biology, Journal Name: Acta Crystallographica. Section D. Structural Biology Vol. 76 Journal Issue: 2; ISSN 2059-7983

Publisher:: IUCrCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Cited by: 7 works

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References (76)

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
The R-factor gap in macromolecular crystallography: an untapped potential for insights on accurate structures Holton, James M.; Classen, Scott; Frankel, Kenneth A. The FEBS Journal, Vol. 281, Issue 18 https://doi.org/10.1111/febs.12922	journal	September 2014
On the limited memory BFGS method for large scale optimization Liu, Dong C.; Nocedal, Jorge Mathematical Programming, Vol. 45, Issue 1-3 https://doi.org/10.1007/BF01589116	journal	August 1989
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
Crystallographic structure analysis of lamprey hemoglobin from anomalous dispersion of synchrotron radiation Hendrickson, Wayne A.; Smith, Janet L.; Phizackerley, R. Paul Proteins: Structure, Function, and Genetics, Vol. 4, Issue 2 https://doi.org/10.1002/prot.340040202	journal	January 1988
A nanosecond time-resolved XFEL analysis of structural changes associated with CO release from cytochrome c oxidase Shimada, Atsuhiro; Kubo, Minoru; Baba, Seiki Science Advances, Vol. 3, Issue 7 https://doi.org/10.1126/sciadv.1603042	journal	July 2017
Application of an ePix100 detector for coherent scattering using a hard X-ray free-electron laser Sikorski, Marcin; Feng, Yiping; Song, Sanghoon Journal of Synchrotron Radiation, Vol. 23, Issue 5 https://doi.org/10.1107/S1600577516010869	journal	August 2016
DIALS : implementation and evaluation of a new integration package Winter, Graeme; Waterman, David G.; Parkhurst, James M. Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 2 https://doi.org/10.1107/S2059798317017235	journal	February 2018
Bulk-solvent and overall scaling revisited: faster calculations, improved results Afonine, P. V.; Grosse-Kunstleve, R. W.; Adams, P. D. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 4 https://doi.org/10.1107/S0907444913000462	journal	March 2013
E pluribus unum, no more: from one crystal, many conformations Woldeyes, Rahel A.; Sivak, David A.; Fraser, James S. Current Opinion in Structural Biology, Vol. 28 https://doi.org/10.1016/j.sbi.2014.07.005	journal	October 2014
The Use of Partial Reflections for Scaling and Averaging X-ray Area-Detector Data Bolotovsky, Robert; Steller, Ingo; Rossmann, Michael G. Journal of Applied Crystallography, Vol. 31, Issue 5 https://doi.org/10.1107/S0021889898004361	journal	October 1998
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
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
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444912001308	journal	March 2012
High resolution 1s core hole X-ray spectroscopy in 3d transition metal complexes—electronic and structural information Glatzel, Pieter; Bergmann, Uwe Coordination Chemistry Reviews, Vol. 249, Issue 1-2 https://doi.org/10.1016/j.ccr.2004.04.011	journal	January 2005
A single-shot transmissive spectrometer for hard x-ray free electron lasers Zhu, Diling; Cammarata, Marco; Feldkamp, Jan M. Applied Physics Letters, Vol. 101, Issue 3 https://doi.org/10.1063/1.4736725	journal	July 2012
A Description of Imperfections in Protein Crystals Nave, C. Acta Crystallographica Section D Biological Crystallography, Vol. 54, Issue 5 https://doi.org/10.1107/S0907444998001875	journal	September 1998
Improved statistics for determining the Patterson symmetry from unmerged diffraction intensities Sauter, Nicholas K.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 39, Issue 2 https://doi.org/10.1107/S0021889805042299	journal	March 2006
Crystal Cryocooling Distorts Conformational Heterogeneity in a Model Michaelis Complex of DHFR Keedy, Daniel A.; van den Bedem, Henry; Sivak, David A. Structure, Vol. 22, Issue 6 https://doi.org/10.1016/j.str.2014.04.016	journal	June 2014
Exploiting the anisotropy of anomalous scattering boosts the phasing power of SAD and MAD experiments Schiltz, Marc; Bricogne, Gérard Acta Crystallographica Section D Biological Crystallography, Vol. 64, Issue 7 https://doi.org/10.1107/S0907444908010202	journal	June 2008
Improved crystal orientation and physical properties from single-shot XFEL stills Sauter, Nicholas K.; Hattne, Johan; Brewster, Aaron S. Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 12 https://doi.org/10.1107/S1399004714024134	journal	November 2014
Unterschiede in der Intensit�t der R�ntgenstrahlen-reflexion an den beiden 111-Fl�chen der Zinkblende Coster, D.; Knol, K. S.; Prins, J. A. Zeitschrift f�r Physik, Vol. 63, Issue 5-6 https://doi.org/10.1007/BF01339610	journal	May 1930
Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers Fuller, Franklin D.; Gul, Sheraz; Chatterjee, Ruchira Nature Methods, Vol. 14, Issue 4 https://doi.org/10.1038/nmeth.4195	journal	February 2017
Simultaneous Femtosecond X-ray Spectroscopy and Diffraction of Photosystem II at Room Temperature Kern, J.; Alonso-Mori, R.; Tran, R. Science, Vol. 340, Issue 6131 https://doi.org/10.1126/science.1234273	journal	February 2013
Towards characterization of photo-excited electron transfer and catalysis in natural and artificial systems using XFELs Alonso-Mori, R.; Asa, K.; Bergmann, U. Faraday Discussions, Vol. 194 https://doi.org/10.1039/C6FD00084C	journal	January 2016
Assignment of Individual Metal Redox States in a Metalloprotein by Crystallographic Refinement at Multiple X-ray Wavelengths Einsle, Oliver; Andrade, Susana L. A.; Dobbek, Holger Journal of the American Chemical Society, Vol. 129, Issue 8 https://doi.org/10.1021/ja067562o	journal	February 2007
A revised partiality model and post-refinement algorithm for X-ray free-electron laser data Ginn, Helen Mary; Brewster, Aaron S.; Hattne, Johan Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 6 https://doi.org/10.1107/S1399004715006902	journal	May 2015
Integration, scaling, space-group assignment and post-refinement Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 133-144 https://doi.org/10.1107/S0907444909047374	journal	January 2010
Towards in cellulo virus crystallography Duyvesteyn, Helen M. E.; Ginn, Helen M.; Pietilä, Maija K. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-21693-3	journal	February 2018
Metalloprotein structures at ambient conditions and in real-time: biological crystallography and spectroscopy using X-ray free electron lasers Kern, Jan; Yachandra, Vittal K.; Yano, Junko Current Opinion in Structural Biology, Vol. 34 https://doi.org/10.1016/j.sbi.2015.07.014	journal	October 2015
Liking likelihood McCoy, Airlie J. Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12 https://doi.org/10.1107/S0907444904016038	journal	November 2004
XFEL structures of the influenza M2 proton channel: Room temperature water networks and insights into proton conduction Thomaston, Jessica L.; Woldeyes, Rahel A.; Nakane, Takanori Proceedings of the National Academy of Sciences, Vol. 114, Issue 51 https://doi.org/10.1073/pnas.1705624114	journal	August 2017
High Resolution Crystal Structures of the Wild Type and Cys-55 → Ser and Cys-59 → Ser Variants of the Thioredoxin-like [2Fe-2S] Ferredoxin from Aquifex aeolicus Yeh, Andrew P.; Ambroggio, Xavier I.; Andrade, Susana L. A. Journal of Biological Chemistry, Vol. 277, Issue 37 https://doi.org/10.1074/jbc.M205096200	journal	June 2002
Accounting for partiality in serial crystallography using ray-tracing principles Kroon-Batenburg, Loes M. J.; Schreurs, Antoine M. M.; Ravelli, Raimond B. G. Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 9 https://doi.org/10.1107/S1399004715011803	journal	August 2015
Energy-dispersive X-ray emission spectroscopy using an X-ray free-electron laser in a shot-by-shot mode Alonso-Mori, R.; Kern, J.; Gildea, R. J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 47, p. 19103-19107 https://doi.org/10.1073/pnas.1211384109	journal	November 2012
Macromolecular crystallography with synchrotron radiation: photographic data collection and polarization correction Kahn, R.; Fourme, R.; Gadet, A. Journal of Applied Crystallography, Vol. 15, Issue 3 https://doi.org/10.1107/S0021889882012060	journal	June 1982
Post-refinement method for snapshot serial crystallography White, Thomas A. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647 https://doi.org/10.1098/rstb.2013.0330	journal	July 2014
Cryoradiolytic reduction of heme proteins: Maximizing dose-dependent yield Denisov, Ilia G.; Victoria, Doreen C.; Sligar, Stephen G. Radiation Physics and Chemistry, Vol. 76, Issue 4 https://doi.org/10.1016/j.radphyschem.2006.03.002	journal	April 2007
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
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
Self-terminating diffraction gates femtosecond X-ray nanocrystallography measurements Barty, Anton; Caleman, Carl; Aquila, Andrew Nature Photonics, Vol. 6, Issue 1 https://doi.org/10.1038/nphoton.2011.297	journal	December 2011
Structure of photosystem II and substrate binding at room temperature Young, Iris D.; Ibrahim, Mohamed; Chatterjee, Ruchira Nature, Vol. 540, Issue 7633 https://doi.org/10.1038/nature20161	journal	November 2016
Pixel array detector for X-ray free electron laser experiments Philipp, Hugh T.; Hromalik, Marianne; Tate, Mark Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment, Vol. 649, Issue 1 https://doi.org/10.1016/j.nima.2010.11.189	journal	September 2011
Mapping the conformational landscape of a dynamic enzyme by multitemperature and XFEL crystallography Keedy, Daniel A.; Kenner, Lillian R.; Warkentin, Matthew eLife, Vol. 4 https://doi.org/10.7554/eLife.07574	journal	September 2015
Protein Hydration Observed by X-ray Diffraction Jiang, Jian-Sheng; Brünger, Axel T. Journal of Molecular Biology, Vol. 243, Issue 1 https://doi.org/10.1006/jmbi.1994.1633	journal	October 1994
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
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
Optimized anomalous dispersion in crystallography: a synchrotron X-ray polychromatic simultaneous profile method Arndt, U. W.; Greenhough, T. J.; Helliwell, J. R. Nature, Vol. 298, Issue 5877 https://doi.org/10.1038/298835a0	journal	August 1982
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
Demonstration of self-seeding in a hard-X-ray free-electron laser Amann, J.; Berg, W.; Blank, V. Nature Photonics, Vol. 6, Issue 10, p. 693-698 https://doi.org/10.1038/nphoton.2012.180	journal	August 2012
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
Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL Suga, Michihiro; Akita, Fusamichi; Sugahara, Michihiro Nature, Vol. 543, Issue 7643 https://doi.org/10.1038/nature21400	journal	February 2017
XXIX. The atomic structure factor in the intensity of reflexion of X-rays by crystals Hartree, D. R. The London, Edinburgh, and Dublin Philosophical Magazine and Journal of Science, Vol. 50, Issue 295 https://doi.org/10.1080/14786442508634740	journal	July 1925
dxtbx : the diffraction experiment toolbox Parkhurst, James M.; Brewster, Aaron S.; Fuentes-Montero, Luis Journal of Applied Crystallography, Vol. 47, Issue 4 https://doi.org/10.1107/S1600576714011996	journal	July 2014
`Broken symmetries' in macromolecular crystallography: phasing from unmerged data Schiltz, Marc; Bricogne, Gérard Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444909053578	journal	March 2010
Improving signal strength in serial crystallography with DIALS geometry refinement Brewster, Aaron S.; Waterman, David G.; Parkhurst, James M. Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 9 https://doi.org/10.1107/S2059798318009191	journal	September 2018
Low-dose X-ray radiation induces structural alterations in proteins Borshchevskiy, Valentin; Round, Ekaterina; Erofeev, Ivan Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 10 https://doi.org/10.1107/S1399004714017295	journal	September 2014
Efficient structure-factor calculation for large molecules by the fast Fourier transform Ten Eyck, L. F. Acta Crystallographica Section A, Vol. 33, Issue 3 https://doi.org/10.1107/S0567739477001211	journal	May 1977
Indications of radiation damage in ferredoxin microcrystals using high-intensity X-FEL beams Nass, Karol; Foucar, Lutz; Barends, Thomas R. M. Journal of Synchrotron Radiation, Vol. 22, Issue 2 https://doi.org/10.1107/S1600577515002349	journal	February 2015
XFEL diffraction: developing processing methods to optimize data quality Sauter, Nicholas K. Journal of Synchrotron Radiation, Vol. 22, Issue 2 https://doi.org/10.1107/S1600577514028203	journal	January 2015
AGIPD, a high dynamic range fast detector for the European XFEL Allahgholi, A.; Becker, J.; Bianco, L. Journal of Instrumentation, Vol. 10, Issue 01 https://doi.org/10.1088/1748-0221/10/01/C01023	journal	January 2015
The Computational Crystallography Toolbox : crystallographic algorithms in a reusable software framework Grosse-Kunstleve, Ralf W.; Sauter, Nicholas K.; Moriarty, Nigel W. Journal of Applied Crystallography, Vol. 35, Issue 1 https://doi.org/10.1107/S0021889801017824	journal	January 2002
Bringing diffuse X-ray scattering into focus Wall, Michael E.; Wolff, Alexander M.; Fraser, James S. Current Opinion in Structural Biology, Vol. 50 https://doi.org/10.1016/j.sbi.2018.01.009	journal	June 2018
X-ray Emission Spectroscopy as an in Situ Diagnostic Tool for X-ray Crystallography of Metalloproteins Using an X-ray Free-Electron Laser Fransson, Thomas; Chatterjee, Ruchira; Fuller, Franklin D. Biochemistry, Vol. 57, Issue 31 https://doi.org/10.1021/acs.biochem.8b00325	journal	April 2018
Integration of macromolecular diffraction data Leslie, A. G. W. Acta Crystallographica Section D Biological Crystallography, Vol. 55, Issue 10 https://doi.org/10.1107/S090744499900846X	journal	October 1999
Imaging protein three-dimensional nanocrystals with cryo-EM Nederlof, Igor; Li, Yao Wang; van Heel, Marin Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 5 https://doi.org/10.1107/S0907444913002734	journal	April 2013
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
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
The Sixteenth Iron in the Nitrogenase MoFe Protein Zhang, Limei; Kaiser, Jens T.; Meloni, Gabriele Angewandte Chemie International Edition, Vol. 52, Issue 40 https://doi.org/10.1002/anie.201303877	journal	August 2013
Angle calculations for 3- and 4-circle X-ray and neutron diffractometers Busing, W. R.; Levy, H. A. Acta Crystallographica, Vol. 22, Issue 4 https://doi.org/10.1107/S0365110X67000970	journal	April 1967
Challenge data set for macromolecular multi-microcrystallography Holton, James M. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2 https://doi.org/10.1107/S2059798319001426	journal	February 2019
Structures of the intermediates of Kok’s photosynthetic water oxidation clock Kern, Jan; Chatterjee, Ruchira; Young, Iris D. Nature, Vol. 563, Issue 7731 https://doi.org/10.1038/s41586-018-0681-2	journal	November 2018
Fast and accurate data collection for macromolecular crystallography using the JUNGFRAU detector Leonarski, Filip; Redford, Sophie; Mozzanica, Aldo Nature Methods, Vol. 15, Issue 10 https://doi.org/10.1038/s41592-018-0143-7	journal	October 2018
Direct observation of ultrafast collective motions in CO myoglobin upon ligand dissociation Barends, T. R. M.; Foucar, L.; Ardevol, A. Science, Vol. 350, Issue 6259 https://doi.org/10.1126/science.aac5492	journal	September 2015
The New Macromolecular Femtosecond Crystallography (MFX) Instrument at LCLS Boutet, Sébastien; Cohen, Aina E.; Wakatsuki, Soichi Synchrotron Radiation News, Vol. 29, Issue 1 https://doi.org/10.1080/08940886.2016.1124681	journal	January 2016
Nitrogenase FeMoco investigated by spatially resolved anomalous dispersion refinement Spatzal, Thomas; Schlesier, Julia; Burger, Eva-Maria Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10902	journal	March 2016