X-ray Emission Spectroscopy as an in Situ Diagnostic Tool for X-ray Crystallography of Metalloproteins Using an X-ray Free-Electron Laser
Abstract
Serial femtosecond crystallography (SFX) using the ultrashort X-ray pulses from a X-ray free-electron laser (XFEL) provides a new way of collecting structural data at room temperature that allows for following the reaction in real time after initiation. XFEL experiments are conducted in a shot-by-shot mode as the sample is destroyed and replenished after each X-ray pulse, and therefore, monitoring and controlling the data quality by using in situ diagnostic tools is critical. To study metalloenzymes, we developed the use of simultaneous collection of X-ray diffraction of crystals along with X-ray emission spectroscopy (XES) data that is used as a diagnostic tool for crystallography, by monitoring the chemical state of the metal catalytic center. We have optimized data analysis methods and sample delivery techniques for fast and active feedback to ensure the quality of each batch of samples and the turnover of the catalytic reaction caused by reaction triggering methods. Here, we describe this active in situ feedback system using Photosystem II as an example that catalyzes the oxidation of H2O to O2at the Mn4CaO5active site. We used the first moments of the Mn Kβ1,3emission spectra, which are sensitive to the oxidation state of Mn, as the primary diagnostics. This approachmore »
- Authors:
-
- SLAC National Accelerator Lab., Menlo Park, CA (United States). Photon Ultrafast Laser Science and Engineering Inst. (PULSE)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- SLAC National Accelerator Lab., Menlo Park, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- Office of Science (SC), Biological and Environmental Research (BER). Earth and Environmental Systems Science Division
- OSTI Identifier:
- 1465465
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Biochemistry
- Additional Journal Information:
- Journal Volume: 57; Journal Issue: 31; Journal ID: ISSN 0006-2960
- Publisher:
- American Chemical Society (ACS)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 47 OTHER INSTRUMENTATION
Citation Formats
Fransson, Thomas, Chatterjee, Ruchira, Fuller, Franklin D., Gul, Sheraz, Weninger, Clemens, Sokaras, Dimosthenis, Kroll, Thomas, Alonso-Mori, Roberto, Bergmann, Uwe, Kern, Jan, Yachandra, Vittal K., and Yano, Junko. X-ray Emission Spectroscopy as an in Situ Diagnostic Tool for X-ray Crystallography of Metalloproteins Using an X-ray Free-Electron Laser. United States: N. p., 2018.
Web. doi:10.1021/acs.biochem.8b00325.
Fransson, Thomas, Chatterjee, Ruchira, Fuller, Franklin D., Gul, Sheraz, Weninger, Clemens, Sokaras, Dimosthenis, Kroll, Thomas, Alonso-Mori, Roberto, Bergmann, Uwe, Kern, Jan, Yachandra, Vittal K., & Yano, Junko. X-ray Emission Spectroscopy as an in Situ Diagnostic Tool for X-ray Crystallography of Metalloproteins Using an X-ray Free-Electron Laser. United States. https://doi.org/10.1021/acs.biochem.8b00325
Fransson, Thomas, Chatterjee, Ruchira, Fuller, Franklin D., Gul, Sheraz, Weninger, Clemens, Sokaras, Dimosthenis, Kroll, Thomas, Alonso-Mori, Roberto, Bergmann, Uwe, Kern, Jan, Yachandra, Vittal K., and Yano, Junko. Thu .
"X-ray Emission Spectroscopy as an in Situ Diagnostic Tool for X-ray Crystallography of Metalloproteins Using an X-ray Free-Electron Laser". United States. https://doi.org/10.1021/acs.biochem.8b00325. https://www.osti.gov/servlets/purl/1465465.
@article{osti_1465465,
title = {X-ray Emission Spectroscopy as an in Situ Diagnostic Tool for X-ray Crystallography of Metalloproteins Using an X-ray Free-Electron Laser},
author = {Fransson, Thomas and Chatterjee, Ruchira and Fuller, Franklin D. and Gul, Sheraz and Weninger, Clemens and Sokaras, Dimosthenis and Kroll, Thomas and Alonso-Mori, Roberto and Bergmann, Uwe and Kern, Jan and Yachandra, Vittal K. and Yano, Junko},
abstractNote = {Serial femtosecond crystallography (SFX) using the ultrashort X-ray pulses from a X-ray free-electron laser (XFEL) provides a new way of collecting structural data at room temperature that allows for following the reaction in real time after initiation. XFEL experiments are conducted in a shot-by-shot mode as the sample is destroyed and replenished after each X-ray pulse, and therefore, monitoring and controlling the data quality by using in situ diagnostic tools is critical. To study metalloenzymes, we developed the use of simultaneous collection of X-ray diffraction of crystals along with X-ray emission spectroscopy (XES) data that is used as a diagnostic tool for crystallography, by monitoring the chemical state of the metal catalytic center. We have optimized data analysis methods and sample delivery techniques for fast and active feedback to ensure the quality of each batch of samples and the turnover of the catalytic reaction caused by reaction triggering methods. Here, we describe this active in situ feedback system using Photosystem II as an example that catalyzes the oxidation of H2O to O2at the Mn4CaO5active site. We used the first moments of the Mn Kβ1,3emission spectra, which are sensitive to the oxidation state of Mn, as the primary diagnostics. This approach is applicable to different metalloproteins to determine the integrity of samples and follow changes in the chemical states of the reaction that can be initiated by light or activated by substrates and offers a metric for determining the diffraction images that are used for the final data sets.},
doi = {10.1021/acs.biochem.8b00325},
journal = {Biochemistry},
number = 31,
volume = 57,
place = {United States},
year = {Thu Apr 05 00:00:00 EDT 2018},
month = {Thu Apr 05 00:00:00 EDT 2018}
}
Web of Science
Works referenced in this record:
Femtosecond X-ray protein nanocrystallography
journal, February 2011
- Chapman, Henry N.; Fromme, Petra; Barty, Anton
- Nature, Vol. 470, Issue 7332, p. 73-77
Room temperature femtosecond X-ray diffraction of photosystem II microcrystals
journal, June 2012
- Kern, J.; Alonso-Mori, R.; Hellmich, J.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 25, p. 9721-9726
High-Resolution Protein Structure Determination by Serial Femtosecond Crystallography
journal, May 2012
- Boutet, S.; Lomb, L.; Williams, G. J.
- Science, Vol. 337, Issue 6092
Serial Femtosecond Crystallography of G Protein-Coupled Receptors
journal, December 2013
- Liu, W.; Wacker, D.; Gati, C.
- Science, Vol. 342, Issue 6165
Natively Inhibited Trypanosoma brucei Cathepsin B Structure Determined by Using an X-ray Laser
journal, November 2012
- Redecke, L.; Nass, K.; DePonte, D. P.
- Science, Vol. 339, Issue 6116
De novo protein crystal structure determination from X-ray free-electron laser data
journal, November 2013
- Barends, Thomas R. M.; Foucar, Lutz; Botha, Sabine
- Nature, Vol. 505, Issue 7482
Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein
journal, December 2014
- Tenboer, Jason; Basu, Shibom; Zatsepin, Nadia
- Science, Vol. 346, Issue 6214
A Bright Future for Serial Femtosecond Crystallography with XFELs
journal, September 2017
- Johansson, Linda C.; Stauch, Benjamin; Ishchenko, Andrii
- Trends in Biochemical Sciences, Vol. 42, Issue 9
Energy-dispersive X-ray emission spectroscopy using an X-ray free-electron laser in a shot-by-shot mode
journal, November 2012
- Alonso-Mori, R.; Kern, J.; Gildea, R. J.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 47, p. 19103-19107
Simultaneous Femtosecond X-ray Spectroscopy and Diffraction of Photosystem II at Room Temperature
journal, February 2013
- Kern, J.; Alonso-Mori, R.; Tran, R.
- Science, Vol. 340, Issue 6131
Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy
journal, July 2014
- Kern, Jan; Tran, Rosalie; Alonso-Mori, Roberto
- Nature Communications, Vol. 5, Issue 1
Towards characterization of photo-excited electron transfer and catalysis in natural and artificial systems using XFELs
journal, January 2016
- Alonso-Mori, R.; Asa, K.; Bergmann, U.
- Faraday Discussions, Vol. 194
Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers
journal, February 2017
- Fuller, Franklin D.; Gul, Sheraz; Chatterjee, Ruchira
- Nature Methods, Vol. 14, Issue 4
X-ray emission spectroscopy
journal, August 2009
- Bergmann, Uwe; Glatzel, Pieter
- Photosynthesis Research, Vol. 102, Issue 2-3
High resolution 1s core hole X-ray spectroscopy in 3d transition metal complexes—electronic and structural information
journal, January 2005
- Glatzel, Pieter; Bergmann, Uwe
- Coordination Chemistry Reviews, Vol. 249, Issue 1-2
A Practical Guide to High-resolution X-ray Spectroscopic Measurements and their Applications in Bioinorganic Chemistry
journal, July 2016
- Kowalska, Joanna K.; Lima, Frederico A.; Pollock, Christopher J.
- Israel Journal of Chemistry, Vol. 56, Issue 9-10
Photon-in photon-out hard X-ray spectroscopy at the Linac Coherent Light Source
journal, April 2015
- Alonso-Mori, Roberto; Sokaras, Dimosthenis; Zhu, Diling
- Journal of Synchrotron Radiation, Vol. 22, Issue 3
Femtosecond electronic response of atoms to ultra-intense X-rays
journal, July 2010
- Young, L.; Kanter, E. P.; Krässig, B.
- Nature, Vol. 466, Issue 7302
X-ray two-photon absorption competing against single and sequential multiphoton processes
journal, February 2014
- Tamasaku, Kenji; Shigemasa, Eiji; Inubushi, Yuichi
- Nature Photonics, Vol. 8, Issue 4
Nanoflow electrospinning serial femtosecond crystallography
journal, October 2012
- Sierra, Raymond G.; Laksmono, Hartawan; Kern, Jan
- Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 11, p. 1584-1587
Concentric-flow electrokinetic injector enables serial crystallography of ribosome and photosystem II
journal, November 2015
- Sierra, Raymond G.; Gati, Cornelius; Laksmono, Hartawan
- Nature Methods, Vol. 13, Issue 1
Mn 4 Ca Cluster in Photosynthesis: Where and How Water is Oxidized to Dioxygen
journal, March 2014
- Yano, Junko; Yachandra, Vittal
- Chemical Reviews, Vol. 114, Issue 8
Reflections on substrate water and dioxygen formation
journal, August 2013
- Cox, Nicholas; Messinger, Johannes
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 8-9
The New Macromolecular Femtosecond Crystallography (MFX) Instrument at LCLS
journal, January 2016
- Boutet, Sébastien; Cohen, Aina E.; Wakatsuki, Soichi
- Synchrotron Radiation News, Vol. 29, Issue 1
First lasing and operation of an ångstrom-wavelength free-electron laser
journal, August 2010
- Emma, P.; Akre, R.; Arthur, J.
- Nature Photonics, Vol. 4, Issue 9
Structure of photosystem II and substrate binding at room temperature
journal, November 2016
- Young, Iris D.; Ibrahim, Mohamed; Chatterjee, Ruchira
- Nature, Vol. 540, Issue 7633
A multi-crystal wavelength dispersive x-ray spectrometer
journal, July 2012
- Alonso-Mori, Roberto; Kern, Jan; Sokaras, Dimosthenis
- Review of Scientific Instruments, Vol. 83, Issue 7
X-ray detectors at the Linac Coherent Light Source
journal, April 2015
- Blaj, Gabriel; Caragiulo, Pietro; Carini, Gabriella
- Journal of Synchrotron Radiation, Vol. 22, Issue 3
Analysis of full charge reconstruction algorithms for X-ray pixelated detectors
conference, October 2011
- Baumbaugh, A.; Carini, G.; Deptuch, G.
- 2011 IEEE Nuclear Science Symposium and Medical Imaging Conference (2011 NSS/MIC), 2011 IEEE Nuclear Science Symposium Conference Record
Absence of Mn-Centered Oxidation in the S2 → S3 Transition: Implications for the Mechanism of Photosynthetic Water Oxidation
journal, July 2001
- Messinger, Johannes; Robblee, John H.; Bergmann, Uwe
- Journal of the American Chemical Society, Vol. 123, Issue 32
X-ray Emission Spectroscopy of Biomimetic Mn Coordination Complexes
journal, May 2017
- Jensen, Scott C.; Davis, Katherine M.; Sullivan, Brendan
- The Journal of Physical Chemistry Letters, Vol. 8, Issue 12
X-ray Emission Spectroscopy of Mn Coordination Complexes Toward Interpreting the Electronic Structure of the Oxygen-Evolving Complex of Photosystem II
journal, February 2016
- Davis, Katherine M.; Palenik, Mark C.; Yan, Lifen
- The Journal of Physical Chemistry C, Vol. 120, Issue 6
Mn oxidation states in tri- and tetra-nuclear Mn compounds structurally relevant to photosystem II: Mn K-edge X-ray absorption and K? X-ray emission spectroscopy studies
journal, January 2004
- PizarroCurrent address: Sandia Nati, Shelly A.; Glatzel, Pieter; VisserCurrent address: California I., Hendrik
- Physical Chemistry Chemical Physics, Vol. 6, Issue 20
Mn K-Edge XANES and Kβ XES Studies of Two Mn−Oxo Binuclear Complexes: Investigation of Three Different Oxidation States Relevant to the Oxygen-Evolving Complex of Photosystem II
journal, July 2001
- Visser, Hendrik; Anxolabéhère-Mallart, Elodie; Bergmann, Uwe
- Journal of the American Chemical Society, Vol. 123, Issue 29
Sequential and Coupled Proton and Electron Transfer Events in the S 2 → S 3 Transition of Photosynthetic Water Oxidation Revealed by Time-Resolved X-ray Absorption Spectroscopy
journal, December 2016
- Zaharieva, Ivelina; Dau, Holger; Haumann, Michael
- Biochemistry, Vol. 55, Issue 50
COOPERATION OF CHARGES IN PHOTOSYNTHETIC O 2 EVOLUTION–I. A LINEAR FOUR STEP MECHANISM
journal, June 1970
- Kok, Bessel; Forbush, Bliss; McGLOIN, Marion
- Photochemistry and Photobiology, Vol. 11, Issue 6
Probing the 3d Spin Momentum with X-ray Emission Spectroscopy: The Case of Molecular-Spin Transitions
journal, June 2006
- Vankó, György; Neisius, Thomas; Molnár, Gábor
- The Journal of Physical Chemistry B, Vol. 110, Issue 24
Simultaneous detection of electronic structure changes from two elements of a bifunctional catalyst using wavelength-dispersive X-ray emission spectroscopy and in situ electrochemistry
journal, January 2015
- Gul, Sheraz; Ng, Jia Wei Desmond; Alonso-Mori, Roberto
- Physical Chemistry Chemical Physics, Vol. 17, Issue 14
The Electronic Structure of Mn in Oxides, Coordination Complexes, and the Oxygen-Evolving Complex of Photosystem II Studied by Resonant Inelastic X-ray Scattering
journal, August 2004
- Glatzel, Pieter; Bergmann, Uwe; Yano, Junko
- Journal of the American Chemical Society, Vol. 126, Issue 32
Electronic Structural Changes of Mn in the Oxygen-Evolving Complex of Photosystem II during the Catalytic Cycle
journal, April 2013
- Glatzel, Pieter; Schroeder, Henning; Pushkar, Yulia
- Inorganic Chemistry, Vol. 52, Issue 10
Photon Beam Transport and Scientific Instruments at the European XFEL
journal, June 2017
- Tschentscher, Thomas; Bressler, Christian; Grünert, Jan
- Applied Sciences, Vol. 7, Issue 6
Works referencing / citing this record:
A high-throughput energy-dispersive tender X-ray spectrometer for shot-to-shot sulfur measurements
journal, April 2019
- Abraham, Baxter; Nowak, Stanislaw; Weninger, Clemens
- Journal of Synchrotron Radiation, Vol. 26, Issue 3
Structural isomers of the S 2 state in photosystem II: do they exist at room temperature and are they important for function?
journal, March 2019
- Chatterjee, Ruchira; Lassalle, Louise; Gul, Sheraz
- Physiologia Plantarum, Vol. 166, Issue 1
Structures of the intermediates of Kok’s photosynthetic water oxidation clock
journal, November 2018
- Kern, Jan; Chatterjee, Ruchira; Young, Iris D.
- Nature, Vol. 563, Issue 7731
The Macromolecular Femtosecond Crystallography Instrument at the Linac Coherent Light Source
journal, February 2019
- Sierra, Raymond G.; Batyuk, Alexander; Sun, Zhibin
- Journal of Synchrotron Radiation, Vol. 26, Issue 2