Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers
Abstract
© 2017 Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved. X-ray crystallography at X-ray free-electron laser sources is a powerful method for studying macromolecules at biologically relevant temperatures. Moreover, when combined with complementary techniques like X-ray emission spectroscopy, both global structures and chemical properties of metalloenzymes can be obtained concurrently, providing insights into the interplay between the protein structure and dynamics and the chemistry at an active site. The implementation of such a multimodal approach can be compromised by conflicting requirements to optimize each individual method. In particular, the method used for sample delivery greatly affects the data quality. We present here a robust way of delivering controlled sample amounts on demand using acoustic droplet ejection coupled with a conveyor belt drive that is optimized for crystallography and spectroscopy measurements of photochemical and chemical reactions over a wide range of time scales. Studies with photosystem II, the phytochrome photoreceptor, and ribonucleotide reductase R2 illustrate the power and versatility of this method.
- Authors:
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- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division
- Washington Univ., St. Louis, MO (United States). Dept. of Biology
- Stockholm Univ. (Sweden). Dept. of Biochemistry and Biophysics
- Rice Univ., Houston, TX (United States). Dept. of BioSciences
- Brookhaven National Lab. (BNL), Upton, NY (United States). National Synchrotron Light Source II (NSLS-II)
- Humboldt Univ. of Berlin (Germany). Inst. fur Biologie
- Umea Univ. (Sweden). Inst. for Kemi, Kemiskt Biologiskt Centrum
- Pennsylvania State Univ., University Park, PA (United States). Dept. of Chemistry
- SLAC National Accelerator Lab., Menlo Park, CA (United States). Photon Ultrafast Laser Science and Engineering Inst. (PULSE)
- SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
- SLAC National Accelerator Lab., Menlo Park, CA (United States). Photon Ultrafast Laser Science and Engineering Inst. (PULSE); SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
- Helmholtz-Zentrum Berlin (HZB), (Germany). German Research Centre for Materials and Energy, Inst. for Methods and Instrumentation on Synchrotron Radiation Research
- Science and Technology Facilities Council (STFC), Harwell Campus, Oxford (United Kingdom). Diamond Light Source, Ltd.
- Science and Technology Facilities Council (STFC), Harwell Campus, Oxford (United Kingdom). Diamond Light Source, Ltd.; Univ. of Oxford (United Kingdom). Dept. of Biochemistry
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division; Zewail City of Science and Technology, Giza (Egypt). Center for Photonics and Smart Materials (CPSM)
- Umea Univ. (Sweden). Inst. for Kemi, Kemiskt Biologiskt Centrum; SLAC National Accelerator Lab., Menlo Park, CA (United States). Photon Ultrafast Laser Science and Engineering Inst. (PULSE)
- Brookhaven National Lab. (BNL), Upton, NY (United States). National Synchrotron Light Source II (NSLS-II); Ventana Medical Systems, Inc., Tucson, AZ (United States)
- SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
- SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS); Paul Scherrer Inst. (PSI), Villigen (Switzerland). SwissFEL
- Umea Univ. (Sweden). Inst. for Kemi, Kemiskt Biologiskt Centrum; Uppsala Univ. (Sweden). Dept. of Chemistry - Angstrom, Molecular Biomimetics
- Pennsylvania State Univ., University Park, PA (United States). Dept. of Chemistry; Pennsylvania State Univ., University Park, PA (United States). Dept. of Biochemistry and Molecular Biology
- Stockholm Univ. (Sweden). Dept. of Biochemistry and Biophysics; Stanford Univ., CA (United States). Dept. of Chemistry
- Rice Univ., Houston, TX (United States). Dept. of BioSciences; Rice Univ., Houston, TX (United States). Dept. of Chemistry
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division; SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
- Publication Date:
- Research Org.:
- SLAC National Accelerator Lab., Menlo Park, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Brookhaven National Lab. (BNL), Upton, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); National Institutes of Health (NIH)
- OSTI Identifier:
- 1360909
- Alternate Identifier(s):
- OSTI ID: 1379743; OSTI ID: 1392209
- Report Number(s):
- BNL-114091-2017-JA
Journal ID: ISSN 1548-7091; nmeth.4195
- Grant/Contract Number:
- AC02-76SF00515; AC02-05CH11231; AC02-98CH10886; SC0012704; GM110501; P41GM111244; P41GM103393; 2013-541; 2013-5884; 8P41GM103473-16; 2-P41-RR012408
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Methods
- Additional Journal Information:
- Journal Volume: 14; Journal Issue: 4; Journal ID: ISSN 1548-7091
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Biocatalysis; Biophysical methods; Enzymes; Molecular biophysics; Nanocrystallography
Citation Formats
Fuller, Franklin D., Gul, Sheraz, Chatterjee, Ruchira, Burgie, E. Sethe, Young, Iris D., Lebrette, Hugo, Srinivas, Vivek, Brewster, Aaron S., Michels-Clark, Tara, Clinger, Jonathan A., Andi, Babak, Ibrahim, Mohamed, Pastor, Ernest, de Lichtenberg, Casper, Hussein, Rana, Pollock, Christopher J., Zhang, Miao, Stan, Claudiu A., Kroll, Thomas, Fransson, Thomas, Weninger, Clemens, Kubin, Markus, Aller, Pierre, Lassalle, Louise, Bräuer, Philipp, Miller, Mitchell D., Amin, Muhamed, Koroidov, Sergey, Roessler, Christian G., Allaire, Marc, Sierra, Raymond G., Docker, Peter T., Glownia, James M., Nelson, Silke, Koglin, Jason E., Zhu, Diling, Chollet, Matthieu, Song, Sanghoon, Lemke, Henrik, Liang, Mengning, Sokaras, Dimosthenis, Alonso-Mori, Roberto, Zouni, Athina, Messinger, Johannes, Bergmann, Uwe, Boal, Amie K., Bollinger, J. Martin, Krebs, Carsten, Högbom, Martin, Phillips, George N., Vierstra, Richard D., Sauter, Nicholas K., Orville, Allen M., Kern, Jan, Yachandra, Vittal K., and Yano, Junko. Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers. United States: N. p., 2017.
Web. doi:10.1038/nmeth.4195.
Fuller, Franklin D., Gul, Sheraz, Chatterjee, Ruchira, Burgie, E. Sethe, Young, Iris D., Lebrette, Hugo, Srinivas, Vivek, Brewster, Aaron S., Michels-Clark, Tara, Clinger, Jonathan A., Andi, Babak, Ibrahim, Mohamed, Pastor, Ernest, de Lichtenberg, Casper, Hussein, Rana, Pollock, Christopher J., Zhang, Miao, Stan, Claudiu A., Kroll, Thomas, Fransson, Thomas, Weninger, Clemens, Kubin, Markus, Aller, Pierre, Lassalle, Louise, Bräuer, Philipp, Miller, Mitchell D., Amin, Muhamed, Koroidov, Sergey, Roessler, Christian G., Allaire, Marc, Sierra, Raymond G., Docker, Peter T., Glownia, James M., Nelson, Silke, Koglin, Jason E., Zhu, Diling, Chollet, Matthieu, Song, Sanghoon, Lemke, Henrik, Liang, Mengning, Sokaras, Dimosthenis, Alonso-Mori, Roberto, Zouni, Athina, Messinger, Johannes, Bergmann, Uwe, Boal, Amie K., Bollinger, J. Martin, Krebs, Carsten, Högbom, Martin, Phillips, George N., Vierstra, Richard D., Sauter, Nicholas K., Orville, Allen M., Kern, Jan, Yachandra, Vittal K., & Yano, Junko. Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers. United States. https://doi.org/10.1038/nmeth.4195
Fuller, Franklin D., Gul, Sheraz, Chatterjee, Ruchira, Burgie, E. Sethe, Young, Iris D., Lebrette, Hugo, Srinivas, Vivek, Brewster, Aaron S., Michels-Clark, Tara, Clinger, Jonathan A., Andi, Babak, Ibrahim, Mohamed, Pastor, Ernest, de Lichtenberg, Casper, Hussein, Rana, Pollock, Christopher J., Zhang, Miao, Stan, Claudiu A., Kroll, Thomas, Fransson, Thomas, Weninger, Clemens, Kubin, Markus, Aller, Pierre, Lassalle, Louise, Bräuer, Philipp, Miller, Mitchell D., Amin, Muhamed, Koroidov, Sergey, Roessler, Christian G., Allaire, Marc, Sierra, Raymond G., Docker, Peter T., Glownia, James M., Nelson, Silke, Koglin, Jason E., Zhu, Diling, Chollet, Matthieu, Song, Sanghoon, Lemke, Henrik, Liang, Mengning, Sokaras, Dimosthenis, Alonso-Mori, Roberto, Zouni, Athina, Messinger, Johannes, Bergmann, Uwe, Boal, Amie K., Bollinger, J. Martin, Krebs, Carsten, Högbom, Martin, Phillips, George N., Vierstra, Richard D., Sauter, Nicholas K., Orville, Allen M., Kern, Jan, Yachandra, Vittal K., and Yano, Junko. Mon .
"Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers". United States. https://doi.org/10.1038/nmeth.4195. https://www.osti.gov/servlets/purl/1360909.
@article{osti_1360909,
title = {Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers},
author = {Fuller, Franklin D. and Gul, Sheraz and Chatterjee, Ruchira and Burgie, E. Sethe and Young, Iris D. and Lebrette, Hugo and Srinivas, Vivek and Brewster, Aaron S. and Michels-Clark, Tara and Clinger, Jonathan A. and Andi, Babak and Ibrahim, Mohamed and Pastor, Ernest and de Lichtenberg, Casper and Hussein, Rana and Pollock, Christopher J. and Zhang, Miao and Stan, Claudiu A. and Kroll, Thomas and Fransson, Thomas and Weninger, Clemens and Kubin, Markus and Aller, Pierre and Lassalle, Louise and Bräuer, Philipp and Miller, Mitchell D. and Amin, Muhamed and Koroidov, Sergey and Roessler, Christian G. and Allaire, Marc and Sierra, Raymond G. and Docker, Peter T. and Glownia, James M. and Nelson, Silke and Koglin, Jason E. and Zhu, Diling and Chollet, Matthieu and Song, Sanghoon and Lemke, Henrik and Liang, Mengning and Sokaras, Dimosthenis and Alonso-Mori, Roberto and Zouni, Athina and Messinger, Johannes and Bergmann, Uwe and Boal, Amie K. and Bollinger, J. Martin and Krebs, Carsten and Högbom, Martin and Phillips, George N. and Vierstra, Richard D. and Sauter, Nicholas K. and Orville, Allen M. and Kern, Jan and Yachandra, Vittal K. and Yano, Junko},
abstractNote = {© 2017 Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved. X-ray crystallography at X-ray free-electron laser sources is a powerful method for studying macromolecules at biologically relevant temperatures. Moreover, when combined with complementary techniques like X-ray emission spectroscopy, both global structures and chemical properties of metalloenzymes can be obtained concurrently, providing insights into the interplay between the protein structure and dynamics and the chemistry at an active site. The implementation of such a multimodal approach can be compromised by conflicting requirements to optimize each individual method. In particular, the method used for sample delivery greatly affects the data quality. We present here a robust way of delivering controlled sample amounts on demand using acoustic droplet ejection coupled with a conveyor belt drive that is optimized for crystallography and spectroscopy measurements of photochemical and chemical reactions over a wide range of time scales. Studies with photosystem II, the phytochrome photoreceptor, and ribonucleotide reductase R2 illustrate the power and versatility of this method.},
doi = {10.1038/nmeth.4195},
journal = {Nature Methods},
number = 4,
volume = 14,
place = {United States},
year = {2017},
month = {2}
}
Web of Science
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- Ke, Tsung-Wei; Brewster, Aaron S.; Yu, Stella X.
- Journal of Synchrotron Radiation, Vol. 25, Issue 3, p. 655-670
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
XANES and EXAFS of dilute solutions of transition metals at XFELs
journal, August 2019
- Chatterjee, Ruchira; Weninger, Clemens; Loukianov, Anton
- Journal of Synchrotron Radiation, Vol. 26, Issue 5
Reducing sample consumption for serial crystallography using acoustic drop ejection
journal, August 2019
- Davy, Bradley; Axford, Danny; Beale, John H.
- Journal of Synchrotron Radiation, Vol. 26, Issue 5
XFELs for structure and dynamics in biology
journal, May 2017
- Spence, J. C. H.
- IUCrJ, Vol. 4, Issue 4
Solving protein structure from sparse serial microcrystal diffraction data at a storage-ring synchrotron source
journal, July 2018
- Lan, Ti-Yen; Wierman, Jennifer L.; Tate, Mark W.
- IUCrJ, Vol. 5, Issue 5, p. 548-558
A fixed-target platform for serial femtosecond crystallography in a hydrated environment
journal, January 2020
- Shelby, M. L.; Gilbile, D.; Grant, T. D.
- IUCrJ, Vol. 7, Issue 1
Where is crystallography going?
journal, February 2018
- Grimes, Jonathan M.; Hall, David R.; Ashton, Alun W.
- Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 2
Using sound pulses to solve the crystal-harvesting bottleneck
journal, October 2018
- Samara, Yasmin N.; Brennan, Haley M.; McCarthy, Liam
- Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 10
Crystallography on a chip – without the chip: sheet-on-sheet sandwich
journal, October 2018
- Doak, R. Bruce; Nass Kovacs, Gabriela; Gorel, Alexander
- Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 10
Sample delivery for serial crystallography at free-electron lasers and synchrotrons
journal, January 2019
- Grünbein, Marie Luise; Nass Kovacs, Gabriela
- Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2
Journey to the center of the protein: allostery from multitemperature multiconformer X-ray crystallography
journal, January 2019
- Keedy, Daniel A.
- Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2
Strategies for sample delivery for femtosecond crystallography
journal, February 2019
- Martiel, Isabelle; Müller-Werkmeister, Henrike M.; Cohen, Aina E.
- Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2
A guide to sample delivery systems for serial crystallography
journal, August 2019
- Zhao, Feng‐Zhu; Zhang, Bin; Yan, Er‐Kai
- The FEBS Journal, Vol. 286, Issue 22
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
Acoustophoretic printing
journal, August 2018
- Foresti, Daniele; Kroll, Katharina T.; Amissah, Robert
- Science Advances, Vol. 4, Issue 8
Pump-Probe Time-Resolved Serial Femtosecond Crystallography at SACLA: Current Status and Data Collection Strategies
journal, December 2019
- Nango, Eriko; Kubo, Minoru; Tono, Kensuke
- Applied Sciences, Vol. 9, Issue 24
Capturing an initial intermediate during the P450nor enzymatic reaction using time-resolved XFEL crystallography and caged-substrate
journal, November 2017
- Tosha, Takehiko; Nomura, Takashi; Nishida, Takuma
- Nature Communications, Vol. 8, Article No. 1585
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
Non-Contact Universal Sample Presentation for Room Temperature Macromolecular Crystallography Using Acoustic Levitation
journal, August 2019
- Morris, R. H.; Dye, E. R.; Axford, D.
- Scientific Reports, Vol. 9, Issue 1
On-demand sample injection: combining acoustic actuation with a tear-drop shaped nozzle to generate droplets with precise spatial and temporal control
journal, January 2020
- Brenker, Jason C.; Devendran, Citsabehsan; Neild, Adrian
- Lab on a Chip, Vol. 20, Issue 2
A fixed-target platform for serial femtosecond crystallography in a hydrated environment
text, January 2020
- Shelby, M. L.; Gilbile, D.; Grant, T. D.
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Acoustophoretic printing
text, January 2018
- Foresti, Daniele; Kroll, Katharina T.; Amissah, Robert
- ETH Zurich
Perspective: Opportunities for ultrafast science at SwissFEL
text, January 2017
- Abela, Rafael; Beaud, Paul; Van Bokhoven, Jeroen A.
- AIP Publishing
Comparing serial X-ray crystallography and microcrystal electron diffraction (MicroED) as methods for routine structure determination from small macromolecular crystals
journal, February 2020
- Wolff, Alexander M.; Young, Iris D.; Sierra, Raymond G.
- IUCrJ, Vol. 7, Issue 2
Strategies for sample delivery for femtosecond crystallography
text, January 2019
- Martiel, Isabelle; Müller-Werkmeister, Henrike M.; Cohen, Aina E.
- International Union of Crystallography (IUCr)
Perspective: Opportunities for ultrafast science at SwissFEL
text, January 2017
- Abela, Rafael; Beaud, Paul; Van Bokhoven, Jeroen A.
- ETH Zurich