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Title: Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers

Abstract

X-ray crystallography at X-ray free-electron laser (XFEL) sources is a powerful method for studying macromolecules at biologically relevant temperatures. Moreover, when combined with complementary techniques like X-ray emission spectroscopy (XES), both global structures and chemical properties of metalloenzymes can be obtained concurrently, providing new insights into the interplay between the protein structure/dynamics and chemistry at an active site. However, implementing such a multimodal approach can be compromised by conflicting requirements to optimize each individual method. In particular, the method used for sample delivery greatly impacts the data quality. We present here a new, 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:
 [1];  [1];  [1];  [2];  [1];  [3];  [3];  [1];  [1];  [4]; ORCiD logo [5];  [6];  [1];  [7];  [6];  [8];  [6];  [9];  [10];  [9] more »;  [11];  [12];  [13];  [1];  [14];  [4];  [15];  [16];  [17];  [1]; ORCiD logo [18];  [13];  [18];  [18]; ORCiD logo [18];  [18];  [18]; ORCiD logo [18]; ORCiD logo [19];  [18];  [10]; ORCiD logo [18];  [6];  [20]; ORCiD logo [9];  [21];  [21];  [21];  [22];  [23];  [2];  [1];  [13]; ORCiD logo [24];  [1]; ORCiD logo [1] « less
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division
  2. Washington Univ., St. Louis, MO (United States). Dept. of Biology
  3. Stockholm Univ. (Sweden). Dept. of Biochemistry and Biophysics
  4. Rice Univ., Houston, TX (United States). Dept. of BioSciences
  5. Brookhaven National Lab. (BNL), Upton, NY (United States). National Synchrotron Light Source II (NSLS-II)
  6. Humboldt Univ. of Berlin (Germany). Inst. fur Biologie
  7. Umea Univ. (Sweden). Inst. for Kemi, Kemiskt Biologiskt Centrum
  8. Pennsylvania State Univ., University Park, PA (United States). Dept. of Chemistry
  9. SLAC National Accelerator Lab., Menlo Park, CA (United States). Photon Ultrafast Laser Science and Engineering Inst. (PULSE)
  10. SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
  11. 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)
  12. Helmholtz-Zentrum Berlin (HZB), (Germany). German Research Centre for Materials and Energy, Inst. for Methods and Instrumentation on Synchrotron Radiation Research
  13. Science and Technology Facilities Council (STFC), Harwell Campus, Oxford (United Kingdom). Diamond Light Source, Ltd.
  14. Science and Technology Facilities Council (STFC), Harwell Campus, Oxford (United Kingdom). Diamond Light Source, Ltd.; Univ. of Oxford (United Kingdom). Dept. of Biochemistry
  15. 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)
  16. 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)
  17. Brookhaven National Lab. (BNL), Upton, NY (United States). National Synchrotron Light Source II (NSLS-II); Ventana Medical Systems, Inc., Tucson, AZ (United States)
  18. SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
  19. SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS); Paul Scherrer Inst. (PSI), Villigen (Switzerland). SwissFEL
  20. Umea Univ. (Sweden). Inst. for Kemi, Kemiskt Biologiskt Centrum; Uppsala Univ. (Sweden). Dept. of Chemistry - Angstrom, Molecular Biomimetics
  21. 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
  22. Stockholm Univ. (Sweden). Dept. of Biochemistry and Biophysics; Stanford Univ., CA (United States). Dept. of Chemistry
  23. Rice Univ., Houston, TX (United States). Dept. of BioSciences; Rice Univ., Houston, TX (United States). Dept. of Chemistry
  24. 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) (SC-22); 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. 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., and Yano, Junko. Mon . "Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers". United States. doi: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 = {X-ray crystallography at X-ray free-electron laser (XFEL) sources is a powerful method for studying macromolecules at biologically relevant temperatures. Moreover, when combined with complementary techniques like X-ray emission spectroscopy (XES), both global structures and chemical properties of metalloenzymes can be obtained concurrently, providing new insights into the interplay between the protein structure/dynamics and chemistry at an active site. However, implementing such a multimodal approach can be compromised by conflicting requirements to optimize each individual method. In particular, the method used for sample delivery greatly impacts the data quality. We present here a new, 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}
}

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