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

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

doi:10.1038/nmeth.4195

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

Journal Article · Mon Feb 27 00:00:00 EST 2017 · Nature Methods

DOI:https://doi.org/10.1038/nmeth.4195· OSTI ID:1360909

Fuller, Franklin D. ^[1]; Gul, Sheraz ^[1]; Chatterjee, Ruchira ^[1]; Burgie, E. Sethe ^[2]; Young, Iris D. ^[1]; Lebrette, Hugo ^[3]; Srinivas, Vivek ^[3]; Brewster, Aaron S. ^[1]; Michels-Clark, Tara ^[1]; Clinger, Jonathan A. ^[4];

^[5]; Ibrahim, Mohamed ^[6]; Pastor, Ernest ^[1]; de Lichtenberg, Casper ^[7]; Hussein, Rana ^[6]; Pollock, Christopher J. ^[8]; Zhang, Miao ^[6]; Stan, Claudiu A. ^[9]; Kroll, Thomas ^[10]; Fransson, Thomas ^[9] more »

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)

© 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.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); National Institutes of Health (NIH)

Grant/Contract Number:: AC02-76SF00515; AC02-05CH11231; AC02-98CH10886; SC0012704; GM110501; P41GM111244; P41GM103393; 2013-541; 2013-5884; 8P41GM103473-16; 2-P41-RR012408

OSTI ID:: 1360909

Alternate ID(s):: OSTI ID: 1379743; OSTI ID: 1392209

Report Number(s):: BNL-114091-2017-JA; nmeth.4195

Journal Information:: Nature Methods, Vol. 14, Issue 4; ISSN 1548-7091

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 125 works

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Capturing an initial intermediate during the P450nor enzymatic reaction using time-resolved XFEL crystallography and caged-substrate Tosha, Takehiko; Nomura, Takashi; Nishida, Takuma Nature Communications, Vol. 8, Article No. 1585 https://doi.org/10.1038/s41467-017-01702-1	journal	November 2017
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
Non-Contact Universal Sample Presentation for Room Temperature Macromolecular Crystallography Using Acoustic Levitation Morris, R. H.; Dye, E. R.; Axford, D. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-48612-4	journal	August 2019
On-demand sample injection: combining acoustic actuation with a tear-drop shaped nozzle to generate droplets with precise spatial and temporal control Brenker, Jason C.; Devendran, Citsabehsan; Neild, Adrian Lab on a Chip, Vol. 20, Issue 2 https://doi.org/10.1039/c9lc00837c	journal	January 2020
A fixed-target platform for serial femtosecond crystallography in a hydrated environment Shelby, M. L.; Gilbile, D.; Grant, T. D. Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2019-05316	text	January 2020
Acoustophoretic printing Foresti, Daniele; Kroll, Katharina T.; Amissah, Robert ETH Zurich https://doi.org/10.3929/ethz-b-000289614	text	January 2018
Perspective: Opportunities for ultrafast science at SwissFEL Abela, Rafael; Beaud, Paul; Van Bokhoven, Jeroen A. AIP Publishing https://doi.org/10.7892/boris.114739	text	January 2017
Comparing serial X-ray crystallography and microcrystal electron diffraction (MicroED) as methods for routine structure determination from small macromolecular crystals Wolff, Alexander M.; Young, Iris D.; Sierra, Raymond G. IUCrJ, Vol. 7, Issue 2 https://doi.org/10.1107/s205225252000072x	journal	February 2020
Strategies for sample delivery for femtosecond crystallography Martiel, Isabelle; Müller-Werkmeister, Henrike M.; Cohen, Aina E. International Union of Crystallography (IUCr) https://doi.org/10.1107/s2059798318017953/ba5296sup1.pdf	text	January 2019
Perspective: Opportunities for ultrafast science at SwissFEL Abela, Rafael; Beaud, Paul; Van Bokhoven, Jeroen A. ETH Zurich https://doi.org/10.3929/ethz-b-000231826	text	January 2017

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