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

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)

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.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: National Institutes of Health; National Institutes of Health (NIH); National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC02-05CH11231; AC02-76SF00515; AC02-98CH10886; SC0012704

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

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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A convolutional neural network-based screening tool for X-ray serial crystallography Ke, Tsung-Wei; Brewster, Aaron S.; Yu, Stella X. Journal of Synchrotron Radiation, Vol. 25, Issue 3, p. 655-670 https://doi.org/10.1107/s1600577518004873	journal	April 2018
The Macromolecular Femtosecond Crystallography Instrument at the Linac Coherent Light Source Sierra, Raymond G.; Batyuk, Alexander; Sun, Zhibin Journal of Synchrotron Radiation, Vol. 26, Issue 2 https://doi.org/10.1107/s1600577519001577	journal	February 2019
XANES and EXAFS of dilute solutions of transition metals at XFELs Chatterjee, Ruchira; Weninger, Clemens; Loukianov, Anton Journal of Synchrotron Radiation, Vol. 26, Issue 5 https://doi.org/10.1107/s1600577519007550	journal	August 2019
Reducing sample consumption for serial crystallography using acoustic drop ejection Davy, Bradley; Axford, Danny; Beale, John H. Journal of Synchrotron Radiation, Vol. 26, Issue 5 https://doi.org/10.1107/s1600577519009329	journal	August 2019
XFELs for structure and dynamics in biology Spence, J. C. H. IUCrJ, Vol. 4, Issue 4 https://doi.org/10.1107/s2052252517005760	journal	May 2017
Solving protein structure from sparse serial microcrystal diffraction data at a storage-ring synchrotron source Lan, Ti-Yen; Wierman, Jennifer L.; Tate, Mark W. IUCrJ, Vol. 5, Issue 5, p. 548-558 https://doi.org/10.1107/s205225251800903x	journal	July 2018
A fixed-target platform for serial femtosecond crystallography in a hydrated environment Shelby, M. L.; Gilbile, D.; Grant, T. D. IUCrJ, Vol. 7, Issue 1 https://doi.org/10.1107/s2052252519014003	journal	January 2020
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
Where is crystallography going? Grimes, Jonathan M.; Hall, David R.; Ashton, Alun W. Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 2 https://doi.org/10.1107/s2059798317016709	journal	February 2018
Using sound pulses to solve the crystal-harvesting bottleneck Samara, Yasmin N.; Brennan, Haley M.; McCarthy, Liam Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 10 https://doi.org/10.1107/s2059798318011506	journal	October 2018
Crystallography on a chip – without the chip: sheet-on-sheet sandwich Doak, R. Bruce; Nass Kovacs, Gabriela; Gorel, Alexander Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 10 https://doi.org/10.1107/s2059798318011634	journal	October 2018
Sample delivery for serial crystallography at free-electron lasers and synchrotrons Grünbein, Marie Luise; Nass Kovacs, Gabriela Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2 https://doi.org/10.1107/s205979831801567x	journal	January 2019
Journey to the center of the protein: allostery from multitemperature multiconformer X-ray crystallography Keedy, Daniel A. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2 https://doi.org/10.1107/s2059798318017941	journal	January 2019
Strategies for sample delivery for femtosecond crystallography Martiel, Isabelle; Müller-Werkmeister, Henrike M.; Cohen, Aina E. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2 https://doi.org/10.1107/s2059798318017953	journal	February 2019
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
A guide to sample delivery systems for serial crystallography Zhao, Feng‐Zhu; Zhang, Bin; Yan, Er‐Kai The FEBS Journal, Vol. 286, Issue 22 https://doi.org/10.1111/febs.15099	journal	August 2019
Structural isomers of the S ₂ state in photosystem II: do they exist at room temperature and are they important for function? Chatterjee, Ruchira; Lassalle, Louise; Gul, Sheraz Physiologia Plantarum, Vol. 166, Issue 1 https://doi.org/10.1111/ppl.12947	journal	March 2019
Acoustophoretic printing Foresti, Daniele; Kroll, Katharina T.; Amissah, Robert Science Advances, Vol. 4, Issue 8 https://doi.org/10.1126/sciadv.aat1659	journal	August 2018
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
Pump-Probe Time-Resolved Serial Femtosecond Crystallography at SACLA: Current Status and Data Collection Strategies Nango, Eriko; Kubo, Minoru; Tono, Kensuke Applied Sciences, Vol. 9, Issue 24 https://doi.org/10.3390/app9245505	journal	December 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
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

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