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

Franklin D. Fuller; Sheraz Gul; Ruchira Chatterjee; E. Sethe Burgie; Iris D. Young; Hugo Lebrette; Vivek Srinivas; Aaron S. Brewster; Tara Michels-Clark; Jonathan A. Clinger; Babak Andi; Mohamed Ibrahim; Ernest Pastor; Casper de Lichtenberg; Rana Hussein; Christopher J. Pollock; Miao Zhang; Claudiu A. Stan; Thomas Kroll; Thomas Fransson; Clemens Weninger; Markus Kubin; Pierre Aller; Louise Lassalle; Philipp Braeuer; Mitchell D. Miller; Muhamed Amin; Sergey Koroidov; Christian G. Roessler; Marc Allaire; Raymond G. Sierra; Peter T. Docker; James M. Glownia; Silke Nelson; Jason E. Koglin; Diling Zhu; Matthieu Chollet; Sanghoon Song; Henrik Lemke; Mengning Liang; Dimosthenis Sokaras; Roberto Alonso-Mori; Athina Zouni; Johannes Messinger; Uwe Bergmann; Amie K. Boal; J. Martin Bollinger; Carsten Krebs; Martin Hoegbom; George N. Phillips; Richard D. Vierstra; Nicholas K. Sauter; Allen M. Orville; Jan Kern; Vittal K. Yachandra; Junko Yano

doi:10.1038/nmeth.4195

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

Franklin D. Fuller, Sheraz Gul, Ruchira Chatterjee, E. Sethe Burgie, Iris D. Young, Hugo Lebrette, Vivek Srinivas, Aaron S. Brewster, Tara Michels-Clark, Jonathan A. Clinger, Babak Andi, Mohamed Ibrahim, Ernest Pastor, Casper de Lichtenberg, Rana Hussein, Christopher J. Pollock, Miao Zhang, Claudiu A. Stan, Thomas Kroll, Thomas FranssonClemens Weninger, Markus Kubin, Pierre Aller, Louise Lassalle, Philipp Braeuer, Mitchell D. Miller, Muhamed Amin, Sergey Koroidov, Christian G. Roessler, Marc Allaire, Raymond G. Sierra, Peter T. Docker, James M. Glownia, Silke Nelson, Jason E. Koglin, Diling Zhu, Matthieu Chollet, Sanghoon Song, Henrik Lemke, Mengning Liang, Dimosthenis Sokaras, Roberto Alonso-Mori, Athina Zouni, Johannes Messinger, Uwe Bergmann, Amie K. Boal, J. Martin Bollinger, Carsten Krebs, Martin Hoegbom, George N. Phillips, Richard D. Vierstra, Nicholas K. Sauter, Allen M. Orville, Jan Kern, Vittal K. Yachandra, Junko Yano

Research output: Contribution to journal › Article › Academic › peer-review

135 Citations (Scopus)

Abstract

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 IIII, the phytochrome photoreceptor, and ribonucleotide reductase R2 illustrate the power and versatility of this method.

Original language	English
Pages (from-to)	443-+
Number of pages	11
Journal	Nature Methods
Volume	14
Issue number	4
DOIs	https://doi.org/10.1038/nmeth.4195
Publication status	Published - Apr-2017
Externally published	Yes

Keywords

PHOTOSYSTEM-II
MANGANESE(IV)/IRON(III) COFACTOR
EMISSION SPECTROSCOPY
PHYTOCHROME
RESOLUTION
WATER
CRYSTALLOGRAPHY
DIFFRACTION
CHROMOPHORE
TRANSITION

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Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers
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Fuller, F. D., Gul, S., Chatterjee, R., Burgie, E. S., Young, I. D., Lebrette, H., Srinivas, V., Brewster, A. S., Michels-Clark, T., Clinger, J. A., Andi, B., Ibrahim, M., Pastor, E., de Lichtenberg, C., Hussein, R., Pollock, C. J., Zhang, M., Stan, C. A., Kroll, T., ... Yano, J. (2017). Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers. Nature Methods, 14(4), 443-+. https://doi.org/10.1038/nmeth.4195

@article{dab44e5533ca4adca62bbf59eb972af6,

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 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 IIII, the phytochrome photoreceptor, and ribonucleotide reductase R2 illustrate the power and versatility of this method.",

keywords = "PHOTOSYSTEM-II, MANGANESE(IV)/IRON(III) COFACTOR, EMISSION SPECTROSCOPY, PHYTOCHROME, RESOLUTION, WATER, CRYSTALLOGRAPHY, DIFFRACTION, CHROMOPHORE, TRANSITION",

author = "Fuller, {Franklin D.} and Sheraz Gul and Ruchira Chatterjee and Burgie, {E. Sethe} and Young, {Iris D.} and Hugo Lebrette and Vivek Srinivas and Brewster, {Aaron S.} and Tara Michels-Clark and Clinger, {Jonathan A.} and Babak Andi and Mohamed Ibrahim and Ernest Pastor and {de Lichtenberg}, Casper and Rana Hussein and Pollock, {Christopher J.} and Miao Zhang and Stan, {Claudiu A.} and Thomas Kroll and Thomas Fransson and Clemens Weninger and Markus Kubin and Pierre Aller and Louise Lassalle and Philipp Braeuer and Miller, {Mitchell D.} and Muhamed Amin and Sergey Koroidov and Roessler, {Christian G.} and Marc Allaire and Sierra, {Raymond G.} and Docker, {Peter T.} and Glownia, {James M.} and Silke Nelson and Koglin, {Jason E.} and Diling Zhu and Matthieu Chollet and Sanghoon Song and Henrik Lemke and Mengning Liang and Dimosthenis Sokaras and Roberto Alonso-Mori and Athina Zouni and Johannes Messinger and Uwe Bergmann and Boal, {Amie K.} and Bollinger, {J. Martin} and Carsten Krebs and Martin Hoegbom and Phillips, {George N.} and Vierstra, {Richard D.} and Sauter, {Nicholas K.} and Orville, {Allen M.} and Jan Kern and Yachandra, {Vittal K.} and Junko Yano",

year = "2017",

month = apr,

doi = "10.1038/nmeth.4195",

language = "English",

volume = "14",

pages = "443--+",

journal = "Nature Methods",

issn = "1548-7091",

publisher = "Nature Publishing Group",

number = "4",

}

Fuller, FD, Gul, S, Chatterjee, R, Burgie, ES, Young, ID, Lebrette, H, Srinivas, V, Brewster, AS, Michels-Clark, T, Clinger, JA, Andi, B, Ibrahim, M, Pastor, E, de Lichtenberg, C, Hussein, R, Pollock, CJ, Zhang, M, Stan, CA, Kroll, T, Fransson, T, Weninger, C, Kubin, M, Aller, P, Lassalle, L, Braeuer, P, Miller, MD, Amin, M, Koroidov, S, Roessler, CG, Allaire, M, Sierra, RG, Docker, PT, Glownia, JM, Nelson, S, Koglin, JE, Zhu, D, Chollet, M, Song, S, Lemke, H, Liang, M, Sokaras, D, Alonso-Mori, R, Zouni, A, Messinger, J, Bergmann, U, Boal, AK, Bollinger, JM, Krebs, C, Hoegbom, M, Phillips, GN, Vierstra, RD, Sauter, NK, Orville, AM, Kern, J, Yachandra, VK & Yano, J 2017, 'Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers', Nature Methods, vol. 14, no. 4, pp. 443-+. https://doi.org/10.1038/nmeth.4195

TY - JOUR

T1 - Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers

AU - Fuller, Franklin D.

AU - Gul, Sheraz

AU - Chatterjee, Ruchira

AU - Burgie, E. Sethe

AU - Young, Iris D.

AU - Lebrette, Hugo

AU - Srinivas, Vivek

AU - Brewster, Aaron S.

AU - Michels-Clark, Tara

AU - Clinger, Jonathan A.

AU - Andi, Babak

AU - Ibrahim, Mohamed

AU - Pastor, Ernest

AU - de Lichtenberg, Casper

AU - Hussein, Rana

AU - Pollock, Christopher J.

AU - Zhang, Miao

AU - Stan, Claudiu A.

AU - Kroll, Thomas

AU - Fransson, Thomas

AU - Weninger, Clemens

AU - Kubin, Markus

AU - Aller, Pierre

AU - Lassalle, Louise

AU - Braeuer, Philipp

AU - Miller, Mitchell D.

AU - Amin, Muhamed

AU - Koroidov, Sergey

AU - Roessler, Christian G.

AU - Allaire, Marc

AU - Sierra, Raymond G.

AU - Docker, Peter T.

AU - Glownia, James M.

AU - Nelson, Silke

AU - Koglin, Jason E.

AU - Zhu, Diling

AU - Chollet, Matthieu

AU - Song, Sanghoon

AU - Lemke, Henrik

AU - Liang, Mengning

AU - Sokaras, Dimosthenis

AU - Alonso-Mori, Roberto

AU - Zouni, Athina

AU - Messinger, Johannes

AU - Bergmann, Uwe

AU - Boal, Amie K.

AU - Bollinger, J. Martin

AU - Krebs, Carsten

AU - Hoegbom, Martin

AU - Phillips, George N.

AU - Vierstra, Richard D.

AU - Sauter, Nicholas K.

AU - Orville, Allen M.

AU - Kern, Jan

AU - Yachandra, Vittal K.

AU - Yano, Junko

PY - 2017/4

Y1 - 2017/4

N2 - 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 IIII, the phytochrome photoreceptor, and ribonucleotide reductase R2 illustrate the power and versatility of this method.

AB - 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 IIII, the phytochrome photoreceptor, and ribonucleotide reductase R2 illustrate the power and versatility of this method.

KW - PHOTOSYSTEM-II

KW - MANGANESE(IV)/IRON(III) COFACTOR

KW - EMISSION SPECTROSCOPY

KW - PHYTOCHROME

KW - RESOLUTION

KW - WATER

KW - CRYSTALLOGRAPHY

KW - DIFFRACTION

KW - CHROMOPHORE

KW - TRANSITION

U2 - 10.1038/nmeth.4195

DO - 10.1038/nmeth.4195

M3 - Article

SN - 1548-7091

VL - 14

SP - 443-+

JO - Nature Methods

JF - Nature Methods

IS - 4

ER -