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Title: Improvements in serial femtosecond crystallography of photosystem II by optimizing crystal uniformity using microseeding procedures

Abstract

In photosynthesis, photosystem II (PSII) is the multi-subunit membrane protein complex that catalyzes photo-oxidation of water into dioxygen through the oxygen evolving complex (OEC). To understand the water oxidation reaction, it is important to get structural information about the transient and intermediate states of the OEC in the dimeric PSII core complex (dPSIIcc). In recent times, femtosecond X-ray pulses from the free electron laser (XFEL) are being used to obtain X-ray diffraction (XRD) data of dPSIIcc microcrystals at room temperature that are free of radiation damage. In our experiments at the XFEL, we used an electrospun liquid microjet setup that requires microcrystals less than 40 μm in size. In this study, we explored various microseeding techniques to get a high yield of monodisperse uniform-sized microcrystals. Monodisperse microcrystals of dPSIIcc of uniform size were a key to improve the stability of the jet and the quality of XRD data obtained at the XFEL. This was evident by an improvement of the quality of the datasets obtained, from 6.5 Å, using crystals grown without the micro seeding approach, to 4.5 Å using crystals generated with the new method.

Authors:
 [1];  [2];  [1];  [2];  [3];  [4];  [2];  [2];  [1]
  1. Humboldt Univ. of Berlin, Berlin (Germany); Technische Univ. Berlin (Germany). Max-Volmer-Lab. fuer Biophysikalische Chemie
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Div.
  3. Humboldt Univ. of Berlin, Berlin (Germany)
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1190859
Alternate Identifier(s):
OSTI ID: 1421052; OSTI ID: 1512111
Grant/Contract Number:  
AC02-05CH11231; GM055302
Resource Type:
Accepted Manuscript
Journal Name:
Structural Dynamics
Additional Journal Information:
Journal Volume: 2; Journal Issue: 4; Journal ID: ISSN 2329-7778
Publisher:
American Crystallographic Association/AIP
Country of Publication:
United States
Language:
English
Subject:
36 MATERIALS SCIENCE; 75 CONDENSED MATTER PHYSICS, SUPERCONDUCTIVITY AND SUPERFLUIDITY; 59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Ibrahim, Mohamed, Chatterjee, Ruchira, Hellmich, Julia, Tran, Rosalie, Bommer, Martin, Yachandra, Vittal K., Yano, Junko, Kern, Jan, and Zouni, Athina. Improvements in serial femtosecond crystallography of photosystem II by optimizing crystal uniformity using microseeding procedures. United States: N. p., 2015. Web. doi:10.1063/1.4919741.
Ibrahim, Mohamed, Chatterjee, Ruchira, Hellmich, Julia, Tran, Rosalie, Bommer, Martin, Yachandra, Vittal K., Yano, Junko, Kern, Jan, & Zouni, Athina. Improvements in serial femtosecond crystallography of photosystem II by optimizing crystal uniformity using microseeding procedures. United States. https://doi.org/10.1063/1.4919741
Ibrahim, Mohamed, Chatterjee, Ruchira, Hellmich, Julia, Tran, Rosalie, Bommer, Martin, Yachandra, Vittal K., Yano, Junko, Kern, Jan, and Zouni, Athina. Wed . "Improvements in serial femtosecond crystallography of photosystem II by optimizing crystal uniformity using microseeding procedures". United States. https://doi.org/10.1063/1.4919741. https://www.osti.gov/servlets/purl/1190859.
@article{osti_1190859,
title = {Improvements in serial femtosecond crystallography of photosystem II by optimizing crystal uniformity using microseeding procedures},
author = {Ibrahim, Mohamed and Chatterjee, Ruchira and Hellmich, Julia and Tran, Rosalie and Bommer, Martin and Yachandra, Vittal K. and Yano, Junko and Kern, Jan and Zouni, Athina},
abstractNote = {In photosynthesis, photosystem II (PSII) is the multi-subunit membrane protein complex that catalyzes photo-oxidation of water into dioxygen through the oxygen evolving complex (OEC). To understand the water oxidation reaction, it is important to get structural information about the transient and intermediate states of the OEC in the dimeric PSII core complex (dPSIIcc). In recent times, femtosecond X-ray pulses from the free electron laser (XFEL) are being used to obtain X-ray diffraction (XRD) data of dPSIIcc microcrystals at room temperature that are free of radiation damage. In our experiments at the XFEL, we used an electrospun liquid microjet setup that requires microcrystals less than 40 μm in size. In this study, we explored various microseeding techniques to get a high yield of monodisperse uniform-sized microcrystals. Monodisperse microcrystals of dPSIIcc of uniform size were a key to improve the stability of the jet and the quality of XRD data obtained at the XFEL. This was evident by an improvement of the quality of the datasets obtained, from 6.5 Å, using crystals grown without the micro seeding approach, to 4.5 Å using crystals generated with the new method.},
doi = {10.1063/1.4919741},
journal = {Structural Dynamics},
number = 4,
volume = 2,
place = {United States},
year = {Wed Apr 29 00:00:00 EDT 2015},
month = {Wed Apr 29 00:00:00 EDT 2015}
}

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Works referenced in this record:

Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen
journal, January 2001

  • Krogh, Anders; Larsson, Björn; von Heijne, Gunnar
  • Journal of Molecular Biology, Vol. 305, Issue 3
  • DOI: 10.1006/jmbi.2000.4315

How many drug targets are there?
journal, December 2006

  • Overington, John P.; Al-Lazikani, Bissan; Hopkins, Andrew L.
  • Nature Reviews Drug Discovery, Vol. 5, Issue 12
  • DOI: 10.1038/nrd2199

Overcoming the challenges of membrane protein crystallography
journal, October 2008

  • Carpenter, Elisabeth P.; Beis, Konstantinos; Cameron, Alexander D.
  • Current Opinion in Structural Biology, Vol. 18, Issue 5
  • DOI: 10.1016/j.sbi.2008.07.001

Small is beautiful: protein micro-crystallography
journal, August 1998

  • Cusack, Stephen; Belrhali, Hassan; Bram, Andreas
  • Nature Structural Biology, Vol. 5, Issue 8
  • DOI: 10.1038/1325

Energy recovery linacs as synchrotron radiation sources (invited)
journal, March 2002

  • Gruner, Sol M.; Bilderback, Don; Bazarov, Ivan
  • Review of Scientific Instruments, Vol. 73, Issue 3
  • DOI: 10.1063/1.1420754

Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy
journal, July 2014

  • Kern, Jan; Tran, Rosalie; Alonso-Mori, Roberto
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms5371

Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein
journal, December 2014


Light induced oxidative water splitting in photosynthesis: Energetics, kinetics and mechanism
journal, July 2011


COOPERATION OF CHARGES IN PHOTOSYNTHETIC O 2 EVOLUTION–I. A LINEAR FOUR STEP MECHANISM
journal, June 1970


Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å
journal, April 2011

  • Umena, Yasufumi; Kawakami, Keisuke; Shen, Jian-Ren
  • Nature, Vol. 473, Issue 7345
  • DOI: 10.1038/nature09913

X-ray damage to the Mn4Ca complex in single crystals of photosystem II: A case study for metalloprotein crystallography
journal, August 2005

  • Yano, J.; Kern, J.; Irrgang, K. -D.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 34
  • DOI: 10.1073/pnas.0505207102

Structural Changes of the Oxygen-evolving Complex in Photosystem II during the Catalytic Cycle
journal, June 2013

  • Glöckner, Carina; Kern, Jan; Broser, Matthias
  • Journal of Biological Chemistry, Vol. 288, Issue 31
  • DOI: 10.1074/jbc.M113.476622

Room temperature femtosecond X-ray diffraction of photosystem II microcrystals
journal, June 2012

  • Kern, J.; Alonso-Mori, R.; Hellmich, J.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 25, p. 9721-9726
  • DOI: 10.1073/pnas.1204598109

Simultaneous Femtosecond X-ray Spectroscopy and Diffraction of Photosystem II at Room Temperature
journal, February 2013


Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser
journal, July 2014

  • Kupitz, Christopher; Basu, Shibom; Grotjohann, Ingo
  • Nature, Vol. 513, Issue 7517
  • DOI: 10.1038/nature13453

Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses
journal, November 2014

  • Suga, Michihiro; Akita, Fusamichi; Hirata, Kunio
  • Nature, Vol. 517, Issue 7532
  • DOI: 10.1038/nature13991

Mix and Inject: Reaction Initiation by Diffusion for Time-Resolved Macromolecular Crystallography
journal, January 2013


Purification, characterisation and crystallisation of photosystem II from Thermosynechococcus elongatus cultivated in a new type of photobioreactor
journal, January 2005

  • Kern, J.; Loll, B.; Lüneberg, C.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1706, Issue 1-2
  • DOI: 10.1016/j.bbabio.2004.10.007

The Coherent X-ray Imaging (CXI) instrument at the Linac Coherent Light Source (LCLS)
journal, March 2010


X-ray tests of a Pixel Array Detector for coherent x-ray imaging at the Linac Coherent Light Source
journal, March 2009


Extinction coefficients and critical solubilisation concentrations of photosystems I and II from Thermosynechococcus elongatus
journal, June 2005


Crystallization and the Crystal Properties of the Oxygen-Evolving Photosystem II from Synechococcus vulcanus
journal, December 2000

  • Shen, Jian-Ren; Kamiya, Nobuo
  • Biochemistry, Vol. 39, Issue 48
  • DOI: 10.1021/bi001402m

Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride
journal, February 2009

  • Guskov, Albert; Kern, Jan; Gabdulkhakov, Azat
  • Nature Structural & Molecular Biology, Vol. 16, Issue 3
  • DOI: 10.1038/nsmb.1559

Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen
journal, January 2001

  • Krogh, Anders; Larsson, Björn; von Heijne, Gunnar
  • Journal of Molecular Biology, Vol. 305, Issue 3
  • DOI: 10.1006/jmbi.2000.4315

Purification, characterisation and crystallisation of photosystem II from Thermosynechococcus elongatus cultivated in a new type of photobioreactor
journal, January 2005

  • Kern, J.; Loll, B.; Lüneberg, C.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1706, Issue 1-2
  • DOI: 10.1016/j.bbabio.2004.10.007

Transport and metabolism of d-lactate in Jerusalem artichoke mitochondria
journal, June 2005

  • Atlante, Anna; de Bari, Lidia; Valenti, Daniela
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1708, Issue 1
  • DOI: 10.1016/j.bbabio.2005.03.003

Light induced oxidative water splitting in photosynthesis: Energetics, kinetics and mechanism
journal, July 2011


Overcoming the challenges of membrane protein crystallography
journal, October 2008

  • Carpenter, Elisabeth P.; Beis, Konstantinos; Cameron, Alexander D.
  • Current Opinion in Structural Biology, Vol. 18, Issue 5
  • DOI: 10.1016/j.sbi.2008.07.001

Seeds to crystals
journal, April 2003


Crystallization and the Crystal Properties of the Oxygen-Evolving Photosystem II from Synechococcus vulcanus
journal, December 2000

  • Shen, Jian-Ren; Kamiya, Nobuo
  • Biochemistry, Vol. 39, Issue 48
  • DOI: 10.1021/bi001402m

Small is beautiful: protein micro-crystallography
journal, August 1998

  • Cusack, Stephen; Belrhali, Hassan; Bram, Andreas
  • Nature Structural Biology, Vol. 5, Issue 8
  • DOI: 10.1038/1325

Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses
journal, November 2014

  • Suga, Michihiro; Akita, Fusamichi; Hirata, Kunio
  • Nature, Vol. 517, Issue 7532
  • DOI: 10.1038/nature13991

How many drug targets are there?
journal, December 2006

  • Overington, John P.; Al-Lazikani, Bissan; Hopkins, Andrew L.
  • Nature Reviews Drug Discovery, Vol. 5, Issue 12
  • DOI: 10.1038/nrd2199

Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride
journal, February 2009

  • Guskov, Albert; Kern, Jan; Gabdulkhakov, Azat
  • Nature Structural & Molecular Biology, Vol. 16, Issue 3
  • DOI: 10.1038/nsmb.1559

X-ray damage to the Mn4Ca complex in single crystals of photosystem II: A case study for metalloprotein crystallography
journal, August 2005

  • Yano, J.; Kern, J.; Irrgang, K. -D.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 34
  • DOI: 10.1073/pnas.0505207102

Room temperature femtosecond X-ray diffraction of photosystem II microcrystals
journal, June 2012

  • Kern, J.; Alonso-Mori, R.; Hellmich, J.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 25, p. 9721-9726
  • DOI: 10.1073/pnas.1204598109

Nanoflow electrospinning serial femtosecond crystallography
journal, October 2012

  • Sierra, Raymond G.; Laksmono, Hartawan; Kern, Jan
  • Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 11, p. 1584-1587
  • DOI: 10.1107/s0907444912038152

COOPERATION OF CHARGES IN PHOTOSYNTHETIC O 2 EVOLUTION–I. A LINEAR FOUR STEP MECHANISM
journal, June 1970


Simultaneous Femtosecond X-ray Spectroscopy and Diffraction of Photosystem II at Room Temperature
journal, February 2013


Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein
journal, December 2014


Mix and Inject: Reaction Initiation by Diffusion for Time-Resolved Macromolecular Crystallography
journal, January 2013


Ultra-precise characterization of LCLS hard X-ray focusing mirrors by high resolution slope measuring deflectometry
journal, January 2012

  • Siewert, Frank; Buchheim, Jana; Boutet, Sébastien
  • Optics Express, Vol. 20, Issue 4
  • DOI: 10.1364/oe.20.004525

Works referencing / citing this record:

Structure of photosystem II and substrate binding at room temperature
journal, November 2016

  • Young, Iris D.; Ibrahim, Mohamed; Chatterjee, Ruchira
  • Nature, Vol. 540, Issue 7633
  • DOI: 10.1038/nature20161

Concentric-flow electrokinetic injector enables serial crystallography of ribosome and photosystem II
journal, November 2015

  • Sierra, Raymond G.; Gati, Cornelius; Laksmono, Hartawan
  • Nature Methods, Vol. 13, Issue 1
  • DOI: 10.1038/nmeth.3667

Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers
journal, February 2017

  • Fuller, Franklin D.; Gul, Sheraz; Chatterjee, Ruchira
  • Nature Methods, Vol. 14, Issue 4
  • DOI: 10.1038/nmeth.4195

Structures of the intermediates of Kok’s photosynthetic water oxidation clock
journal, November 2018


Supersaturation-controlled microcrystallization and visualization analysis for serial femtosecond crystallography
journal, February 2018


Assessment of the manganese cluster’s oxidation state via photoactivation of photosystem II microcrystals
journal, December 2019

  • Cheah, Mun Hon; Zhang, Miao; Shevela, Dmitry
  • Proceedings of the National Academy of Sciences, Vol. 117, Issue 1
  • DOI: 10.1073/pnas.1915879117

Successful sample preparation for serial crystallography experiments
journal, November 2019

  • Beale, John H.; Bolton, Rachel; Marshall, Stephen A.
  • Journal of Applied Crystallography, Vol. 52, Issue 6
  • DOI: 10.1107/s1600576719013517

Supersaturation-controlled microcrystallization and visualization analysis for serial femtosecond crystallography
text, January 2018

  • Lee, Dan Bi; Kim, Jong-Min; Seok, Jong Hyeon
  • Deutsches Elektronen-Synchrotron, DESY, Hamburg
  • DOI: 10.3204/pubdb-2018-01143

Supersaturation-controlled microcrystallization and visualization analysis for serial femtosecond crystallography
text, January 2018

  • Lee, Dan Bi; Kim, Jong-Min; Seok, Jong Hyeon
  • Deutsches Elektronen-Synchrotron, DESY, Hamburg
  • DOI: 10.3204/pubdb-2018-01143