High-resolution x-ray diffraction microscopy of specifically labeled yeast cells
Abstract
X-ray diffraction microscopy complements other x-ray microscopy methods by being free of lens-imposed radiation dose and resolution limits, and it allows for high-resolution imaging of biological specimens too thick to be viewed by electron microscopy. We report here the highest resolution (11-13 nm) x-ray diffraction micrograph of biological specimens, and a demonstration of molecular-specific gold labeling at different depths within cells via through-focus propagation of the reconstructed wavefield. The lectin concanavalin A conjugated to colloidal gold particles was used to label the α-mannan sugar in the cell wall of the yeast Saccharomyces cerevisiae. Cells were plunge-frozen in liquid ethane and freeze-dried, after which they were imaged whole using x-ray diffraction microscopy at 750 eV photon energy.
- Authors:
-
- Stony Brook Univ., Stony Brook, NY (United States)
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Advanced Light Source
- Northwestern Univ., Evanston, IL (United States)
- Stony Brook Univ., Stony Brook, NY (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Advanced Light Source; Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source
- Publication Date:
- Research Org.:
- Stony Brook Univ., NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1164150
- Grant/Contract Number:
- FG02-04ER46128
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 107; Journal Issue: 16; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 36 MATERIALS SCIENCE; 77 NANOSCIENCE AND NANOTECHNOLOGY
Citation Formats
Nelson, Johanna, Huang, Xiaojing, Steinbrener, Jan, Shapiro, David, Kirz, Janos, Marchesini, Stephano, Neiman, Aaron M., Turner, Joshua J., and Jacobsen, Chris. High-resolution x-ray diffraction microscopy of specifically labeled yeast cells. United States: N. p., 2010.
Web. doi:10.1073/pnas.0910874107.
Nelson, Johanna, Huang, Xiaojing, Steinbrener, Jan, Shapiro, David, Kirz, Janos, Marchesini, Stephano, Neiman, Aaron M., Turner, Joshua J., & Jacobsen, Chris. High-resolution x-ray diffraction microscopy of specifically labeled yeast cells. United States. https://doi.org/10.1073/pnas.0910874107
Nelson, Johanna, Huang, Xiaojing, Steinbrener, Jan, Shapiro, David, Kirz, Janos, Marchesini, Stephano, Neiman, Aaron M., Turner, Joshua J., and Jacobsen, Chris. Tue .
"High-resolution x-ray diffraction microscopy of specifically labeled yeast cells". United States. https://doi.org/10.1073/pnas.0910874107. https://www.osti.gov/servlets/purl/1164150.
@article{osti_1164150,
title = {High-resolution x-ray diffraction microscopy of specifically labeled yeast cells},
author = {Nelson, Johanna and Huang, Xiaojing and Steinbrener, Jan and Shapiro, David and Kirz, Janos and Marchesini, Stephano and Neiman, Aaron M. and Turner, Joshua J. and Jacobsen, Chris},
abstractNote = {X-ray diffraction microscopy complements other x-ray microscopy methods by being free of lens-imposed radiation dose and resolution limits, and it allows for high-resolution imaging of biological specimens too thick to be viewed by electron microscopy. We report here the highest resolution (11-13 nm) x-ray diffraction micrograph of biological specimens, and a demonstration of molecular-specific gold labeling at different depths within cells via through-focus propagation of the reconstructed wavefield. The lectin concanavalin A conjugated to colloidal gold particles was used to label the α-mannan sugar in the cell wall of the yeast Saccharomyces cerevisiae. Cells were plunge-frozen in liquid ethane and freeze-dried, after which they were imaged whole using x-ray diffraction microscopy at 750 eV photon energy.},
doi = {10.1073/pnas.0910874107},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 16,
volume = 107,
place = {United States},
year = {Tue Apr 20 00:00:00 EDT 2010},
month = {Tue Apr 20 00:00:00 EDT 2010}
}
Web of Science
Works referenced in this record:
The history and future of X-ray microscopy
journal, September 2009
- Kirz, J.; Jacobsen, C.
- Journal of Physics: Conference Series, Vol. 186
Phase recovery and lensless imaging by iterative methods in optical, X-ray and electron diffraction
journal, May 2002
- Spence, J. C. H.; Weierstall, U.; Howells, M.
- Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences, Vol. 360, Issue 1794
Three-Dimensional Visualization of a Human Chromosome Using Coherent X-Ray Diffraction
journal, January 2009
- Nishino, Yoshinori; Takahashi, Yukio; Imamoto, Naoko
- Physical Review Letters, Vol. 102, Issue 1
Imaging whole Escherichia coli bacteria by using single-particle x-ray diffraction
journal, December 2002
- Miao, J.; Hodgson, K. O.; Ishikawa, T.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 1
X-ray fluorescence microprobe imaging in biology and medicine
journal, January 2006
- Paunesku, Tatjana; Vogt, Stefan; Maser, Jörg
- Journal of Cellular Biochemistry, Vol. 99, Issue 6
Signal-to-noise and radiation exposure considerations in conventional and diffraction x-ray microscopy
journal, January 2009
- Huang, Xiaojing; Miao, Huijie; Steinbrener, Jan
- Optics Express, Vol. 17, Issue 16
Extending the methodology of X-ray crystallography to allow imaging of micrometre-sized non-crystalline specimens
journal, July 1999
- Miao, Jianwei; Charalambous, Pambos; Kirz, Janos
- Nature, Vol. 400, Issue 6742
Compact water-window transmission X-ray microscopy
journal, March 2000
- Berglund, M.; Rymell, L.; Peuker, M.
- Journal of Microscopy, Vol. 197, Issue 3, p. 268-273
Coherent X-Ray Diffraction Imaging with Nanofocused Illumination
journal, August 2008
- Schroer, C. G.; Boye, P.; Feldkamp, J. M.
- Physical Review Letters, Vol. 101, Issue 9
High-resolution ab initio three-dimensional x-ray diffraction microscopy
journal, January 2006
- Chapman, Henry N.; Barty, Anton; Marchesini, Stefano
- Journal of the Optical Society of America A, Vol. 23, Issue 5
Cryogenic X-Ray Diffraction Microscopy for Biological Samples
journal, November 2009
- Lima, Enju; Wiegart, Lutz; Pernot, Petra
- Physical Review Letters, Vol. 103, Issue 19
Soft X-Ray Diffraction Microscopy of a Frozen Hydrated Yeast Cell
journal, November 2009
- Huang, Xiaojing; Nelson, Johanna; Kirz, Janos
- Physical Review Letters, Vol. 103, Issue 19
High-Resolution Scanning X-ray Diffraction Microscopy
journal, July 2008
- Thibault, P.; Dierolf, M.; Menzel, A.
- Science, Vol. 321, Issue 5887
Factors affecting the chronic hepatotoxicity of pyrrolizidine alkaloids
journal, September 1971
- Jago, Marjorie V.
- The Journal of Pathology, Vol. 105, Issue 1
Focusing of hard x-rays to 16 nanometers with a multilayer Laue lens
journal, June 2008
- Kang, Hyon Chol; Yan, Hanfei; Winarski, Robert P.
- Applied Physics Letters, Vol. 92, Issue 22
Three-dimensional structure determination from a single view
journal, December 2009
- Raines, Kevin S.; Salha, Sara; Sandberg, Richard L.
- Nature, Vol. 463, Issue 7278
Far-field optical nanoscopy
conference, November 2010
- Hell, Stefan W.
- 2010 23rd Annual Meeting of the IEEE Photonics Society (Formerly LEOS Annual Meeting), 2010 IEEE Photinic Society's 23rd Annual Meeting
Phase retrieval by iterated projections
journal, January 2003
- Elser, Veit
- Journal of the Optical Society of America A, Vol. 20, Issue 1
Diffractive imaging of nonperiodic materials with future coherent X-ray sources
journal, August 2004
- Shen, Qun; Bazarov, Ivan; Thibault, Pierre
- Journal of Synchrotron Radiation, Vol. 11, Issue 5
Nanoscale Imaging of Mineral Crystals inside Biological Composite Materials Using X-Ray Diffraction Microscopy
journal, January 2008
- Jiang, Huaidong; Ramunno-Johnson, Damien; Song, Changyong
- Physical Review Letters, Vol. 100, Issue 3
X-ray image reconstruction from a diffraction pattern alone
journal, October 2003
- Marchesini, S.; He, H.; Chapman, H. N.
- Physical Review B, Vol. 68, Issue 14
Biological imaging by soft x-ray diffraction microscopy
journal, October 2005
- Shapiro, D.; Thibault, P.; Beetz, T.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 43
Zone-Doubling Technique to Produce Ultrahigh-Resolution X-Ray Optics
journal, December 2007
- Jefimovs, K.; Vila-Comamala, J.; Pilvi, T.
- Physical Review Letters, Vol. 99, Issue 26
Biological applications of X-ray fluorescence microscopy: exploring the subcellular topography and speciation of transition metals
journal, April 2007
- Fahrni, Christoph J.
- Current Opinion in Chemical Biology, Vol. 11, Issue 2
Far-field optical nanoscopy
conference, June 2009
- Hell, Stefan W.
- 11th European Quantum Electronics Conference (CLEO/EQEC), CLEO/Europe - EQEC 2009 - European Conference on Lasers and Electro-Optics and the European Quantum Electronics Conference
X-ray Tomography Generates 3-D Reconstructions of the Yeast, Saccharomyces cerevisiae , at 60-nm Resolution
journal, March 2004
- Larabell, Carolyn A.; Le Gros, Mark A.
- Molecular Biology of the Cell, Vol. 15, Issue 3
Far-Field Optical Nanoscopy
book, November 2009
- Hell, Stefan W.
- Single Molecule Spectroscopy in Chemistry, Physics and Biology
Soft X-ray microscopy with a cryo scanning transmission X-ray microscope: I. Instrumentation, imaging and spectroscopy
journal, January 2000
- Maser,
- Journal of Microscopy, Vol. 197, Issue 1
Systematic Identification of Pathways That Couple Cell Growth and Division in Yeast
journal, June 2002
- Jorgensen, P.
- Science, Vol. 297, Issue 5580
Quantitative Imaging of Single, Unstained Viruses with Coherent X Rays
journal, October 2008
- Song, Changyong; Jiang, Huaidong; Mancuso, Adrian
- Physical Review Letters, Vol. 101, Issue 15
An assessment of the resolution limitation due to radiation-damage in X-ray diffraction microscopy
journal, March 2009
- Howells, M. R.; Beetz, T.; Chapman, H. N.
- Journal of Electron Spectroscopy and Related Phenomena, Vol. 170, Issue 1-3
Apparatus for X-ray diffraction microscopy and tomography of cryo specimens
journal, June 2005
- Beetz, T.; Howells, M. R.; Jacobsen, C.
- Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment, Vol. 545, Issue 1-2
Quantitative 3-D imaging of eukaryotic cells using soft X-ray tomography
journal, June 2008
- Parkinson, Dilworth Y.; McDermott, Gerry; Etkin, Laurence D.
- Journal of Structural Biology, Vol. 162, Issue 3
Soft X-ray microscopy at a spatial resolution better than 15 nm
journal, June 2005
- Chao, Weilun; Harteneck, Bruce D.; Liddle, J. Alexander
- Nature, Vol. 435, Issue 7046
High-resolution X-ray imaging of Plasmodium falciparum -infected red blood cells
journal, October 2008
- Williams, Garth J.; Hanssen, Eric; Peele, Andrew G.
- Cytometry Part A, Vol. 73A, Issue 10
Potential operating region for ultrasoft x-ray microscopy of biological materials
journal, June 1977
- Sayre, D.; Kirz, J.; Feder, R.
- Science, Vol. 196, Issue 4296
Reconstruction of an object from the modulus of its Fourier transform
journal, January 1978
- Fienup, J. R.
- Optics Letters, Vol. 3, Issue 1, p. 27-29
Reinvestigation of hydrazinium tetrafluoroborate
journal, November 2006
- Kowalewski, Markus; Mayer, Peter; Schulz, Axel
- Acta Crystallographica Section E Structure Reports Online, Vol. 62, Issue 12
Hard-X-Ray Lensless Imaging of Extended Objects
journal, January 2007
- Rodenburg, J. M.; Hurst, A. C.; Cullis, A. G.
- Physical Review Letters, Vol. 98, Issue 3
High Resolution 3D X-Ray Diffraction Microscopy
journal, August 2002
- Miao, Jianwei; Ishikawa, Tetsuya; Johnson, Bart
- Physical Review Letters, Vol. 89, Issue 8
Macromolecular Architecture in Eukaryotic Cells Visualized by Cryoelectron Tomography
journal, November 2002
- Medalia, O.
- Science, Vol. 298, Issue 5596
Energy filtered electron tomography of ice-embedded actin and vesicles
journal, January 1997
- Grimm, R.; Bärmann, M.; Häckl, W.
- Biophysical Journal, Vol. 72, Issue 1
Computed tomography of cryogenic biological specimens based on X-ray microscopic images
journal, August 2000
- Weiß, D.; Schneider, G.; Niemann, B.
- Ultramicroscopy, Vol. 84, Issue 3-4
Soft X-ray microscopy with a cryo scanning transmission X-ray microscope: II. Tomography
journal, January 2000
- Wang,
- Journal of Microscopy, Vol. 197, Issue 1
Computed Tomography of Cryogenic Cells
journal, February 2002
- Schneider, G.; Anderson, E.; Vogt, S.
- Surface Review and Letters, Vol. 09, Issue 01
X-ray computed tomography in Zernike phase contrast mode at 8 keV with 50-nm resolution using Cu rotating anode X-ray source
journal, January 2007
- Tkachuk, Andrei; Duewer, Fred; Cui, Hongtao
- Zeitschrift für Kristallographie - Crystalline Materials, Vol. 222, Issue 11/2007
Cryo X-ray microscopy with high spatial resolution in amplitude and phase contrast
journal, November 1998
- Schneider, Gerd
- Ultramicroscopy, Vol. 75, Issue 2
Spiegelsysteme streifenden Einfalls als abbildende Optiken für Röntgenstrahlen
journal, January 1952
- Wolter, Hans
- Annalen der Physik, Vol. 445, Issue 1-2
Reconstruction of a yeast cell from X-ray diffraction data
journal, June 2006
- Thibault, Pierre; Elser, Veit; Jacobsen, Chris
- Acta Crystallographica Section A Foundations of Crystallography, Vol. 62, Issue 4
Specific Staining of Wall Mannan in Yeast Cells with Fluorescein-Conjugated Concanavalin A
journal, January 1971
- Tkacz, J. S.; Cybulska, E. Barbara; Lampen, J. O.
- Journal of Bacteriology, Vol. 105, Issue 1
Principles of Optics
book, January 1999
- Born, Max; Wolf, Emil; Bhatia, A. B.
- Cambridge University Press
Three-dimensional structure determination from a single view
text, January 2009
- Raines, Kevin S.; Salha, Sara; Sandberg, Richard L.
- arXiv
An assessment of the resolution limitation due to radiation-damage in x-ray diffraction microscopy
text, January 2005
- Howells, M. R.; Beetz, T.; Chapman, H. N.
- arXiv
Works referencing / citing this record:
Phase-contrast tomography of neuronal tissues: from laboratory- to high resolution synchrotron CT
conference, October 2016
- Töpperwien, Mareike; Krenkel, Martin; Müller, Kristin
- SPIE Optical Engineering + Applications, SPIE Proceedings
Imaging live cell in micro-liquid enclosure by X-ray laser diffraction
journal, January 2014
- Kimura, Takashi; Joti, Yasumasa; Shibuya, Akemi
- Nature Communications, Vol. 5, Issue 1
Coherent lensless X-ray imaging
journal, November 2010
- Chapman, Henry N.; Nugent, Keith A.
- Nature Photonics, Vol. 4, Issue 12
Imaging single cells in a beam of live cyanobacteria with an X-ray laser
journal, February 2015
- van der Schot, Gijs; Svenda, Martin; Maia, Filipe R. N. C.
- Nature Communications, Vol. 6, Issue 1
Phase-contrast tomography of neuronal tissues: from laboratory- to high resolution synchrotron CT
text, January 2016
- Töpperwien, Mareike; Krenkel, Martin; Müller, Kristin
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Laboratory-Based Cryogenic Soft X-Ray Tomography with Correlative Cryo-Light and Electron Microscopy
journal, January 2013
- Carlson, David B.; Gelb, Jeff; Palshin, Vadim
- Microscopy and Microanalysis, Vol. 19, Issue 1
Identification of Ca-rich dense granules in human platelets using scanning transmission X-ray microscopy
journal, March 2020
- Trinh, Tung X.; Kwon, Sook Jin; Gerelkhuu, Zayakhuu
- Journal of Synchrotron Radiation, Vol. 27, Issue 3
Simultaneous cryo X-ray ptychographic and fluorescence microscopy of green algae
journal, February 2015
- Deng, Junjing; Vine, David J.; Chen, Si
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 8
Three-dimensional coherent diffractive imaging on non-periodic specimens at the ESRF beamline ID10
journal, March 2014
- Chushkin, Y.; Zontone, F.; Lima, E.
- Journal of Synchrotron Radiation, Vol. 21, Issue 3
Phase-contrast zoom tomography reveals precise locations of macrophages in mouse lungs
journal, May 2015
- Krenkel, Martin; Markus, Andrea; Bartels, Matthias
- Scientific Reports, Vol. 5, Issue 1
Imaging Fully Hydrated Whole Cells by Coherent X-Ray Diffraction Microscopy
journal, February 2013
- Nam, Daewoong; Park, Jaehyun; Gallagher-Jones, Marcus
- Physical Review Letters, Vol. 110, Issue 9
Three-dimensional optical trapping and orientation of microparticles for coherent X-ray diffraction imaging
journal, February 2019
- Gao, Yuan; Harder, Ross; Southworth, Stephen H.
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 10
Transmission and emission x-ray microscopy: operation modes, contrast mechanisms and applications
journal, February 2011
- Kaulich, Burkhard; Thibault, Pierre; Gianoncelli, Alessandra
- Journal of Physics: Condensed Matter, Vol. 23, Issue 8
Three-dimensional coherent X-ray diffractive imaging of whole frozen-hydrated cells
journal, August 2015
- Rodriguez, Jose A.; Xu, Rui; Chen, Chien-Chun
- IUCrJ, Vol. 2, Issue 5
X-ray lasers for structural and dynamic biology
journal, September 2012
- Spence, J. C. H.; Weierstall, U.; Chapman, H. N.
- Reports on Progress in Physics, Vol. 75, Issue 10
Beyond crystallography: Diffractive imaging using coherent x-ray light sources
journal, April 2015
- Miao, J.; Ishikawa, T.; Robinson, I. K.
- Science, Vol. 348, Issue 6234
Identification of Ca-rich dense granules in human platelets using scanning transmission X-ray microscopy
posted_content, January 2019
- Trinh, Tung X.; Kwon, Sook Jin; Gerelkhuu, Zayakhuu
- Journal of Synchrotron Radiation
X-ray microscopy
journal, July 1965
- Cosslett, V. E.
- Reports on Progress in Physics, Vol. 28, Issue 1
Oversampling smoothness (OSS): an effective algorithm for phase retrieval of noisy diffraction intensities
text, January 2012
- Rodriguez, Jose A.; Xu, Rui; Chen, Chien-Chun
- arXiv
Tabletop Nanometer Extreme Ultraviolet Imaging in an Extended Reflection Mode using Coherent Fresnel Ptychography
preprint, January 2013
- Seaberg, Matthew D.; Zhang, Bosheng; Gardner, Dennis F.
- arXiv
Three-dimensional double helical DNA structure directly revealed from its X-ray fiber diffraction pattern by iterative phase retrieval
text, January 2018
- Latychevskaia, Tatiana; Fink, Hans-Werner
- arXiv
Imaging live cell in micro-liquid enclosure by X-ray laser diffraction
journal, January 2014
- Kimura, Takashi; Joti, Yasumasa; Shibuya, Akemi
- Nature Communications, Vol. 5, Issue 1
Correlative cellular ptychography with functionalized nanoparticles at the Fe L-edge
journal, July 2017
- Gallagher-Jones, Marcus; Dias, Carlos Sato Baraldi; Pryor, Alan
- Scientific Reports, Vol. 7, Issue 1
Phase-contrast zoom tomography reveals precise locations of macrophages in mouse lungs
journal, May 2015
- Krenkel, Martin; Markus, Andrea; Bartels, Matthias
- Scientific Reports, Vol. 5, Issue 1
Three-dimensional Reconstruction of the Microstructure of Human Acellular Nerve Allograft
journal, August 2016
- Zhu, Shuang; Zhu, Qingtang; Liu, Xiaolin
- Scientific Reports, Vol. 6, Issue 1
In situ coherent diffractive imaging
text, January 2017
- Lo, Yuan Hung; Zhao, Lingrong; Gallagher-Jones, Marcus
- arXiv
Free log-likelihood as an unbiased metric for coherent diffraction imaging
text, January 2019
- Favre-Nicolin, Vincent; Leake, Steven; Chushkin, Yuriy
- arXiv