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Title: 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:
 [1];  [1];  [1];  [2];  [2];  [2];  [3];  [1];  [4]
  1. Stony Brook Univ., Stony Brook, NY (United States)
  2. Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). Advanced Light Source
  3. Northwestern Univ., Evanston, IL (United States)
  4. 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}
}

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Works referenced in this record:

The history and future of X-ray microscopy
journal, September 2009


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
  • DOI: 10.1098/rsta.2001.0972

Three-Dimensional Visualization of a Human Chromosome Using Coherent X-Ray Diffraction
journal, January 2009


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
  • DOI: 10.1073/pnas.232691299

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
  • DOI: 10.1002/jcb.21047

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
  • DOI: 10.1364/OE.17.013541

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
  • DOI: 10.1038/22498

Compact water-window transmission X-ray microscopy
journal, March 2000


Coherent X-Ray Diffraction Imaging with Nanofocused Illumination
journal, August 2008


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
  • DOI: 10.1364/JOSAA.23.001179

Cryogenic X-Ray Diffraction Microscopy for Biological Samples
journal, November 2009


Soft X-Ray Diffraction Microscopy of a Frozen Hydrated Yeast Cell
journal, November 2009


High-Resolution Scanning X-ray Diffraction Microscopy
journal, July 2008


Factors affecting the chronic hepatotoxicity of pyrrolizidine alkaloids
journal, September 1971


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
  • DOI: 10.1063/1.2912503

Three-dimensional structure determination from a single view
journal, December 2009

  • Raines, Kevin S.; Salha, Sara; Sandberg, Richard L.
  • Nature, Vol. 463, Issue 7278
  • DOI: 10.1038/nature08705

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
  • DOI: 10.1109/photonics.2010.5698725

Phase retrieval by iterated projections
journal, January 2003


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
  • DOI: 10.1107/S0909049504016772

Nanoscale Imaging of Mineral Crystals inside Biological Composite Materials Using X-Ray Diffraction Microscopy
journal, January 2008


X-ray image reconstruction from a diffraction pattern alone
journal, October 2003


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
  • DOI: 10.1073/pnas.0503305102

Zone-Doubling Technique to Produce Ultrahigh-Resolution X-Ray Optics
journal, December 2007


Biological applications of X-ray fluorescence microscopy: exploring the subcellular topography and speciation of transition metals
journal, April 2007


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
  • DOI: 10.1109/cleoe-eqec.2009.5191624

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
  • DOI: 10.1091/mbc.E03-07-0522

Far-Field Optical Nanoscopy
book, November 2009


Systematic Identification of Pathways That Couple Cell Growth and Division in Yeast
journal, June 2002


Quantitative Imaging of Single, Unstained Viruses with Coherent X Rays
journal, October 2008


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
  • DOI: 10.1016/j.elspec.2008.10.008

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
  • DOI: 10.1016/j.nima.2004.12.040

Far-Field Optical Nanoscopy
journal, May 2007


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
  • DOI: 10.1016/j.jsb.2008.02.003

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
  • DOI: 10.1038/nature03719

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
  • DOI: 10.1002/cyto.a.20616

Potential operating region for ultrasoft x-ray microscopy of biological materials
journal, June 1977


Reconstruction of an object from the modulus of its Fourier transform
journal, January 1978


Reinvestigation of hydrazinium tetrafluoroborate
journal, November 2006

  • Kowalewski, Markus; Mayer, Peter; Schulz, Axel
  • Acta Crystallographica Section E Structure Reports Online, Vol. 62, Issue 12
  • DOI: 10.1107/S1600536806045922

Hard-X-Ray Lensless Imaging of Extended Objects
journal, January 2007


High Resolution 3D X-Ray Diffraction Microscopy
journal, August 2002


Macromolecular Architecture in Eukaryotic Cells Visualized by Cryoelectron Tomography
journal, November 2002


Energy filtered electron tomography of ice-embedded actin and vesicles
journal, January 1997


Computed tomography of cryogenic biological specimens based on X-ray microscopic images
journal, August 2000


Computed Tomography of Cryogenic Cells
journal, February 2002


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
  • DOI: 10.1524/zkri.2007.222.11.650

Cryo X-ray microscopy with high spatial resolution in amplitude and phase contrast
journal, November 1998


Spiegelsysteme streifenden Einfalls als abbildende Optiken für Röntgenstrahlen
journal, January 1952


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
  • DOI: 10.1107/S0108767306016515

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
  • DOI: 10.1128/jb.105.1.1-5.1971

Principles of Optics
book, January 1999


Three-dimensional structure determination from a single view
text, January 2009


Phase retrieval by iterated projections
preprint, January 2001


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
  • DOI: 10.1117/12.2238496

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
  • DOI: 10.1038/ncomms4052

Coherent lensless X-ray imaging
journal, November 2010


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
  • DOI: 10.1038/ncomms6704

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
  • DOI: 10.3204/pubdb-2016-05139

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
  • DOI: 10.1017/s1431927612013827

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
  • DOI: 10.1107/s1600577520002702

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
  • DOI: 10.1073/pnas.1413003112

Three-dimensional coherent diffractive imaging on non-periodic specimens at the ESRF beamline ID10
journal, March 2014


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
  • DOI: 10.1038/srep09973

Imaging Fully Hydrated Whole Cells by Coherent X-Ray Diffraction Microscopy
journal, February 2013


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
  • DOI: 10.1073/pnas.1720785116

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
  • DOI: 10.1088/0953-8984/23/8/083002

Three-dimensional coherent X-ray diffractive imaging of whole frozen-hydrated cells
journal, August 2015


X-ray lasers for structural and dynamic biology
journal, September 2012


Beyond crystallography: Diffractive imaging using coherent x-ray light sources
journal, April 2015


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
  • DOI: 10.1101/622100

X-ray microscopy
journal, July 1965


Tabletop Nanometer Extreme Ultraviolet Imaging in an Extended Reflection Mode using Coherent Fresnel Ptychography
preprint, January 2013


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
  • DOI: 10.1038/ncomms4052

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
  • DOI: 10.1038/s41598-017-04784-5

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
  • DOI: 10.1038/srep09973

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
  • DOI: 10.1038/srep30694

In situ coherent diffractive imaging
text, January 2017


Free log-likelihood as an unbiased metric for coherent diffraction imaging
text, January 2019