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Title: Soft X-Ray Diffraction Microscopy of a Frozen Hydrated Yeast Cell

Abstract

We report the first image of an intact, frozen hydrated eukaryotic cell using x-ray diffraction microscopy, or coherent x-ray diffraction imaging. By plunge freezing the specimen in liquid ethane and maintaining it below -170 °C, artifacts due to dehydration, ice crystallization, and radiation damage are greatly reduced. In this example, coherent diffraction data using 520 eV x rays were recorded and reconstructed to reveal a budding yeast cell at a resolution better than 25 nm. This demonstration represents an important step towards high resolution imaging of cells in their natural, hydrated state, without limitations imposed by x-ray optics.

Authors:
 [1];  [1];  [1];  [1];  [2];  [1];  [3];  [2];  [1];  [1];  [1];  [1]
  1. Stony Brook Univ., NY (United States) Dept. of Physics and Astronomy
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  3. Stony Brook Univ., NY (United States) Dept. of Biochemistry and Cell Biology
Publication Date:
Research Org.:
Stony Brook Univ., NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1164142
Grant/Contract Number:  
FG02-04ER46128
Resource Type:
Accepted Manuscript
Journal Name:
Physical Review Letters
Additional Journal Information:
Journal Volume: 103; Journal Issue: 19; Journal ID: ISSN 0031-9007
Publisher:
American Physical Society (APS)
Country of Publication:
United States
Language:
English
Subject:
36 MATERIALS SCIENCE; 77 NANOSCIENCE AND NANOTECHNOLOGY

Citation Formats

Huang, Xiaojing, Nelson, Johanna, Kirz, Janos, Lima, Enju, Marchesini, Stefano, Miao, Huijie, Neiman, Aaron M., Shapiro, David, Steinbrener, Jan, Stewart, Andrew, Turner, Joshua J., and Jacobsen, Chris. Soft X-Ray Diffraction Microscopy of a Frozen Hydrated Yeast Cell. United States: N. p., 2009. Web. doi:10.1103/PhysRevLett.103.198101.
Huang, Xiaojing, Nelson, Johanna, Kirz, Janos, Lima, Enju, Marchesini, Stefano, Miao, Huijie, Neiman, Aaron M., Shapiro, David, Steinbrener, Jan, Stewart, Andrew, Turner, Joshua J., & Jacobsen, Chris. Soft X-Ray Diffraction Microscopy of a Frozen Hydrated Yeast Cell. United States. https://doi.org/10.1103/PhysRevLett.103.198101
Huang, Xiaojing, Nelson, Johanna, Kirz, Janos, Lima, Enju, Marchesini, Stefano, Miao, Huijie, Neiman, Aaron M., Shapiro, David, Steinbrener, Jan, Stewart, Andrew, Turner, Joshua J., and Jacobsen, Chris. Sun . "Soft X-Ray Diffraction Microscopy of a Frozen Hydrated Yeast Cell". United States. https://doi.org/10.1103/PhysRevLett.103.198101. https://www.osti.gov/servlets/purl/1164142.
@article{osti_1164142,
title = {Soft X-Ray Diffraction Microscopy of a Frozen Hydrated Yeast Cell},
author = {Huang, Xiaojing and Nelson, Johanna and Kirz, Janos and Lima, Enju and Marchesini, Stefano and Miao, Huijie and Neiman, Aaron M. and Shapiro, David and Steinbrener, Jan and Stewart, Andrew and Turner, Joshua J. and Jacobsen, Chris},
abstractNote = {We report the first image of an intact, frozen hydrated eukaryotic cell using x-ray diffraction microscopy, or coherent x-ray diffraction imaging. By plunge freezing the specimen in liquid ethane and maintaining it below -170 °C, artifacts due to dehydration, ice crystallization, and radiation damage are greatly reduced. In this example, coherent diffraction data using 520 eV x rays were recorded and reconstructed to reveal a budding yeast cell at a resolution better than 25 nm. This demonstration represents an important step towards high resolution imaging of cells in their natural, hydrated state, without limitations imposed by x-ray optics.},
doi = {10.1103/PhysRevLett.103.198101},
journal = {Physical Review Letters},
number = 19,
volume = 103,
place = {United States},
year = {Sun Nov 01 00:00:00 EDT 2009},
month = {Sun Nov 01 00:00:00 EDT 2009}
}

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Works referenced in this record:

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


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


Soft X-ray microscopes and their biological applications
journal, February 1995

  • Kirz, Janos; Jacobsen, Chris; Howells, Malcolm
  • Quarterly Reviews of Biophysics, Vol. 28, Issue 1
  • DOI: 10.1017/S0033583500003139

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


Microholography of Living Organisms
journal, October 1982


Feasibility of imaging living cells at subnanometer resolutions by ultrafast X-ray diffraction
journal, November 2008

  • Bergh, Magnus; Huldt, Gösta; Tîmneanu, Nicusor
  • Quarterly Reviews of Biophysics, Vol. 41, Issue 3-4
  • DOI: 10.1017/S003358350800471X

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 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

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

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


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

Phase zone plates for x rays and the extreme uv
journal, January 1974


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


Phase retrieval from the magnitude of the Fourier transforms of nonperiodic objects
journal, January 1998

  • Miao, J.; Sayre, D.; Chapman, H. N.
  • Journal of the Optical Society of America A, Vol. 15, Issue 6
  • DOI: 10.1364/JOSAA.15.001662

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

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

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

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


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

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


Electron Diffraction of Frozen, Hydrated Protein Crystals
journal, December 1974


Electron microscopy of frozen hydrated biological specimens
journal, June 1976


High Voltage Cryomicroscopy of Human Blood Platelets
journal, January 1993

  • O'Toole, Eileen; Wray, George; Kremer, James
  • Journal of Structural Biology, Vol. 110, Issue 1
  • DOI: 10.1006/jsbi.1993.1004

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


Multiscale imaging of neurons grown in culture: From light microscopy to cryo-electron tomography
journal, November 2007

  • Lučić, Vladan; Kossel, Albrecht H.; Yang, Ting
  • Journal of Structural Biology, Vol. 160, Issue 2
  • DOI: 10.1016/j.jsb.2007.08.014

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

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

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


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


Phase retrieval by iterated projections
journal, January 2003


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

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

Cryo diffraction microscopy: Ice conditions and finite supports
journal, September 2009


Does contamination buildup limit throughput for automated cryoEM?
journal, June 2006

  • Cheng, Anchi; Fellmann, Denis; Pulokas, James
  • Journal of Structural Biology, Vol. 154, Issue 3
  • DOI: 10.1016/j.jsb.2006.03.005

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

Femtosecond diffractive imaging with a soft-X-ray free-electron laser
journal, November 2006

  • Chapman, Henry N.; Barty, Anton; Bogan, Michael J.
  • Nature Physics, Vol. 2, Issue 12
  • DOI: 10.1038/nphys461

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


Phase retrieval by iterated projections
preprint, January 2001


Works referencing / citing this record:

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


Humidity-controlled preparation of frozen-hydrated biological samples for cryogenic coherent x-ray diffraction microscopy
journal, May 2012

  • Takayama, Yuki; Nakasako, Masayoshi
  • Review of Scientific Instruments, Vol. 83, Issue 5
  • DOI: 10.1063/1.4718359

KOTOBUKI-1 apparatus for cryogenic coherent X-ray diffraction imaging
journal, September 2013

  • Nakasako, Masayoshi; Takayama, Yuki; Oroguchi, Tomotaka
  • Review of Scientific Instruments, Vol. 84, Issue 9
  • DOI: 10.1063/1.4822123

X-ray ptychography on low-dimensional hard-condensed matter materials
journal, March 2019

  • Shi, Xiaowen; Burdet, Nicolas; Chen, Bo
  • Applied Physics Reviews, Vol. 6, Issue 1
  • DOI: 10.1063/1.5045131

High-resolution x-ray diffraction microscopy of specifically labeled yeast cells
journal, April 2010

  • Nelson, J.; Huang, X.; Steinbrener, J.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 16
  • DOI: 10.1073/pnas.0910874107

Quantitative 3D imaging of whole, unstained cells by using X-ray diffraction microscopy
journal, June 2010

  • Jiang, H.; Song, C.; Chen, C. -C.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 25
  • DOI: 10.1073/pnas.1000156107

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

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

Coherent X-Ray Diffraction Imaging of Chloroplasts from Cyanidioschyzon merolae by Using X-Ray Free Electron Laser
journal, March 2015

  • Takayama, Yuki; Inui, Yayoi; Sekiguchi, Yuki
  • Plant and Cell Physiology, Vol. 56, Issue 7
  • DOI: 10.1093/pcp/pcv032

Three-dimensional structure determination protocol for noncrystalline biomolecules using x-ray free-electron laser diffraction imaging
journal, February 2013


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


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


Fresnel coherent diffraction tomography
journal, January 2010

  • Putkunz, C. T.; Pfeifer, M. A.; Peele, A. G.
  • Optics Express, Vol. 18, Issue 11
  • DOI: 10.1364/oe.18.011746

X-ray microscopy
journal, February 2017


X-ray microscopy
journal, July 1965