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

Xiaojing, Huang; Nelson, Johanna; Lima, Enju; Miao, Huijie; Steinbrener, Jan; Stewart, Andrew; Turner, Joshua J; Jacobsen, Chris; Kirz, Janos; Marchesini, Stefano; Shapiro, David; Neiman, Aaron M

doi:10.1103/PHYSREVLETT.103.198101

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

Journal Article · Fri Nov 06 04:00:00 EST 2009 · Physical Review Letters

DOI:https://doi.org/10.1103/PHYSREVLETT.103.198101· OSTI ID:21370816

Xiaojing, Huang; Nelson, Johanna; Lima, Enju; Miao, Huijie; Steinbrener, Jan; Stewart, Andrew; Turner, Joshua J; Jacobsen, Chris ^[1]; Kirz, Janos ^[1]; Marchesini, Stefano; Shapiro, David ^[2]; Neiman, Aaron M ^[3]

Department of Physics and Astronomy, Stony Brook University, Stony Brook, New York 11794-3800 (United States)
Advanced Light Source, Lawrence Berkeley National Laboratory, Berkeley, California 94720 (United States)
Department of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, New York 11794-5215 (United States)

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 deg. 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.

OSTI ID:: 21370816

Journal Information:: Physical Review Letters, Journal Name: Physical Review Letters Journal Issue: 19 Vol. 103; ISSN 0031-9007; ISSN PRLTAO

Country of Publication:: United States

Language:: English

References (46)

Signal-to-noise and radiation exposure considerations in conventional and diffraction x-ray microscopy Huang, Xiaojing; Miao, Huijie; Steinbrener, Jan Optics Express, Vol. 17, Issue 16 https://doi.org/10.1364/oe.17.013541	journal	January 2009
Diffractive imaging of nonperiodic materials with future coherent X-ray sources Shen, Qun; Bazarov, Ivan; Thibault, Pierre Journal of Synchrotron Radiation, Vol. 11, Issue 5 https://doi.org/10.1107/s0909049504016772	journal	August 2004
X-ray image reconstruction from a diffraction pattern alone Marchesini, S.; He, H.; Chapman, H. N. Physical Review B, Vol. 68, Issue 14 https://doi.org/10.1103/physrevb.68.140101	journal	October 2003
Zone-Doubling Technique to Produce Ultrahigh-Resolution X-Ray Optics Jefimovs, K.; Vila-Comamala, J.; Pilvi, T. Physical Review Letters, Vol. 99, Issue 26 https://doi.org/10.1103/physrevlett.99.264801	journal	December 2007
Multiscale imaging of neurons grown in culture: From light microscopy to cryo-electron tomography Lučić, Vladan; Kossel, Albrecht H.; Yang, Ting Journal of Structural Biology, Vol. 160, Issue 2 https://doi.org/10.1016/j.jsb.2007.08.014	journal	November 2007
Electron Diffraction of Frozen, Hydrated Protein Crystals Taylor, K. A.; Glaeser, R. M. Science, Vol. 186, Issue 4168 https://doi.org/10.1126/science.186.4168.1036	journal	December 1974
Energy filtered electron tomography of ice-embedded actin and vesicles Grimm, R.; Bärmann, M.; Häckl, W. Biophysical Journal, Vol. 72, Issue 1 https://doi.org/10.1016/s0006-3495(97)78689-2	journal	January 1997
Phase retrieval by iterated projections Elser, Veit arXiv https://doi.org/10.48550/arxiv.math/0111080	preprint	January 2001
Macromolecular Architecture in Eukaryotic Cells Visualized by Cryoelectron Tomography Medalia, O. Science, Vol. 298, Issue 5596 https://doi.org/10.1126/science.1076184	journal	November 2002
High-resolution X-ray imaging of Plasmodium falciparum -infected red blood cells Williams, Garth J.; Hanssen, Eric; Peele, Andrew G. Cytometry Part A, Vol. 73A, Issue 10 https://doi.org/10.1002/cyto.a.20616	journal	October 2008
Cryo X-ray microscopy with high spatial resolution in amplitude and phase contrast Schneider, Gerd Ultramicroscopy, Vol. 75, Issue 2 https://doi.org/10.1016/s0304-3991(98)00054-0	journal	November 1998
Microholography of Living Organisms Solem, J. C.; Baldwin, G. C. Science, Vol. 218, Issue 4569 https://doi.org/10.1126/science.218.4569.229	journal	October 1982
Soft X-ray microscopes and their biological applications Kirz, Janos; Jacobsen, Chris; Howells, Malcolm Quarterly Reviews of Biophysics, Vol. 28, Issue 1 https://doi.org/10.1017/s0033583500003139	journal	February 1995
Femtosecond diffractive imaging with a soft-X-ray free-electron laser Chapman, Henry N.; Barty, Anton; Bogan, Michael J. Nature Physics, Vol. 2, Issue 12 https://doi.org/10.1038/nphys461	journal	November 2006
Spiegelsysteme streifenden Einfalls als abbildende Optiken für Röntgenstrahlen Wolter, Hans Annalen der Physik, Vol. 445, Issue 1-2 https://doi.org/10.1002/andp.19524450108	journal	January 1952
Imaging whole Escherichia coli bacteria by using single-particle x-ray diffraction Miao, J.; Hodgson, K. O.; Ishikawa, T. Proceedings of the National Academy of Sciences, Vol. 100, Issue 1 https://doi.org/10.1073/pnas.232691299	journal	December 2002
Phase recovery and lensless imaging by iterative methods in optical, X-ray and electron diffraction 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 https://doi.org/10.1098/rsta.2001.0972	journal	May 2002
X-ray Tomography Generates 3-D Reconstructions of the Yeast, Saccharomyces cerevisiae , at 60-nm Resolution Larabell, Carolyn A.; Le Gros, Mark A. Molecular Biology of the Cell, Vol. 15, Issue 3 https://doi.org/10.1091/mbc.e03-07-0522	journal	March 2004
Phase zone plates for x rays and the extreme uv Kirz, Janos Journal of the Optical Society of America, Vol. 64, Issue 3 https://doi.org/10.1364/josa.64.000301	journal	January 1974
An assessment of the resolution limitation due to radiation-damage in x-ray diffraction microscopy Howells, M. R.; Beetz, T.; Chapman, H. N. arXiv https://doi.org/10.48550/arxiv.physics/0502059	text	January 2005
Computed tomography of cryogenic biological specimens based on X-ray microscopic images Weiß, D.; Schneider, G.; Niemann, B. Ultramicroscopy, Vol. 84, Issue 3-4 https://doi.org/10.1016/s0304-3991(00)00034-6	journal	August 2000
Phase retrieval from the magnitude of the Fourier transforms of nonperiodic objects Miao, J.; Sayre, D.; Chapman, H. N. Journal of the Optical Society of America A, Vol. 15, Issue 6 https://doi.org/10.1364/josaa.15.001662	journal	January 1998
Does contamination buildup limit throughput for automated cryoEM? Cheng, Anchi; Fellmann, Denis; Pulokas, James Journal of Structural Biology, Vol. 154, Issue 3 https://doi.org/10.1016/j.jsb.2006.03.005	journal	June 2006
Electron microscopy of frozen hydrated biological specimens Taylor, Kenneth A.; Glaeser, Robert M. Journal of Ultrastructure Research, Vol. 55, Issue 3 https://doi.org/10.1016/s0022-5320(76)80099-8	journal	June 1976
Soft X-ray microscopy at a spatial resolution better than 15 nm Chao, Weilun; Harteneck, Bruce D.; Liddle, J. Alexander Nature, Vol. 435, Issue 7046 https://doi.org/10.1038/nature03719	journal	June 2005
Quantitative 3-D imaging of eukaryotic cells using soft X-ray tomography Parkinson, Dilworth Y.; McDermott, Gerry; Etkin, Laurence D. Journal of Structural Biology, Vol. 162, Issue 3 https://doi.org/10.1016/j.jsb.2008.02.003	journal	June 2008
Focusing of hard x-rays to 16 nanometers with a multilayer Laue lens Kang, Hyon Chol; Yan, Hanfei; Winarski, Robert P. Applied Physics Letters, Vol. 92, Issue 22 https://doi.org/10.1063/1.2912503	journal	June 2008
Soft X-ray microscopy with a cryo scanning transmission X-ray microscope: I. Instrumentation, imaging and spectroscopy No authors listed Journal of Microscopy, Vol. 197, Issue 1 https://doi.org/10.1046/j.1365-2818.2000.00630.x	journal	January 2000
Feasibility of imaging living cells at subnanometer resolutions by ultrafast X-ray diffraction Bergh, Magnus; Huldt, Gösta; Tîmneanu, Nicusor Quarterly Reviews of Biophysics, Vol. 41, Issue 3-4 https://doi.org/10.1017/s003358350800471x	journal	November 2008
Potential operating region for ultrasoft x-ray microscopy of biological materials Sayre, D.; Kirz, J.; Feder, R. Science, Vol. 196, Issue 4296 https://doi.org/10.1126/science.867033	journal	June 1977
Three-Dimensional Visualization of a Human Chromosome Using Coherent X-Ray Diffraction Nishino, Yoshinori; Takahashi, Yukio; Imamoto, Naoko Physical Review Letters, Vol. 102, Issue 1 https://doi.org/10.1103/physrevlett.102.018101	journal	January 2009
Phase retrieval by iterated projections Elser, Veit Journal of the Optical Society of America A, Vol. 20, Issue 1 https://doi.org/10.1364/josaa.20.000040	journal	January 2003
High Resolution 3D X-Ray Diffraction Microscopy Miao, Jianwei; Ishikawa, Tetsuya; Johnson, Bart Physical Review Letters, Vol. 89, Issue 8 https://doi.org/10.1103/physrevlett.89.088303	journal	August 2002
Computed Tomography of Cryogenic Cells Schneider, G.; Anderson, E.; Vogt, S. Surface Review and Letters, Vol. 09, Issue 01 https://doi.org/10.1142/s0218625x02001914	journal	February 2002
High Voltage Cryomicroscopy of Human Blood Platelets O'Toole, Eileen; Wray, George; Kremer, James Journal of Structural Biology, Vol. 110, Issue 1 https://doi.org/10.1006/jsbi.1993.1004	journal	January 1993
Extending the methodology of X-ray crystallography to allow imaging of micrometre-sized non-crystalline specimens Miao, Jianwei; Charalambous, Pambos; Kirz, Janos Nature, Vol. 400, Issue 6742 https://doi.org/10.1038/22498	journal	July 1999
Soft X-ray microscopy with a cryo scanning transmission X-ray microscope: II. Tomography No authors listed Journal of Microscopy, Vol. 197, Issue 1 https://doi.org/10.1046/j.1365-2818.2000.00629.x	journal	January 2000
Reconstruction of a yeast cell from X-ray diffraction data Thibault, Pierre; Elser, Veit; Jacobsen, Chris Acta Crystallographica Section A Foundations of Crystallography, Vol. 62, Issue 4 https://doi.org/10.1107/s0108767306016515	journal	June 2006
Biological imaging by soft x-ray diffraction microscopy Shapiro, D.; Thibault, P.; Beetz, T. Proceedings of the National Academy of Sciences, Vol. 102, Issue 43 https://doi.org/10.1073/pnas.0503305102	journal	October 2005
Reconstruction of an object from the modulus of its Fourier transform Fienup, J. R. Optics Letters, Vol. 3, Issue 1, p. 27-29 https://doi.org/10.1364/ol.3.000027	journal	January 1978
High-resolution ab initio three-dimensional x-ray diffraction microscopy Chapman, Henry N.; Barty, Anton; Marchesini, Stefano Journal of the Optical Society of America A, Vol. 23, Issue 5 https://doi.org/10.1364/josaa.23.001179	journal	January 2006
Comparison of the Saccharomyces cerevisiae G1 cyclins: Cln3 may be an upstream activator of Cln1, Cln2 and other cyclins. Tyers, M.; Tokiwa, G.; Futcher, B. The EMBO Journal, Vol. 12, Issue 5 https://doi.org/10.1002/j.1460-2075.1993.tb05845.x	journal	May 1993
Cryo diffraction microscopy: Ice conditions and finite supports Miao, H.; Downing, K.; Huang, X. Journal of Physics: Conference Series, Vol. 186 https://doi.org/10.1088/1742-6596/186/1/012055	journal	September 2009
Quantitative Imaging of Single, Unstained Viruses with Coherent X Rays Song, Changyong; Jiang, Huaidong; Mancuso, Adrian Physical Review Letters, Vol. 101, Issue 15 https://doi.org/10.1103/physrevlett.101.158101	journal	October 2008
An assessment of the resolution limitation due to radiation-damage in X-ray diffraction microscopy Howells, M. R.; Beetz, T.; Chapman, H. N. Journal of Electron Spectroscopy and Related Phenomena, Vol. 170, Issue 1-3 https://doi.org/10.1016/j.elspec.2008.10.008	journal	March 2009
Apparatus for X-ray diffraction microscopy and tomography of cryo specimens 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 https://doi.org/10.1016/j.nima.2004.12.040	journal	June 2005

Cited By (22)

Coherent X-Ray Diffraction Imaging of Chloroplasts from Cyanidioschyzon merolae by Using X-Ray Free Electron Laser Takayama, Yuki; Inui, Yayoi; Sekiguchi, Yuki Plant and Cell Physiology, Vol. 56, Issue 7 https://doi.org/10.1093/pcp/pcv032	journal	March 2015
X-ray microscopy Lider, V. V. Physics-Uspekhi, Vol. 60, Issue 2 https://doi.org/10.3367/ufne.2016.06.037830	journal	February 2017
X-ray Microscopy Jacobsen, Chris Cambridge University Press https://doi.org/10.1017/9781139924542	book	January 2019
High-resolution x-ray diffraction microscopy of specifically labeled yeast cells Nelson, J.; Huang, X.; Steinbrener, J. Proceedings of the National Academy of Sciences, Vol. 107, Issue 16 https://doi.org/10.1073/pnas.0910874107	journal	April 2010
Oversampling smoothness: an effective algorithm for phase retrieval of noisy diffraction intensities Rodriguez, Jose A.; Xu, Rui; Chen, Chien-Chun Journal of Applied Crystallography, Vol. 46, Issue 2 https://doi.org/10.1107/s0021889813002471	journal	February 2013
Fresnel coherent diffraction tomography Putkunz, C. T.; Pfeifer, M. A.; Peele, A. G. Optics Express, Vol. 18, Issue 11 https://doi.org/10.1364/oe.18.011746	journal	January 2010
Quantitative 3D imaging of whole, unstained cells by using X-ray diffraction microscopy Jiang, H.; Song, C.; Chen, C. -C. Proceedings of the National Academy of Sciences, Vol. 107, Issue 25 https://doi.org/10.1073/pnas.1000156107	journal	June 2010
Oversampling smoothness (OSS): an effective algorithm for phase retrieval of noisy diffraction intensities Rodriguez, Jose A.; Xu, Rui; Chen, Chien-Chun arXiv https://doi.org/10.48550/arxiv.1211.4519	text	January 2012
Three-dimensional double helical DNA structure directly revealed from its X-ray fiber diffraction pattern by iterative phase retrieval Latychevskaia, Tatiana; Fink, Hans-Werner arXiv https://doi.org/10.48550/arxiv.1811.04459	text	January 2018
Three-dimensional double helical DNA structure directly revealed from its X-ray fiber diffraction pattern by iterative phase retrieval Latychevskaia, Tatiana; Fink, Hans-Werner Optics Express, Vol. 26, Issue 23 https://doi.org/10.1364/oe.26.030991	journal	January 2018
Simultaneous cryo X-ray ptychographic and fluorescence microscopy of green algae Deng, Junjing; Vine, David J.; Chen, Si Proceedings of the National Academy of Sciences, Vol. 112, Issue 8 https://doi.org/10.1073/pnas.1413003112	journal	February 2015
Transmission and emission x-ray microscopy: operation modes, contrast mechanisms and applications Kaulich, Burkhard; Thibault, Pierre; Gianoncelli, Alessandra Journal of Physics: Condensed Matter, Vol. 23, Issue 8 https://doi.org/10.1088/0953-8984/23/8/083002	journal	February 2011
Imaging Fully Hydrated Whole Cells by Coherent X-Ray Diffraction Microscopy Nam, Daewoong; Park, Jaehyun; Gallagher-Jones, Marcus Physical Review Letters, Vol. 110, Issue 9 https://doi.org/10.1103/physrevlett.110.098103	journal	February 2013
X-ray ptychography on low-dimensional hard-condensed matter materials Shi, Xiaowen; Burdet, Nicolas; Chen, Bo Applied Physics Reviews, Vol. 6, Issue 1 https://doi.org/10.1063/1.5045131	journal	March 2019
Three-dimensional coherent X-ray diffractive imaging of whole frozen-hydrated cells Rodriguez, Jose A.; Xu, Rui; Chen, Chien-Chun IUCrJ, Vol. 2, Issue 5 https://doi.org/10.1107/s205225251501235x	journal	August 2015
Three-dimensional structure determination protocol for noncrystalline biomolecules using x-ray free-electron laser diffraction imaging Oroguchi, Tomotaka; Nakasako, Masayoshi Physical Review E, Vol. 87, Issue 2 https://doi.org/10.1103/physreve.87.022712	journal	February 2013
Imaging cell morphology and physiology using X-rays Weinhardt, Venera; Chen, Jian-Hua; Ekman, Axel Biochemical Society Transactions, Vol. 47, Issue 2 https://doi.org/10.1042/bst20180036	journal	April 2019
Humidity-controlled preparation of frozen-hydrated biological samples for cryogenic coherent x-ray diffraction microscopy Takayama, Yuki; Nakasako, Masayoshi Review of Scientific Instruments, Vol. 83, Issue 5 https://doi.org/10.1063/1.4718359	journal	May 2012
X-ray microscopy Cosslett, V. E. Reports on Progress in Physics, Vol. 28, Issue 1 https://doi.org/10.1088/0034-4885/28/1/311	journal	July 1965
Imaging live cell in micro-liquid enclosure by X-ray laser diffraction Kimura, Takashi; Joti, Yasumasa; Shibuya, Akemi Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4052	journal	January 2014
Coherent lensless X-ray imaging Chapman, Henry N.; Nugent, Keith A. Nature Photonics, Vol. 4, Issue 12 https://doi.org/10.1038/nphoton.2010.240	journal	November 2010
KOTOBUKI-1 apparatus for cryogenic coherent X-ray diffraction imaging Nakasako, Masayoshi; Takayama, Yuki; Oroguchi, Tomotaka Review of Scientific Instruments, Vol. 84, Issue 9 https://doi.org/10.1063/1.4822123	journal	September 2013

Similar Records

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

Journal Article · Sat Oct 31 20:00:00 EDT 2009 · Physical Review Letters · OSTI ID:1164142

High-resolution x-ray diffraction microscopy of specifically labeled yeast cells

Journal Article · Mon Apr 19 20:00:00 EDT 2010 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1164150

Cryogenic X-ray Diffraction Microscopy for Biological Samples

Journal Article · Fri Dec 30 23:00:00 EST 2011 · Physical Review Letters · OSTI ID:1041692

Related Subjects

60 APPLIED LIFE SCIENCES
ALKANES
COHERENT SCATTERING
CRYSTALLIZATION
DEHYDRATION
DIFFRACTION
ELECTROMAGNETIC RADIATION
ENERGY RANGE
ETHANE
EUMYCOTA
EV RANGE
EV RANGE 100-1000
FREEZING
FUNGI
HYDROCARBONS
ICE
IONIZING RADIATIONS
MICROORGANISMS
MICROSCOPY
ORGANIC COMPOUNDS
PHASE TRANSFORMATIONS
PLANTS
RADIATION EFFECTS
RADIATIONS
SCATTERING
SOFT X RADIATION
X RADIATION
X-RAY DIFFRACTION
YEASTS

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

Citation Formats

References (46)

Cited By (22)

Similar Records

Related Subjects