Abstract

X-ray imaging techniques have proven invaluable to study biological systems at high resolution due to the penetration power and short wavelength of this radiation. In practice, the resolution and sensitivity of current X-ray imaging techniques are not limited by the performance of optics or image-recovery methods but by radiation damage. We propose the use of Compton (inelastic) X-ray scattering for high-resolution cellular imaging and provide a study of a scanning microscope geometry that requires a dose to achieve a given resolution that is three orders of magnitude lower than for coherent (elastic) scattering. We find that the dose per imaging signal is minimized at a photon energy of 64 keV. This corresponds to a short enough wavelength (0.02 nm) to provide nanometer transverse resolution and micrometer depth of field for tomographic imaging of whole cells. The microscope could be implemented at future high-energy and high-brightness synchrotron-radiation facilities to provide images of unsectioned and unlabeled cells in their native conditions at enough detail to bridge the techniques of super-resolution optical microscopy and cryo-electron microscopy.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2018 (1)

S. Bajt, M. Prasciolu, H. Fleckenstein, M. Domaracký, H. N. Chapman, A. J. Morgan, O. Yefanov, M. Messerschmidt, Y. Du, K. T. Murray, V. Mariani, M. Kuhn, S. Aplin, K. Pande, P. Villanueva-Perez, K. Stachnik, J. P. J. Chen, A. Andrejczuk, A. Meents, A. Burkhardt, D. Pennicard, X. Huang, H. Yan, E. Nazaretski, Y. S. Chu, and C. E. Hamm, “X-ray focusing with efficient high-NA multilayer laue lenses,” Light Sci. Appl. 7, e17162 (2018).
[Crossref]

2017 (3)

J. Deng, D. J. Vine, S. Chen, Q. Jin, Y. S. G. Nashed, T. Peterka, S. Vogt, and C. Jacobsen, “X-ray ptychographic and fluorescence microscopy of frozen-hydrated cells using continuous scanning,” Sci. Rep. 7, 445 (2017).
[Crossref]

J. Cesar da Silva, A. Pacureanu, Y. Yang, S. Bohic, C. Morawe, R. Barrett, and P. Cloetens, “Efficient concentration of high-energy x-rays for diffraction-limited imaging resolution,” Optica 4, 492–495 (2017).
[Crossref]

A. Meents, M. O. Wiedorn, V. Srajer, R. Henning, I. Sarrou, J. Bergtholdt, M. Barthelmess, P. Y. A. Reinke, D. Dierksmeyer, A. Tolstikova, S. Schaible, M. Messerschmidt, C. M. Ogata, D. J. Kissick, M. H. Taft, D. J. Manstein, J. Lieske, D. Oberthuer, R. F. Fischetti, and H. N. Chapman, “Pink-beam serial crystallography,” Nat. Commun. 8, 1281 (2017).
[Crossref]

2016 (1)

2015 (3)

A. Diaz, B. Malkova, M. Holler, M. Guizar-Sicairos, E. Lima, V. Panneels, G. Pigino, A. G. Bittermann, L. Wettstein, T. Tomizaki, O. Bunk, G. Schertler, T. Ishikawa, R. Wepf, and A. Menzel, “Three-dimensional mass density mapping of cellular ultrastructure by ptychographic x-ray nanotomography,” J. Struct. Biol. 192, 461–469 (2015).
[Crossref]

M. Prasciolu, A. F. G. Leontowich, J. Krzywinski, A. Andrejczuk, H. N. Chapman, and S. Bajt, “Fabrication of wedged multilayer Laue lenses,” Opt. Mater. Express 5, 748–755 (2015).
[Crossref]

A. J. Morgan, M. Prasciolu, A. Andrejczuk, J. Krzywinski, A. Meents, D. Pennicard, H. Graafsma, A. Barty, R. J. Bean, M. Barthelmess, D. Oberthuer, O. Yefanov, A. Aquila, H. N. Chapman, and S. Bajt, “High numerical aperture multilayer Laue lenses,” Sci. Rep. 5, 9892 (2015).
[Crossref]

2014 (6)

Y. Chushkin, F. Zontone, E. Lima, L. De Caro, P. Guardia, L. Manna, and C. Giannini, “Three-dimensional coherent diffractive imaging on non-periodic specimens at the ESRF beamline ID10,” J. Synchrotron Radiat. 21, 594–599 (2014).
[Crossref]

M. Holler, A. Diaz, M. Guizar-Sicairos, P. Karvinen, E. Färm, E. Härkönen, M. Ritala, A. Menzel, J. Raabe, and O. Bunk, “X-ray ptychographic computed tomography at 16 nm isotropic 3D resolution,” Sci. Rep. 4, 3857 (2014).
[Crossref]

M. Eriksson, J. F. van der Veen, and C. Quitmann, “Diffraction-limited storage rings—a window to the science of tomorrow,” J. Synchrotron Radiat. 21, 837–842 (2014).
[Crossref]

R. Carzaniga, M.-C. Domart, L. M. Collinson, and E. Duke, “Cryo-soft x-ray tomography: a journey into the world of the native-state cell,” Protoplasma 251, 449–458 (2014).
[Crossref]

H. Yan, R. Conley, N. Bouet, and Y. S. Chu, “Hard x-ray nanofocusing by multilayer Laue lenses,” J. Phys. D 47, 263001 (2014).
[Crossref]

C. G. Ryan, D. P. Siddons, R. Kirkham, Z. Y. Li, M. D. De Jonge, D. J. Paterson, A. Kuczewski, D. L. Howard, P. A. Dunn, G. Falkenberg, U. Boesenberg, G. De Geronimo, L. A. Fisher, A. Halfpenny, M. J. Lintern, E. Lombi, K. A. Dyl, M. Jensen, G. F. Moorhead, J. S. Cleverley, R. M. Hough, B. Godel, S. J. Barnes, S. A. James, K. M. Spiers, M. Alfeld, G. Wellenreuther, Z. Vukmanovic, and S. Borg, “Maia x-ray fluorescence imaging: capturing detail in complex natural samples,” J. Phys. Conf. Ser. 499, 012002 (2014).
[Crossref]

2012 (1)

R. Fourme, V. Honkimäki, E. Girard, K. Medjoubi, A.-C. Dhaussy, and R. Kahn, and IUCr, “Reduction of radiation damage and other benefits of short wavelengths for macromolecular crystallography data collection,” J. Appl. Crystallogr. 45, 652–661 (2012).
[Crossref]

2010 (3)

A. Schropp and C. G. Schroer, “Dose requirements for resolving a given feature in an object by coherent x-ray diffraction imaging,” New J. Phys. 12, 035016 (2010).
[Crossref]

G. Schneider, P. Guttmann, S. Heim, S. Rehbein, F. Mueller, K. Nagashima, J. B. Heymann, W. G. Muller, J. G. McNally, and W. G. Müller, “Three-dimensional cellular ultrastructure resolved by x-ray microscopy,” Nat. Methods 7, 985–987 (2010).
[Crossref]

C. Holzner, M. Feser, S. Vogt, B. Hornberger, S. B. Baines, and C. Jacobsen, “Zernike phase contrast in scanning microscopy with x-rays,” Nat. Phys. 6, 883–887 (2010).
[Crossref]

2009 (1)

M. R. Howells, T. Beetz, H. N. Chapman, C. Cui, J. M. Holton, C. J. Jacobsen, J. Kirz, E. Lima, S. Marchesini, H. Miao, D. Sayre, D. A. Shapiro, J. C. H. Spence, and D. Starodub, “An assessment of the resolution limitation due to radiation-damage in x-ray diffraction microscopy,” J. Electron. Spectrosc. Relat. Phenom. 170, 4–12 (2009).
[Crossref]

2008 (3)

P. Thibault, M. Dierolf, A. Menzel, O. Bunk, C. David, and F. Pfeiffer, “High-resolution scanning x-ray diffraction microscopy,” Science 321, 379–382 (2008).
[Crossref]

M. Eriksson, L. J. Lindgren, M. Sjöström, E. Wallén, L. Rivkin, and A. Streun, “Some small-emittance light-source lattices with multi-bend achromats,” Nucl. Instrum. Methods Phys. Res., Sect. A 587, 221–226 (2008).
[Crossref]

J. A. Cowan and C. Nave, “The optimum conditions to collect x-ray data from very small samples,” J. Synchrotron Radiat. 15, 458–462 (2008).
[Crossref]

2005 (2)

C. Nave and M. A. Hill, “Will reduced radiation damage occur with very small crystals?” J. Synchrotron Radiat. 12, 299–303 (2005).
[Crossref]

D. H. Bilderback, P. Elleaume, and E. Weckert, “Review of third and next generation synchrotron light sources,” J. Phys. B 38, S773–S797 (2005).
[Crossref]

2004 (1)

2003 (2)

T. Beetz and C. Jacobsen, “Soft X-ray radiation-damage studies in PMMA using a cryo-STXM,” J. Synchrotron Radiat. 10, 280–283 (2003).
[Crossref]

Y. Wang, W. Yun, and C. Jacobsen, “Achromatic Fresnel optics for wideband extreme-ultraviolet and x-ray imaging,” Nature 424, 50–53 (2003).
[Crossref]

2002 (1)

S. C. Mayo, P. R. Miller, S. W. Wilkins, T. J. Davis, D. Gao, T. E. Gureyev, D. Paganin, D. J. Parry, A. Pogany, and A. W. Stevenson, “Quantitative x-ray projection microscopy: phase-contrast and multi-spectral imaging,” J. Microsc. 207, 79–96 (2002).
[Crossref]

2000 (2)

D. Weiß, G. Schneider, B. Niemann, P. Guttmann, D. Rudolph, and G. Schmahl, “Computed tomography of cryogenic biological specimens based on x-ray microscopic images,” Ultramicroscopy 84, 185–197 (2000).
[Crossref]

T. Y. Teng and K. Moffat, “Primary radiation damage of protein crystals by an intense synchrotron x-ray beam,” J. Synchrotron Radiat. 7, 313–317 (2000).
[Crossref]

1999 (1)

J. Miao, P. Charalambous, J. Kirz, and D. Sayre, “Extending the methodology of x-ray crystallography to allow imaging of micrometre-sized non-crystalline specimens,” Nature 400, 342–344 (1999).
[Crossref]

1998 (1)

C. Jacobsen and J. Kirz, “X-ray microscopy with synchrotron radiation,” Nat. Struct. Biol. 5, 650–653 (1998).
[Crossref]

1996 (2)

H. N. Chapman, “Phase-retrieval X-ray microscopy by Wigner-distribution deconvolution,” Ultramicroscopy 66, 153–172 (1996).
[Crossref]

A. Snigirev, V. Kohn, I. Snigireva, and B. Lengeler, “A compound refractive lens for focusing high-energy x-rays,” Nature 384, 49–51 (1996).
[Crossref]

1995 (2)

D. Sayre and H. N. Chapman, “X-ray microscopy,” Acta Crystallogr. Sect. A 51, 237–252 (1995).
[Crossref]

R. Henderson, “The potential and limitations of neutrons, electrons and X-rays for atomic resolution microscopy of unstained biological molecules,” Q. Rev. Biophys. 28, 171–193 (1995).
[Crossref]

1994 (1)

P. Siffert, “Cadmium telluride and related materials as x-ray and gamma-ray detectors: a review of recent progress,” Proc. SPIE 2305, 98–109 (1994).
[Crossref]

1992 (1)

G. F. Foster, C. J. Buckley, P. M. Bennett, and R. E. Burge, “Investigation of radiation damage to biological specimens at water window wavelengths,” Rev. Sci. Instrum. 63, 599–600 (1992).
[Crossref]

1989 (1)

1980 (1)

J. R. Fienup, “Iterative method applied to image reconstruction and to computer-generated holograms,” Opt. Eng. 19, 193297 (1980).
[Crossref]

1976 (1)

R. Hegerl and W. Hoppe, “Influence of electron noise on three-dimensional image reconstruction,” Z. Naturforsch. 31, 1717–1721 (1976).
[Crossref]

1975 (1)

J. H. Hubbell, W. J. Veigele, E. A. Briggs, R. T. Brown, D. T. Cromer, and R. J. Howerton, “Atomic form factors, incoherent scattering functions, and photon scattering cross sections,” J. Phys. Chem. Ref. Data 4, 471–538 (1975).
[Crossref]

1972 (1)

R. W. Gerchberg and W. O. Saxton, “A practical algorithm for the determination of phase from image and diffraction plane pictures,” Optik 35, 237–246 (1972).

1946 (1)

A. Rose, “A unified approach to the performance of photographic film, television pickup tubes, and the human eye,” J. Soc. Motion Pict. Eng. 47, 273–294 (1946).
[Crossref]

Alfeld, M.

C. G. Ryan, D. P. Siddons, R. Kirkham, Z. Y. Li, M. D. De Jonge, D. J. Paterson, A. Kuczewski, D. L. Howard, P. A. Dunn, G. Falkenberg, U. Boesenberg, G. De Geronimo, L. A. Fisher, A. Halfpenny, M. J. Lintern, E. Lombi, K. A. Dyl, M. Jensen, G. F. Moorhead, J. S. Cleverley, R. M. Hough, B. Godel, S. J. Barnes, S. A. James, K. M. Spiers, M. Alfeld, G. Wellenreuther, Z. Vukmanovic, and S. Borg, “Maia x-ray fluorescence imaging: capturing detail in complex natural samples,” J. Phys. Conf. Ser. 499, 012002 (2014).
[Crossref]

Andrejczuk, A.

S. Bajt, M. Prasciolu, H. Fleckenstein, M. Domaracký, H. N. Chapman, A. J. Morgan, O. Yefanov, M. Messerschmidt, Y. Du, K. T. Murray, V. Mariani, M. Kuhn, S. Aplin, K. Pande, P. Villanueva-Perez, K. Stachnik, J. P. J. Chen, A. Andrejczuk, A. Meents, A. Burkhardt, D. Pennicard, X. Huang, H. Yan, E. Nazaretski, Y. S. Chu, and C. E. Hamm, “X-ray focusing with efficient high-NA multilayer laue lenses,” Light Sci. Appl. 7, e17162 (2018).
[Crossref]

M. Prasciolu, A. F. G. Leontowich, J. Krzywinski, A. Andrejczuk, H. N. Chapman, and S. Bajt, “Fabrication of wedged multilayer Laue lenses,” Opt. Mater. Express 5, 748–755 (2015).
[Crossref]

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Supplementary Material (1)

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Figures (4)

Fig. 1.
Fig. 1. (a) Photoabsorption (black dotted), coherent scattering (continuous blue), and Compton scattering (dashed red) cross sections for carbon as a function of the photon energy. (b) Number of reactions per deposited eV in carbon as a function of the photon energy for photoabsorption (black dotted), coherent scattering (blue), and total scattering (red dashed) [28]. (c) Differential Compton and (d) coherent scattering cross sections per carbon atom at photon energies of 30 keV (continuous), 60 keV (dotted), and 90 keV (dashed).
Fig. 2.
Fig. 2. (a) Minimum required fluence and (b) dose by SCXM to distinguish between a 10 nm voxel of biomolecule and water, as a function of photon energy. The minimum imaging dose is compared to the maximum tolerable dose of 109  Gy to image a radiosensitive material with a resolution of 10 nm (red-dotted curve) as reported in Ref. [23].
Fig. 3.
Fig. 3. (a) Plot of the dose required to discern a biomolecular voxel feature embedded in a 5-μm cell of water to a signal to noise level of 5 as a function of the width of the voxel in SCXM at 64 keV photon energy (red dashed line) and coherent diffractive imaging at 10 keV (continuous blue line). The black dotted line represents the maximum tolerable dose as a function of the resolution for a biological sample as reported in Ref. [23]. (b) Simulated images for SCXM and (c) coherent diffractive imaging of a cell-like object with objects of 34 nm width (Gaussian profiles with 1/e radius equal to 17 nm) at the predicted required fluxes and doses for that feature size. The dose for the coherent diffraction image is about 103 higher than scanned image that makes use of all scattered photons.
Fig. 4.
Fig. 4. (a) A diffractive optic such as a MLL produces different focal lengths for a long (red dotted) and a short (blue dashed-dotted) wavelength. (b) Schematic diagram of a proposed X-ray achromat lens which combines a stack of refractive negative lenses which compensate the dispersion of the MLL. (c) A schematic of a scanning Compton X-ray microscope with a detector that covers almost a 4π solid angle around the sample. The sample is scanned relative to the beam.

Tables (2)

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Table 1. Imaging Requirement of SCXM at 64 keV Photon Energy to Reconstruct 34 nm PMMA, Protein, and DNA Features Embedded in 5-μm-Wide Water Cell

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Table 2. Imaging Requirement for Coherent Diffraction Imaging at 10 keV Photon Energy to Reconstruct 34 nm PMMA, Protein, and DNA Features Embedded in 5-μm Thickness of Water

Equations (4)

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NSi=ϕΩdetdσSidΩdΩ,
Δr=1.22λ2NA.
5|NSmNSw|NSm+NSw.
D=EdepoρV,

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