Abstract

Computed tomography based on high-resolution soft x-ray microscopy utilizes the natural contrast for biological specimens provided by the water window (λ=2.4-4.4 nm) and the high resolving power of zone plate objectives. It is capable of revealing the 3D structure of biological specimens at sub-visible-microscopic resolution. To date, the technique has only been available at synchrotron-based microscopes, which limits the researchers access. In the present paper we demonstrate high-resolution soft x-ray tomography with a laboratory zone-plate-based soft x-ray microscope. The specimen, a diatom mounted on a glass capillary, was reconstructed from a tilt series of 53 images covering 180° using a filtered back projection algorithm. The resolution of the tomogram was estimated to a half period of 140 nm using a differential-phase-residual method. Cryo-fixation, increased source brightness and extended-depth-of-focus objectives are important for pushing the resolution of compact systems for biological samples.

© 2009 Optical Society of America

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2008

M. Hoshino and S. Aoki, "Laboratory-scale soft X-ray imaging microtomography using Wolter mirror optics," Appl. Phys. Expr. 1, 067005 (2008).
[CrossRef]

D. Y. Parkinson, G. McDermott, L. D. Etkin, M. A. Le Gros and C. A. Larabell, "Quantitative 3-D imaging of eukaryotic cells using soft X-ray tomography," J. Struct. Biol. 162, 380-386 (2008).
[CrossRef] [PubMed]

M. Benk, K. Bergmann, D. Schäfer, and T. Wilhein, "Compact soft x-ray microscope using a gas-discharge light source," Opt. Lett. 33, 2359-2361 (2008)
[CrossRef] [PubMed]

2007

P. A. C. Takman, H. Stollberg, G. A. Johansson, A. Holmberg, M. Lindblom, and H. M. Hertz, "High-resolution compact X-ray microscopy," J. Microsc. 226, 175 (2007).
[CrossRef] [PubMed]

2006

A. Tkachuk, M. Feser, H. Cui, F. Duewer, H Chang, and W. Yun, Xradia, Inc. "High-resolution x-ray tomography using laboratory sources," Proc. SPIE 6318, 1-8 (2006), http://www.xradia.com.

H. Stollberg, S. Yulin, P. A. C. Takman, and H. M. Hertz, "High-reflectivity Cr/Sc multilayer condenser for compact water-window microscopy," Rev. Sci. Instrum. 77, 123101 (2006).
[CrossRef]

2005

W. Chao, B. D. Harteneck, J. A. Liddle, E. H. Anderson, and D. Attwood, "Soft X-ray microscopy at a spatial resolution better than 15 nm," Nature 435, 1210-1213 (2005).
[CrossRef] [PubMed]

2004

A. Holmberg, S. Rehbein, and H. M. Hertz, "Nano-fabrication of condenser and micro zone plates for compact x-ray microscopy," Microelectron. Eng. 73-74, 639 (2004).
[CrossRef]

C. A. Larabell and M. A. Le Gros, "X-ray tomography generates 3-D reconstructions fo the yeast, Saccharomyces cerevisiae, at 60-nm resolution," Mol. Biol. Cell. 15, 957-962 (2004).
[CrossRef]

2003

J. de Groot, O. Hemberg, A. Holmberg, and H. M. Hertz, "Target optimization of a water-window liquid-jet laser-plasma source," J. Appl. Phys. 94, 3717 (2003).
[CrossRef]

2001

D. Wiess, G. Schneider, S. Vogt, P. Guttmann, B. Niemann, D. Rudolph, and G. Schmahl, "Tomographic imaging of biological specimens with the cryo transmission x-ray microscope," NIMPR A 467-468, 1308-1311 (2001).

2000

D. Weiss, G. Schneider, B. Niemann, P Guttman, D. Rudolph, and G. Schmahl, "Computed tomography of cryogenic biological specimens based on X-ray microscopic images," Ultramicroscopy. 84, 185-197 (2000).
[CrossRef] [PubMed]

M. Berglund, L. Rymell, M. Peuker, T. Wilhein, and H. M. Hertz, "Compact water-window transmission X-ray microscopy," J. Microsc. 197, 268-273 (2000).
[CrossRef] [PubMed]

1997

J. Lehr, "3D X-ray microscopy: tomographic imaging of mineral sheaths of bacteria Leptothrix Ochracea with the Gottingen X-ray microscope at BESSY," Optik 104, 166 (1997).

1996

J. R. Kremer, D. N. Mastronarde, and R. McIntosh, "Computer visualization of three-dimensional image data using IMOD," J. Struct. Biol. 116, 71-76 (1996). [http://bio3d.colorado.edu/imod/].
[CrossRef] [PubMed]

Anderson, E. H.

W. Chao, B. D. Harteneck, J. A. Liddle, E. H. Anderson, and D. Attwood, "Soft X-ray microscopy at a spatial resolution better than 15 nm," Nature 435, 1210-1213 (2005).
[CrossRef] [PubMed]

Aoki, S.

M. Hoshino and S. Aoki, "Laboratory-scale soft X-ray imaging microtomography using Wolter mirror optics," Appl. Phys. Expr. 1, 067005 (2008).
[CrossRef]

Attwood, D.

W. Chao, B. D. Harteneck, J. A. Liddle, E. H. Anderson, and D. Attwood, "Soft X-ray microscopy at a spatial resolution better than 15 nm," Nature 435, 1210-1213 (2005).
[CrossRef] [PubMed]

Benk, M.

Berglund, M.

M. Berglund, L. Rymell, M. Peuker, T. Wilhein, and H. M. Hertz, "Compact water-window transmission X-ray microscopy," J. Microsc. 197, 268-273 (2000).
[CrossRef] [PubMed]

Bergmann, K.

Chang, H

A. Tkachuk, M. Feser, H. Cui, F. Duewer, H Chang, and W. Yun, Xradia, Inc. "High-resolution x-ray tomography using laboratory sources," Proc. SPIE 6318, 1-8 (2006), http://www.xradia.com.

Chao, W.

W. Chao, B. D. Harteneck, J. A. Liddle, E. H. Anderson, and D. Attwood, "Soft X-ray microscopy at a spatial resolution better than 15 nm," Nature 435, 1210-1213 (2005).
[CrossRef] [PubMed]

Cui, H.

A. Tkachuk, M. Feser, H. Cui, F. Duewer, H Chang, and W. Yun, Xradia, Inc. "High-resolution x-ray tomography using laboratory sources," Proc. SPIE 6318, 1-8 (2006), http://www.xradia.com.

de Groot, J.

J. de Groot, O. Hemberg, A. Holmberg, and H. M. Hertz, "Target optimization of a water-window liquid-jet laser-plasma source," J. Appl. Phys. 94, 3717 (2003).
[CrossRef]

Duewer, F.

A. Tkachuk, M. Feser, H. Cui, F. Duewer, H Chang, and W. Yun, Xradia, Inc. "High-resolution x-ray tomography using laboratory sources," Proc. SPIE 6318, 1-8 (2006), http://www.xradia.com.

Etkin, L. D.

D. Y. Parkinson, G. McDermott, L. D. Etkin, M. A. Le Gros and C. A. Larabell, "Quantitative 3-D imaging of eukaryotic cells using soft X-ray tomography," J. Struct. Biol. 162, 380-386 (2008).
[CrossRef] [PubMed]

Feser, M.

A. Tkachuk, M. Feser, H. Cui, F. Duewer, H Chang, and W. Yun, Xradia, Inc. "High-resolution x-ray tomography using laboratory sources," Proc. SPIE 6318, 1-8 (2006), http://www.xradia.com.

Guttman, P

D. Weiss, G. Schneider, B. Niemann, P Guttman, D. Rudolph, and G. Schmahl, "Computed tomography of cryogenic biological specimens based on X-ray microscopic images," Ultramicroscopy. 84, 185-197 (2000).
[CrossRef] [PubMed]

Guttmann, P.

D. Wiess, G. Schneider, S. Vogt, P. Guttmann, B. Niemann, D. Rudolph, and G. Schmahl, "Tomographic imaging of biological specimens with the cryo transmission x-ray microscope," NIMPR A 467-468, 1308-1311 (2001).

Harteneck, B. D.

W. Chao, B. D. Harteneck, J. A. Liddle, E. H. Anderson, and D. Attwood, "Soft X-ray microscopy at a spatial resolution better than 15 nm," Nature 435, 1210-1213 (2005).
[CrossRef] [PubMed]

Hemberg, O.

J. de Groot, O. Hemberg, A. Holmberg, and H. M. Hertz, "Target optimization of a water-window liquid-jet laser-plasma source," J. Appl. Phys. 94, 3717 (2003).
[CrossRef]

Hertz, H. M.

P. A. C. Takman, H. Stollberg, G. A. Johansson, A. Holmberg, M. Lindblom, and H. M. Hertz, "High-resolution compact X-ray microscopy," J. Microsc. 226, 175 (2007).
[CrossRef] [PubMed]

H. Stollberg, S. Yulin, P. A. C. Takman, and H. M. Hertz, "High-reflectivity Cr/Sc multilayer condenser for compact water-window microscopy," Rev. Sci. Instrum. 77, 123101 (2006).
[CrossRef]

A. Holmberg, S. Rehbein, and H. M. Hertz, "Nano-fabrication of condenser and micro zone plates for compact x-ray microscopy," Microelectron. Eng. 73-74, 639 (2004).
[CrossRef]

J. de Groot, O. Hemberg, A. Holmberg, and H. M. Hertz, "Target optimization of a water-window liquid-jet laser-plasma source," J. Appl. Phys. 94, 3717 (2003).
[CrossRef]

M. Berglund, L. Rymell, M. Peuker, T. Wilhein, and H. M. Hertz, "Compact water-window transmission X-ray microscopy," J. Microsc. 197, 268-273 (2000).
[CrossRef] [PubMed]

Holmberg, A.

P. A. C. Takman, H. Stollberg, G. A. Johansson, A. Holmberg, M. Lindblom, and H. M. Hertz, "High-resolution compact X-ray microscopy," J. Microsc. 226, 175 (2007).
[CrossRef] [PubMed]

A. Holmberg, S. Rehbein, and H. M. Hertz, "Nano-fabrication of condenser and micro zone plates for compact x-ray microscopy," Microelectron. Eng. 73-74, 639 (2004).
[CrossRef]

J. de Groot, O. Hemberg, A. Holmberg, and H. M. Hertz, "Target optimization of a water-window liquid-jet laser-plasma source," J. Appl. Phys. 94, 3717 (2003).
[CrossRef]

Hoshino, M.

M. Hoshino and S. Aoki, "Laboratory-scale soft X-ray imaging microtomography using Wolter mirror optics," Appl. Phys. Expr. 1, 067005 (2008).
[CrossRef]

Johansson, G. A.

P. A. C. Takman, H. Stollberg, G. A. Johansson, A. Holmberg, M. Lindblom, and H. M. Hertz, "High-resolution compact X-ray microscopy," J. Microsc. 226, 175 (2007).
[CrossRef] [PubMed]

Kremer, J. R.

J. R. Kremer, D. N. Mastronarde, and R. McIntosh, "Computer visualization of three-dimensional image data using IMOD," J. Struct. Biol. 116, 71-76 (1996). [http://bio3d.colorado.edu/imod/].
[CrossRef] [PubMed]

Larabell, C. A.

D. Y. Parkinson, G. McDermott, L. D. Etkin, M. A. Le Gros and C. A. Larabell, "Quantitative 3-D imaging of eukaryotic cells using soft X-ray tomography," J. Struct. Biol. 162, 380-386 (2008).
[CrossRef] [PubMed]

C. A. Larabell and M. A. Le Gros, "X-ray tomography generates 3-D reconstructions fo the yeast, Saccharomyces cerevisiae, at 60-nm resolution," Mol. Biol. Cell. 15, 957-962 (2004).
[CrossRef]

Le Gros, M. A.

D. Y. Parkinson, G. McDermott, L. D. Etkin, M. A. Le Gros and C. A. Larabell, "Quantitative 3-D imaging of eukaryotic cells using soft X-ray tomography," J. Struct. Biol. 162, 380-386 (2008).
[CrossRef] [PubMed]

C. A. Larabell and M. A. Le Gros, "X-ray tomography generates 3-D reconstructions fo the yeast, Saccharomyces cerevisiae, at 60-nm resolution," Mol. Biol. Cell. 15, 957-962 (2004).
[CrossRef]

Lehr, J.

J. Lehr, "3D X-ray microscopy: tomographic imaging of mineral sheaths of bacteria Leptothrix Ochracea with the Gottingen X-ray microscope at BESSY," Optik 104, 166 (1997).

Liddle, J. A.

W. Chao, B. D. Harteneck, J. A. Liddle, E. H. Anderson, and D. Attwood, "Soft X-ray microscopy at a spatial resolution better than 15 nm," Nature 435, 1210-1213 (2005).
[CrossRef] [PubMed]

Lindblom, M.

P. A. C. Takman, H. Stollberg, G. A. Johansson, A. Holmberg, M. Lindblom, and H. M. Hertz, "High-resolution compact X-ray microscopy," J. Microsc. 226, 175 (2007).
[CrossRef] [PubMed]

Mastronarde, D. N.

J. R. Kremer, D. N. Mastronarde, and R. McIntosh, "Computer visualization of three-dimensional image data using IMOD," J. Struct. Biol. 116, 71-76 (1996). [http://bio3d.colorado.edu/imod/].
[CrossRef] [PubMed]

McDermott, G.

D. Y. Parkinson, G. McDermott, L. D. Etkin, M. A. Le Gros and C. A. Larabell, "Quantitative 3-D imaging of eukaryotic cells using soft X-ray tomography," J. Struct. Biol. 162, 380-386 (2008).
[CrossRef] [PubMed]

McIntosh, R.

J. R. Kremer, D. N. Mastronarde, and R. McIntosh, "Computer visualization of three-dimensional image data using IMOD," J. Struct. Biol. 116, 71-76 (1996). [http://bio3d.colorado.edu/imod/].
[CrossRef] [PubMed]

Niemann, B.

D. Wiess, G. Schneider, S. Vogt, P. Guttmann, B. Niemann, D. Rudolph, and G. Schmahl, "Tomographic imaging of biological specimens with the cryo transmission x-ray microscope," NIMPR A 467-468, 1308-1311 (2001).

D. Weiss, G. Schneider, B. Niemann, P Guttman, D. Rudolph, and G. Schmahl, "Computed tomography of cryogenic biological specimens based on X-ray microscopic images," Ultramicroscopy. 84, 185-197 (2000).
[CrossRef] [PubMed]

Parkinson, D. Y.

D. Y. Parkinson, G. McDermott, L. D. Etkin, M. A. Le Gros and C. A. Larabell, "Quantitative 3-D imaging of eukaryotic cells using soft X-ray tomography," J. Struct. Biol. 162, 380-386 (2008).
[CrossRef] [PubMed]

Peuker, M.

M. Berglund, L. Rymell, M. Peuker, T. Wilhein, and H. M. Hertz, "Compact water-window transmission X-ray microscopy," J. Microsc. 197, 268-273 (2000).
[CrossRef] [PubMed]

Rehbein, S.

A. Holmberg, S. Rehbein, and H. M. Hertz, "Nano-fabrication of condenser and micro zone plates for compact x-ray microscopy," Microelectron. Eng. 73-74, 639 (2004).
[CrossRef]

Rudolph, D.

D. Wiess, G. Schneider, S. Vogt, P. Guttmann, B. Niemann, D. Rudolph, and G. Schmahl, "Tomographic imaging of biological specimens with the cryo transmission x-ray microscope," NIMPR A 467-468, 1308-1311 (2001).

D. Weiss, G. Schneider, B. Niemann, P Guttman, D. Rudolph, and G. Schmahl, "Computed tomography of cryogenic biological specimens based on X-ray microscopic images," Ultramicroscopy. 84, 185-197 (2000).
[CrossRef] [PubMed]

Rymell, L.

M. Berglund, L. Rymell, M. Peuker, T. Wilhein, and H. M. Hertz, "Compact water-window transmission X-ray microscopy," J. Microsc. 197, 268-273 (2000).
[CrossRef] [PubMed]

Schäfer, D.

Schmahl, G.

D. Wiess, G. Schneider, S. Vogt, P. Guttmann, B. Niemann, D. Rudolph, and G. Schmahl, "Tomographic imaging of biological specimens with the cryo transmission x-ray microscope," NIMPR A 467-468, 1308-1311 (2001).

D. Weiss, G. Schneider, B. Niemann, P Guttman, D. Rudolph, and G. Schmahl, "Computed tomography of cryogenic biological specimens based on X-ray microscopic images," Ultramicroscopy. 84, 185-197 (2000).
[CrossRef] [PubMed]

Schneider, G.

D. Wiess, G. Schneider, S. Vogt, P. Guttmann, B. Niemann, D. Rudolph, and G. Schmahl, "Tomographic imaging of biological specimens with the cryo transmission x-ray microscope," NIMPR A 467-468, 1308-1311 (2001).

D. Weiss, G. Schneider, B. Niemann, P Guttman, D. Rudolph, and G. Schmahl, "Computed tomography of cryogenic biological specimens based on X-ray microscopic images," Ultramicroscopy. 84, 185-197 (2000).
[CrossRef] [PubMed]

Stollberg, H.

P. A. C. Takman, H. Stollberg, G. A. Johansson, A. Holmberg, M. Lindblom, and H. M. Hertz, "High-resolution compact X-ray microscopy," J. Microsc. 226, 175 (2007).
[CrossRef] [PubMed]

H. Stollberg, S. Yulin, P. A. C. Takman, and H. M. Hertz, "High-reflectivity Cr/Sc multilayer condenser for compact water-window microscopy," Rev. Sci. Instrum. 77, 123101 (2006).
[CrossRef]

Takman, P. A. C.

P. A. C. Takman, H. Stollberg, G. A. Johansson, A. Holmberg, M. Lindblom, and H. M. Hertz, "High-resolution compact X-ray microscopy," J. Microsc. 226, 175 (2007).
[CrossRef] [PubMed]

H. Stollberg, S. Yulin, P. A. C. Takman, and H. M. Hertz, "High-reflectivity Cr/Sc multilayer condenser for compact water-window microscopy," Rev. Sci. Instrum. 77, 123101 (2006).
[CrossRef]

Tkachuk, A.

A. Tkachuk, M. Feser, H. Cui, F. Duewer, H Chang, and W. Yun, Xradia, Inc. "High-resolution x-ray tomography using laboratory sources," Proc. SPIE 6318, 1-8 (2006), http://www.xradia.com.

Vogt, S.

D. Wiess, G. Schneider, S. Vogt, P. Guttmann, B. Niemann, D. Rudolph, and G. Schmahl, "Tomographic imaging of biological specimens with the cryo transmission x-ray microscope," NIMPR A 467-468, 1308-1311 (2001).

Weiss, D.

D. Weiss, G. Schneider, B. Niemann, P Guttman, D. Rudolph, and G. Schmahl, "Computed tomography of cryogenic biological specimens based on X-ray microscopic images," Ultramicroscopy. 84, 185-197 (2000).
[CrossRef] [PubMed]

Wiess, D.

D. Wiess, G. Schneider, S. Vogt, P. Guttmann, B. Niemann, D. Rudolph, and G. Schmahl, "Tomographic imaging of biological specimens with the cryo transmission x-ray microscope," NIMPR A 467-468, 1308-1311 (2001).

Wilhein, T.

M. Benk, K. Bergmann, D. Schäfer, and T. Wilhein, "Compact soft x-ray microscope using a gas-discharge light source," Opt. Lett. 33, 2359-2361 (2008)
[CrossRef] [PubMed]

M. Berglund, L. Rymell, M. Peuker, T. Wilhein, and H. M. Hertz, "Compact water-window transmission X-ray microscopy," J. Microsc. 197, 268-273 (2000).
[CrossRef] [PubMed]

Yulin, S.

H. Stollberg, S. Yulin, P. A. C. Takman, and H. M. Hertz, "High-reflectivity Cr/Sc multilayer condenser for compact water-window microscopy," Rev. Sci. Instrum. 77, 123101 (2006).
[CrossRef]

Yun, W.

A. Tkachuk, M. Feser, H. Cui, F. Duewer, H Chang, and W. Yun, Xradia, Inc. "High-resolution x-ray tomography using laboratory sources," Proc. SPIE 6318, 1-8 (2006), http://www.xradia.com.

Appl. Phys. Expr.

M. Hoshino and S. Aoki, "Laboratory-scale soft X-ray imaging microtomography using Wolter mirror optics," Appl. Phys. Expr. 1, 067005 (2008).
[CrossRef]

J. Appl. Phys.

J. de Groot, O. Hemberg, A. Holmberg, and H. M. Hertz, "Target optimization of a water-window liquid-jet laser-plasma source," J. Appl. Phys. 94, 3717 (2003).
[CrossRef]

J. Microsc.

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Supplementary Material (2)

» Media 1: MOV (1146 KB)     
» Media 2: MOV (1624 KB)     

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Figures (5)

Fig. 1.
Fig. 1.

Illustration showing the arrangement of the microscope.

Fig. 2.
Fig. 2.

(a) shows an original projection image, whereas (b) shows the same projection image after denoising and illumination correction. The inserts have been added to more clearly demonstrate the improvements.

Fig. 3.
Fig. 3.

Selected slices through the reconstructed tomgram showing the structure of the diatom. (a) shows a section of the whole reconstructed region, (b) and (c) are slizes showing the large diatom opening and some internal structures, (d-f) show slizes through the diatom in which the small grating-like structure of the diatom is resolved.

Fig. 4.
Fig. 4.

Rotation series of the reconstructed diatom. The capillary has been removed to show the internal structure. Animations are available online (Media 1), (Media 2).

Fig. 5.
Fig. 5.

The sectional average differential phase residual (DPR) calculated between two equally masked but independently reconstructed regions of the diatom. The dashed line shows the DPR when the same mask was applied to random noise.

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