Cryo-electron tomography of bacteria: Progress, challenges and future prospects

Nature Reviews Microbiology

Volumn 7, Issue 9, 2009, Pages 666-675

  Milne, Jacqueline L S ^a   Subramaniam, Sriram ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN;

BACTERIAL CELL; BACTERIUM EXAMINATION; CELL COMPOSITION; CELL LABELING; CELL ORGANELLE; CELL SIZE; CELL STRUCTURE; CELLULAR DISTRIBUTION; CRYOELECTRON TOMOGRAPHY; CYANOBACTERIUM; ELECTRON MICROSCOPY; FROZEN SECTION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; IMAGE PROCESSING; IMAGE RECONSTRUCTION; LIGHT SCATTERING; MOLECULAR IMAGING; MYCOBACTERIUM; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OPTICAL RESOLUTION; PRIORITY JOURNAL; REVIEW; SCANNING ELECTRON MICROSCOPY; STRUCTURE ANALYSIS; THREE DIMENSIONAL IMAGING; TOMOGRAPHY; VITRIFICATION; WHOLE CELL; X RAY CRYSTALLOGRAPHY;

BACTERIA; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; IMAGING, THREE-DIMENSIONAL;

BACTERIA (MICROORGANISMS);

EID: 69249213558     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro2183     Document Type: Review

References (91)

1. Goodsell, D. S. Inside a living cell. Trends Biochem. Sci. 16 203-206 (1991).
2. Lučić, V., Leis, A. & Baumeister, W. Cryo-electron tomography of cells: Connecting structure and function. Histochem. Cell Biol. 130, 185-196 (2008).
3. Morris, D. M. & Jensen, G. J. Toward a biomechanical understanding of whole bacterial cells. Annu. Rev. Biochem. 77, 583-613 (2008).
4. Subramaniam, S. Bridging the imaging gap: Visualizing subcellular architecture with electron tomography. Curr. Opin. Microbiol. 8 316-322 (2005).
5. Egelman, E. H. Single-particle reconstruction from EM images of helical filaments. Curr. Opin. Struct. Biol. 17, 556-561 (2007).
6. Frank, J. Three-dimensional electron microscopy of macromolecular assemblies: Visualization of biological molecules in their native state (Oxford University Press, 2006).
7. Orlova, E. V. & Saibil, H. R. Structure determination of macromolecular assemblies by single-particle analysis of cryo-electron micrographs. Curr. Opin. Struct. Biol. 14, 584-590 (2004).
8. Yonekura, K., Maki-Yonekura, S. & Namba, K. Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424, 643-650 (2003).
9. Zhou, Z. H. Towards atomic resolution structural determination by single-particle cryo-electron microscopy. Curr. Opin. Struct. Biol. 18, 218-228 (2008).
10. Bellare, J. R., Davis, H. T., Scriven, L. E. & Talmon, Y. Controlled environment vitrification system: An improved sample preparation technique. J. Electron. Microsc. Tech. 10, 87-111 (1988).
11. Frederik, P. M. & Hubert, D. H. W. Cryoelectron microscopy of liposomes. Meth. Enzymol. 391, 431-448 (2005).
12. Dubochet, J. et al. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21, 129-228 (1988).
13. Iancu, C. V., Wright, E. R., Heymann, J. B. & Jensen, G. J. A comparison of liquid nitrogen and liquid helium as cryogens for electron cryotomography. J. Struct. Biol. 153, 231-240 (2006).
14. McIntosh, J. R. Cellular electron microscopy (ed. McIntosh, J. R.) (Academic, San Diego, 2007).
15. Mastronarde, D. N. Correction for nonperpendicularity of beam and tilt axis in tomographic reconstructions with the IMOD package. J. Microsc. 230, 212-217 (2008).
16. Boudier, T. et al. A public software for energy filtering transmission electron tomography (EFTET-J.): Application to the study of granular inclusions in bacteria from Riftia pachyptila. J. Struct. Biol. 151, 151-159 (2005).
17. Messaoudii, C., Boudier, T., Sanchez Sorzano, C. O. & Marco, S. TomoJ: tomography software for threedimensional reconstruction in transmission electron microscopy. BMC Bioinformatics 8, 288 (2007).
18. Frangakis, A. S. & Hegerl, R. Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. J. Struct. Biol. 135, 239-250 (2001).
19. Narasimha, R. et al. Evaluation of denoising algorithms for biological electron tomography. J. Struct. Biol. 164, 7-17 (2008).
20. Borgnia, M. J., Subramaniam, S. & Milne, J. L. S. Three-dimensional imaging of the highly bent architecture of Bdellovibrio bacteriovorus by using cryo-electron tomography. J. Bacteriol. 190, 2588-2596 (2008).
21. Briegel, A. et al. Multiple large filament bundles observed in Caulobacter crescentus by electron cryotomography. Mol. Microbiol. 62, 5-14 (2006).
22. Charon, N. W. et al. The flat ribbon configuration of the periplasmic flagella of Borrelia burgdorferi and its relationship to motility and morphology. J. Bacteriol. 191, 600-607 (2009).
23. Comolli, L. R., Baker, B. J., Downing, K. H., Siegerist, C. E. & Banfield, J. F. Three-dimensional analysis of the structure and ecology of a novel, ultra-small archaeon. ISME J. 3, 159-167 (2009).
24. Grimm, R. et al. Electron. tomography of ice-embedded prokaryotic cells. Biophys. J. 74, 1031-1042 (1998).
25. Henderson, G. P. & Jensen, G. J. Three-dimensional structure of Mycoplasma pneumoniae's attachment organelle and a model for its role in gliding motility. Mol. Microbiol 60, 376-385 (2006).
26. Hoffmann, C., Leis, A., Niederweis, M., Plitzko, J. M. & Engelhardt, H. Disclosure of the mycobacterial outer membrane: Cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc. Natl Acad. Sci. USA 105, 3963-3967 (2008).
27. Izard, J., Hsieh, C.-E., Limberger, R. J., Mannella, C. A. & Marko, M. Native cellular architecture of Treponema denticola revealed by cryo-electron tomography. J. Struct. Biol. 163, 10-17 (2008).
28. Murphy, G. E., Matson, E. G., Leadbetter, J. R., Berg, H. C. & Jensen, G. J. Novel ultrastructures of Treponema primitia and their implications for motility. Mol. Microbiol. 67, 1184-1195 (2008).
29. Junglas, B. et al. Ignicoccus hospitalis and Nanoarchaeum equitans: Ultrastructure, cell-cell interaction, and 3D reconstruction from serial sections of freeze-substituted cells and by electron cryotomography. Arch. Microbiol. 190, 395-408 (2008).
30. Komeili, A., Li, Z., Newman, D. K. & Jensen, G. J. Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 311, 242-245 (2006).
31. Konorty, M., Kahana, N., Linaroudis, A., Minsky, A. & Medalia, O. Structural analysis of photosynthetic membranes by cryo-electron tomography of intact Rhodopseudomonas viridis cells. J. Struct. Biol. 161, 393-400 (2008).
32. Liu, J., McBride, M. J. & Subramaniam, S. Cell surface filaments of the gliding bacterium Flavobacterium johnsoniae revealed by cryo-electron tomography. J. Bacteriol. 189, 7503-7506 (2007).
33. Nickell, S., Hegerl, R., Baumeister, W. & Rachel, R. Pyrodictium cannulae enter the periplasmic space but do not enter the cytoplasm, as revealed by cryo-electron tomography. J. Struct. Biol. 141 34-42 (2003).
34. Ting, C. S., Hsieh, C.-E., Sundararaman, S., Mannella, C. & Marko, M. Cryo-electron tomography reveals the comparative three-dimensional architecture of Prochlorococcus, a globally important marine cyanobacterium. J. Bacteriol. 189, 4485-4493 (2007).
35. Zhang, P., Khursigara, C. M., Hartnell, L. M. & Subramaniam, S. Direct visualization of Escherichia coli chemotaxis receptor arrays using cryo-electron microscopy. Proc. Natl Acad. Sci. USA 104, 3777-3781 (2007).
36. Matias, V. R. F. & Beveridge, T. J. Cryo-electron microscopy reveals native polymeric cell wall structure in Bacillus subtilis 168 and the existence of a periplasmic space. Mol. Microbiol 56, 240-251 (2005).
37. Kürner, Frangakis & Baumeister, W. Cryo-electron tomography reveals the cytoskeletal structure of Spiroplasma melliferum. Science 307, 436-438 (2005).
38. Murphy, G. E., Leadbetter, J. R. & Jensen, G. J. In situ structure of the complete Treponema primitia flagellar motor. Nature 442, 1062-1064 (2006).
39. Baumeister, W., Grimm, R. & Walz, J. Electron tomography of molecules and cells. Trends Cell Biol. 9, 81-85 (1999).
40. Brandt, F. et al. The native 3D organization of bacterial polysomes. Cell 136, 261-271 (2009).
41. Seybert, A., Herrmann, R. & Frangakis, A. S. Structural analysis of Mycoplasma pneumoniae by cryo-electron tomography. J. Struct. Biol. 156, 342-354 (2006).
42. Li, Z., Trimble, M. J., Brun, Y. V. & Jensen, G. J. The structure of FtsZ filaments in vivo suggests a forcegenerating role in cell division. EMBO J. 26, 4694-4708 (2007).
43. Scheffel, A. et al. An acidic protein aligns magnetosomes along a filamentous structure in magnetotactic bacteria. Nature 440, 110-114 (2006).
44. Briegel, A. et al. Location and architecture of the Caulobacter crescentus chemoreceptor array. Mol. Microbiol. 69, 30-41 (2008).
45. Khursigara, C. M., Wu, X. & Subramaniam, S. Chemoreceptors in Caulobacter crescentus: Trimers of receptor dimers in a partially ordered hexagonally packed array. J. Bacteriol. 190, 6805-6810 (2008).
46. Comolli, L. R., Kundmann, M. & Downing, K. H. Characterization of intact subcellular bodies in whole bacteria by cryo-electron tomography and spectroscopic imaging. J. Microsc. 223, 40-52 (2006).
47. Glaeser, R. M. Limitations to significant information in biological electron microscopy as a result of radiation damage. J. Ultrastruct. Res. 36, 466-482 (1971).
48. Best, C., Nickell, S. & Baumeister, W. Localization of protein complexes by pattern recognition. Methods Cell Biol. 79, 615-638 (2007).
49. Bohm, J. et al. Toward detecting and identifying macromolecules in a cellular context: Template matching applied to electron tomograms. Proc. Natl Acad. Sci. USA 97, 14245-14250 (2000).
50. Diestra, E., Fontana, J., Guichard, P., Marco, S. & Risco, C. Visualization of proteins in intact cells with a clonable tag for electron microscopy. J. Struct. Biol. 165, 157-168 (2009).
51. Mercogliano, C. P. & DeRosier, D. J. Concatenated metallothionein as a clonable gold label for electron microscopy. J. Struct. Biol. 160, 70-82 (2007).
52. Leapman, R. D. Novel techniques in electron microscopy. Curr. Opin. Neurobiol. 14, 591-598 (2004).
53. Sousa, A. A. et al. On the feasibility of visualizing ultrasmall gold labels in biological specimens by STEM tomography. J. Struct. Biol. 159, 507-522 (2007).
54. Gaietta, G. M. et al. Golgi twins in late mitosis revealed by genetically encoded tags for live cell imaging and correlated electron microscopy. Proc. Natl Acad. Sci. USA 103, 17777-17782 (2006).
55. Sartori, A. et al. Correlative microscopy: Bridging the gap between fluorescence light microscopy and cryo-electron tomography. J. Struct. Biol. 160, 135-145 (2007).
56. Schwartz, C. L., Sarbash, V. I., Ataullakhanov, F. I., McIntosh, J. R. & Nicastro, D. Cryo-fluorescence microscopy facilitates correlations between light and cryo-electron microscopy and reduces the rate of photobleaching. J. Microsc. 227, 98-109 (2007).
57. Parkinson, D. Y., McDermott, G., Etkin, L. D., Le Gros, M. A. & Larabell, C. A. Quantitative 3-D imaging of eukaryotic cells using soft X-ray tomography. J. Struct. Biol. 162, 380-386 (2008).
58. Bonfigli, F. et al. High-resolution water window X-ray imaging of in vivo cells and their products using LiF crystal detectors. Microsc. Res. Tech. 71, 35-41 (2008).
59. Adam, J.-F., Moy, J.-P. & Susini, J. Table-top water window transmission x-ray microscopy: Review of the key issues, and conceptual design of an instrument for biology. Rev. Sci. Instrum. 76, 091301 (2005).
60. Miao, J. et al. Imaging whole Escherichia coli bacteria by using single-particle x-ray diffraction. Proc. Natl Acad. Sci. USA 100, 110-112 (2003).
61. Sandberg, R. L. et al. High numerical aperture tabletop soft x-ray diffraction microscopy with 70-nm resolution. Proc. Natl Acad. Sci. USA 105, 24-27 (2008).
62. 2 nanoparticles as a soft X-ray molecular probe. Chem. Commun. (Camb.), 2471-2473 (2008).
63. Grimm, R., Typke, D., Bärmann, M. & Baumeister, W. Determination of the inelastic mean free path in ice by examination of tilted vesicles and automated most probable loss imaging. Ultramicroscopy 63 169-179 (1996).
64. Heymann, J. A. W. et al. 3D Imaging of mammalian cells with ion-abrasion scanning electron microscopy. J. Struct. Biol. 166 1-7 (2008).
65. Heymann, J. A. W. et al. Site-specific 3D imaging of cells and tissues with a dual beam microscope. J. Struct. Biol. 155, 63-73 (2006).
66. Marko, M., Hsieh, C., Schalek, R., Frank, J. & Mannella, C. Focused-ion-beam thinning of frozen-hydrated biological specimens for cryo-electron microscopy. Nature Methods 4, 215-217 (2007).
67. Matias, V. R. & Beveridge, T. J. Native cell wall organization shown by cryo-electron microscopy confirms the existence of a periplasmic space in Staphylococcus aureus. J. Bacteriol. 188, 1011-1021 (2006).
68. Zuber, B. et al. Granular layer in the periplasmic space of gram-positive bacteria and fine structures of Enterococcus gallinarum and Streptococcus gordonii septa revealed by cryo-electron microscopy of vitreous sections. J. Bacteriol. 188, 6652-6660 (2006).
69. Matias, V. R. F., Al-Amoudi, A., Dubochet, J. & Beveridge, T. J. Cryo-transmission electron microscopy of frozen-hydrated sections of Escherichia coli and Pseudomonas aeruginosa. J. Bacteriol. 185, 6112-6118 (2003).
70. Matias, V. R. F. & Beveridge, T. J. Cryo-electron microscopy of cell division in Staphylococcus aureus reveals a mid-zone between nascent cross walls. Mol. Microbiol. 64, 195-206 (2007).
71. Matias, V. R. F. & Beveridge, T. J. Lipoteichoic acid is a major component of the Bacillus subtilis periplasm. J. Bacteriol. 190, 7414-7418 (2008).
72. Zhang, P. et al. Direct visualization of receptor arrays in frozen-hydrated sections and plunge-frozen specimens of E. coli engineered to overproduce the chemotaxis receptor Tsr. J. Microsc. 216, 76-83 (2004).
73. Zuber, B. et al. Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J. Bacteriol. 190, 5672-5680 (2008).
74. Eltsov, M. & Dubochet, J. Fine structure of the Deinococcus radiodurans nucleoid revealed by cryoelectron microscopy of vitreous sections. J. Bacteriol. 187, 8047-8054 (2005).
75. Salje, J., Zuber, B. & Löwe, J. Electron. Cryomicroscopy of E. coli reveals filament bundles involved in plasmid DNA segregation. Science 323, 509-512 (2008).
76. Sartori, N., Richter, K. & Dubochet, J. Vitrification depth can be increased more than 10-fold by high pressure freezing. J. Microsc. 172, 55-61 (1993).
77. Studer, D., Graber, W., Al-Amoudi, A. & Eggli, P. A new approach for cryofixation by high-pressure freezing. J. Microsc. 203, 285-294 (2001).
78. Peters, P. J. & Hunziker, W. Subcellular localization of Rab17 by cryo-immunogold electron microscopy in epithelial cells grown on polycarbonate filters. Methods Enzymol. 329, 210-225 (2001).
79. Trachtenberg, S. et al. Structure of the cytoskeleton of Spiroplasma melliferum BC3 and its interactions with the cell membrane. J. Mol. Biol. 378, 778-789 (2008).
80. van Niftrik, L. et al. Combined structural and chemical analysis of the anammoxosome: A membrane-bounded intracytoplasmic compartment in anammox bacteria. J. Struct. Biol. 161, 401-410 (2008).
81. Lefman, J. et al. Three-dimensional electron microscopic imaging of membrane invaginations in Escherichia coli overproducing the chemotaxis receptor Tsr. J. Bacteriol. 186, 5052-5061 (2004).
82. van de Meene, A. M. L., Hohmann-Marriott, M. F., Vermaas, W. F. J. & Roberson, R. W. The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803. Arch. Microbiol 184, 259-270 (2006).
83. Subramaniam, S., Bartesaghi, A., Liu, J., Bennett, A. E. & Sougrat, R. Electron. tomography of viruses. Curr. Opin. Struct. Biol. 17 596-602 (2007).
84. Bartesaghi, A. et al. Classification and 3D averaging with missing wedge correction in biological electron tomography. J. Struct. Biol. 162, 436-450 (2008).
85. Förster, F., Pruggnaller, S., Seybert, A. & Frangakis, A. S. Classification of cryo-electron sub-tomograms using constrained correlation. J. Struct. Biol. 161, 276-286 (2008).
86. Ortiz, J. O., Förster, F., Kürner, J., Linaroudis, A. A. & Baumeister, W. Mapping 70S ribosomes in intact cells by cryoelectron tomography and pattern recognition. J. Struct. Biol. 156, 334-341 (2006).
87. Khursigara, C. M., Wu, X., Zhang, P., Lefman, J. & Subramaniam, S. Role of HAMP domains in chemotaxis signaling by bacterial chemoreceptors. Proc. Natl Acad. Sci. USA 105, 16555-16560 (2008).
88. Freudiger, C. W. et al. Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy. Science 322, 1857-1861 (2008).
89. Al-Amoudi, A. et al. Cryo-electron microscopy of vitreous sections. EMBO J. 23, 3583-3588 (2004).
90. Lieber, A., Leis, A., Kushmaro, A., Minsky, A. & Medalia, O. Chromatin organization and radio-resistance in the bacterium Gemmata obscuriglobus. J. Bacteriol. 191, 1439-1445 (2009).
91. Eltsov M. & Zuber B. Transmission electron microscopy of the bacterial nucleoid. J. Struct. Biol. 156, 246-254 (2006).