Electron cryotomography: a new view into microbial ultrastructure.

Electron cryotomography (ECT) is an emerging technology that allows thin samples such as small bacterial cells to be imaged in 3D in a nearly native state to 'molecular' (approximately 4nm) resolution. As such, ECT is beginning to deliver long-awaited insight into the positions and structures of cytoskeletal filaments, cell wall elements, motility machines, chemoreceptor arrays, internal compartments, and other ultrastructures. Here we briefly explain ECT, review its recent contributions to microbiology, and conclude with a discussion of future prospects.

[1]  M. Borgnia,et al.  Three-Dimensional Imaging of the Highly Bent Architecture of Bdellovibrio bacteriovorus by Using Cryo-Electron Tomography , 2008, Journal of bacteriology.

[2]  Shengdong Li,et al.  Future directions for camera systems in electron microscopy. , 2007, Methods in cell biology.

[3]  Florian Beck,et al.  Correlative microscopy: bridging the gap between fluorescence light microscopy and cryo-electron tomography. , 2007, Journal of structural biology.

[4]  Friedrich Förster,et al.  Computational exploration of structural information from cryo-electron tomograms. , 2004, Current opinion in structural biology.

[5]  Grant J. Jensen,et al.  Molecular organization of Gram-negative peptidoglycan , 2008, Proceedings of the National Academy of Sciences.

[6]  Xiongwu Wu,et al.  Role of HAMP domains in chemotaxis signaling by bacterial chemoreceptors , 2008, Proceedings of the National Academy of Sciences.

[7]  S. Subramaniam,et al.  Direct visualization of Escherichia coli chemotaxis receptor arrays using cryo-electron microscopy , 2007, Proceedings of the National Academy of Sciences.

[8]  J. Löwe,et al.  Electron Cryomicroscopy of E. coli Reveals Filament Bundles Involved in Plasmid DNA Segregation , 2009, Science.

[9]  Grant J Jensen,et al.  The structure of isolated Synechococcus strain WH8102 carboxysomes as revealed by electron cryotomography. , 2007, Journal of molecular biology.

[10]  Alexandros A. Linaroudis,et al.  Structural analysis of photosynthetic membranes by cryo-electron tomography of intact Rhodopseudomonas viridis cells. , 2008, Journal of structural biology.

[11]  V. Lučić,et al.  Structural studies by electron tomography: from cells to molecules. , 2005, Annual review of biochemistry.

[12]  H. Erickson,et al.  FtsZ, a tubulin homologue in prokaryote cell division. , 1997, Trends in cell biology.

[13]  G. Jensen,et al.  Haloquadratum walsbyi gen. nov., sp. nov., the square haloarchaeon of Walsby, isolated from saltern crystallizers in Australia and Spain. , 2007, International journal of systematic and evolutionary microbiology.

[14]  J. Dubochet,et al.  Cryo‐electron microscopy of vitreous sections , 2004, The EMBO journal.

[15]  R. Weis Inch by inch, row by row , 2006, Nature Structural &Molecular Biology.

[16]  Tobias Bonhoeffer,et al.  Multiscale imaging of neurons grown in culture: from light microscopy to cryo-electron tomography. , 2007, Journal of structural biology.

[17]  Michael Marko,et al.  Native cellular architecture of Treponema denticola revealed by cryo-electron tomography. , 2008, Journal of structural biology.

[18]  E. Bi,et al.  FtsZ ring structure associated with division in Escherichia coli , 1991, Nature.

[19]  Mark Ellisman,et al.  Applications of direct detection device in transmission electron microscopy. , 2008, Journal of structural biology.

[20]  J. Bono,et al.  Borrelia burgdorferi periplasmic flagella have both skeletal and motility functions. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Mark Horowitz,et al.  Markov random field based automatic image alignment for electron tomography. , 2007, Journal of structural biology.

[22]  J. McIntosh,et al.  Cryo‐fluorescence microscopy facilitates correlations between light and cryo‐electron microscopy and reduces the rate of photobleaching , 2007, Journal of microscopy.

[23]  H. Berg,et al.  How spirochetes may swim. , 1976, Journal of theoretical biology.

[24]  Grant J. Jensen,et al.  Magnetosomes Are Cell Membrane Invaginations Organized by the Actin-Like Protein MamK , 2006, Science.

[25]  Xiongwu Wu,et al.  Chemoreceptors in Caulobacter crescentus: Trimers of Receptor Dimers in a Partially Ordered Hexagonally Packed Array , 2008, Journal of bacteriology.

[26]  G. Murphy,et al.  In situ structure of the complete Treponema primitia flagellar motor , 2006, Nature.

[27]  J. Izard,et al.  Cytoplasmic Filament-Deficient Mutant ofTreponema denticola Has Pleiotropic Defects , 2001, Journal of bacteriology.

[28]  T. Yeates,et al.  Protein-based organelles in bacteria: carboxysomes and related microcompartments , 2008, Nature Reviews Microbiology.

[29]  C. Mannella,et al.  Cryo-Electron Tomography Reveals the Comparative Three-Dimensional Architecture of Prochlorococcus, a Globally Important Marine Cyanobacterium , 2007, Journal of bacteriology.

[30]  R. Wirth,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 , 2008, Archives of Microbiology.

[31]  Julio O. Ortiz,et al.  The Native 3D Organization of Bacterial Polysomes , 2009, Cell.

[32]  A. Frangakis,et al.  The molecular architecture of cadherins in native epidermal desmosomes , 2007, Nature.

[33]  A. Miyazawa,et al.  A genetically encoded metallothionein tag enabling efficient protein detection by electron microscopy. , 2007, Journal of electron microscopy.

[34]  G. Jensen,et al.  A Self-Associating Protein Critical for Chromosome Attachment, Division, and Polar Organization in Caulobacter , 2008, Cell.

[35]  J. Fontana,et al.  Visualization of proteins in intact cells with a clonable tag for electron microscopy. , 2009, Journal of structural biology.

[36]  K. Venkateswaran,et al.  Tetrasphaera remsis sp. nov., isolated from the Regenerative Enclosed Life Support Module Simulator (REMS) air system. , 2007, International journal of systematic and evolutionary microbiology.

[37]  Kenneth H Downing,et al.  Three-dimensional analysis of the structure and ecology of a novel, ultra-small archaeon , 2009, The ISME Journal.

[38]  L. Shapiro,et al.  A Polymeric Protein Anchors the Chromosomal Origin/ParB Complex at a Bacterial Cell Pole , 2008, Cell.

[39]  W. Baumeister,et al.  Electron tomography of ice-embedded prokaryotic cells. , 1998, Biophysical journal.

[40]  O. Medalia,et al.  Chromatin Organization and Radio Resistance in the Bacterium Gemmata obscuriglobus , 2008, Journal of bacteriology.

[41]  W. Chiu,et al.  Structure of Halothiobacillus neapolitanus carboxysomes by cryo-electron tomography. , 2006, Journal of molecular biology.

[42]  Anchi Cheng,et al.  Automated molecular microscopy: the new Leginon system. , 2005, Journal of structural biology.

[43]  M. Marko,et al.  The Flat-Ribbon Configuration of the Periplasmic Flagella of Borrelia burgdorferi and Its Relationship to Motility and Morphology , 2008, Journal of bacteriology.

[44]  S. Subramaniam,et al.  Cell Surface Filaments of the Gliding Bacterium Flavobacterium johnsoniae Revealed by Cryo-Electron Tomography , 2007, Journal of bacteriology.

[45]  G. Jensen,et al.  The structure of FtsZ filaments in vivo suggests a force‐generating role in cell division , 2007, The EMBO journal.

[46]  Andrew Leis,et al.  Disclosure of the mycobacterial outer membrane: Cryo-electron tomography and vitreous sections reveal the lipid bilayer structure , 2008, Proceedings of the National Academy of Sciences.

[47]  J. Pogliano The bacterial cytoskeleton. , 2008, Current opinion in cell biology.

[48]  Ariane Briegel,et al.  How electron cryotomography is opening a new window onto prokaryotic ultrastructure. , 2007, Current opinion in structural biology.

[49]  D. DeRosier,et al.  Concatenated metallothionein as a clonable gold label for electron microscopy. , 2007, Journal of structural biology.

[50]  R. B. Jensen,et al.  Location and architecture of the Caulobacter crescentus chemoreceptor array , 2008, Molecular microbiology.

[51]  Mohamed Chami,et al.  Direct Visualization of the Outer Membrane of Mycobacteria and Corynebacteria in Their Native State , 2008, Journal of bacteriology.

[52]  Jared R. Leadbetter,et al.  Novel ultrastructures of Treponema primitia and their implications for motility , 2008, Molecular microbiology.

[53]  R. Losick,et al.  Transcription factor Spo0A switches the localization of the cell division protein FtsZ from a medial to a bipolar pattern in Bacillus subtilis. , 1996, Genes & development.