Comparative cryo-electron tomography of pathogenic Lyme disease spirochetes

Molecular Microbiology

Volumn 71, Issue 6, 2009, Pages 1415-1434

  Kudryashev, Mikhail ^a   Cyrklaff, Marek ^a,b   Baumeister, Wolfgang ^b   Simon, Markus M ^c   Wallich, Reinhard ^a   Frischknecht, Friedrich ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BORRELIA AFZELII; BORRELIA BURGDORFERI; BORRELIA GARINII; BORRELIA INFECTION; COMPARATIVE STUDY; CRYOELECTRON TOMOGRAPHY; CYTOPLASM; FLAGELLUM; LYME DISEASE; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; SPIROCHETE; TOMOGRAPHY;

BORRELIA BURGDORFERI GROUP; CRYOELECTRON MICROSCOPY; CYTOSKELETON; ELECTRON MICROSCOPE TOMOGRAPHY; FLAGELLA; IMAGE PROCESSING, COMPUTER-ASSISTED; PERIPLASM;

BORRELIA; BORRELIA AFZELII; BORRELIA BURGDORFERI; BORRELIA BURGDORFERI GROUP; BORRELIA GARINII; BORRELIA HERMSII; TREPONEMA;

EID: 62449236570     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06613.x     Document Type: Article

References (95)

1. Barbour, A.G. Hayes, S.F. (1986) Biology of Borrelia species. Microbiol Rev 50 : 381 400.
2. Breznak, J.A. Switzer, J.M. (1986) Acetate synthesis from H(2) plus CO(2) by termite gut microbes. Appl Environ Microbiol 52 : 623 630.
3. Burgdorfer, W., Barbour, A.G., Hayes, S.F., Benach, J.L., Grunwaldt, E. Davis, J.P. (1982) Lyme disease - a tick-borne spirochetosis? Science 216 : 1317 1319.
4. Charon, N.W. Goldstein, S.F. (2002) Genetics of motility and chemotaxis of a fascinating group of bacteria: the spirochetes. Annu Rev Genet 36 : 47 73.
5. Charon, N.W., Goldstein, S.F., Block, S.M., Curci, K., Ruby, J.D., Kreiling, J.A. Limberger, R.J. (1992) Morphology and dynamics of protruding spirochete periplasmic flagella. J Bacteriol 174 : 832 840.
6. Ciofu, O., Beveridge, T.J., Kadurugamuwa, J., Walther-Rasmussen, J. Hoiby, N. (2000) Chromosomal beta-lactamase is packaged into membrane vesicles and secreted from Pseudomonas aeruginosa. J Antimicrob Chemother 45 : 9 13.
7. Cox, D.L., Akins, D.R., Bourell, K.W., Lahdenne, P., Norgard, M.V. Radolf, J.D. (1996) Limited surface exposure of Borrelia burgdorferi outer surface lipoproteins. Proc Natl Acad Sci USA 93 : 7973 7978.
8. Cullen, P.A., Haake, D.A. Adler, B. (2004) Outer membrane proteins of pathogenic spirochetes. FEMS Microbiol Rev 28 : 291 318.
9. Cyrklaff, M., Kudryashev, M., Leis, A., Leonard, K., Baumeister, W., Menard, R., et al. (2007) Cryoelectron tomography reveals periodic material at the inner side of subpellicular microtubules in apicomplexan parasites. J Exp Med 204 : 1281 1287.
10. Daniel, R.A. Errington, J. (2003) Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113 : 767 776.
11. Defeu Soufo, H.J. Graumann, P.L. (2004) Dynamic movement of actin-like proteins within bacterial cells. EMBO Rep 5 : 789 794.
12. Divakaruni, A.V., Baida, C., White, C.L. Gober, J.W. (2007) The cell shape proteins MreB and MreC control cell morphogenesis by positioning cell wall synthetic complexes. Mol Microbiol 66 : 174 188.
13. Dorward, D.W., Garon, C.F. Judd, R.C. (1989) Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae. J Bacteriol 171 : 2499 2505.
14. Dorward, D.W., Schwan, T.G. Garon, C.F. (1991) Immune capture and detection of Borrelia burgdorferi antigens in urine, blood, or tissues from infected ticks, mice, dogs, and humans. J Clin Microbiol 29 : 1162 1170.
15. Dubochet, J., Adrian, M., Chang, J.J., Homo, J.C., Lepault, J., McDowall, A.W. Schultz, P. (1988) Cryo-electron microscopy of vitrified specimens. Q Rev Biophys 21 : 129 228.
16. Dubytska, L., Godfrey, H.P. Cabello, F.C. (2006) Borrelia burgdorferi ftsZ plays a role in cell division. J Bacteriol 188 : 1969 1978.
17. van den Ent, F., Amos, L.A. Lowe, J. (2001) Prokaryotic origin of the actin cytoskeleton. Nature 413 : 39 44.
18. Erickson, H.P. (2007) Evolution of the cytoskeleton. Bioessays 29 : 668 677.
19. Figge, R.M., Divakaruni, A.V. Gober, J.W. (2004) MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol Microbiol 51 : 1321 1332.
20. Frangakis, A.S. Hegerl, R. (2001) Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. J Struct Biol 135 : 239 250.
21. Frischknecht, F. Way, M. (2001) Surfing pathogens and the lessons learned for actin polymerization. Trends Cell Biol 11 : 30 38.
22. Fuchs, H., Wallich, R., Simon, M.M. Kramer, M.D. (1994) The outer surface protein A of the spirochete Borrelia burgdorferi is a plasmin (ogen) receptor. Proc Natl Acad Sci USA 91 : 12594 12598.
23. Garon, C.F., Dorward, D.W. Corwin, M.D. (1989) Structural features of Borrelia burgdorferi- the Lyme disease spirochete: silver staining for nucleic acids. Scanning Microsc Suppl 3 : 109 115.
24. Garvalov, B.K., Zuber, B., Bouchet-Marquis, C., Kudryashev, M., Gruska, M., Beck, M., et al. (2006) Luminal particles within cellular microtubules. J Cell Biol 174 : 759 765.
25. Ge, Y., Li, C., Corum, L., Slaughter, C.A. Charon, N.W. (1998) Structure and expression of the FlaA periplasmic flagellar protein of Borrelia burgdorferi. J Bacteriol 180 : 2418 2425.
26. Goldstein, S.F., Charon, N.W. Kreiling, J.A. (1994) Borrelia burgdorferi swims with a planar waveform similar to that of eukaryotic flagella. Proc Natl Acad Sci USA 91 : 3433 3437.
27. Goldstein, S.F., Buttle, K.F. Charon, N.W. (1996) Structural analysis of the Leptospiraceae and Borrelia burgdorferi by high-voltage electron microscopy. J Bacteriol 178 : 6539 6545.
28. Gouin, E., Welch, M.D. Cossart, P. (2005) Actin-based motility of intracellular pathogens. Curr Opin Microbiol 8 : 35 45.
29. Graumann, P.L. (2007) Cytoskeletal elements in bacteria. Annu Rev Microbiol 61 : 589 618.
30. Grunewald, K. Cyrklaff, M. (2006) Structure of complex viruses and virus-infected cells by electron cryo tomography. Curr Opin Microbiol 9 : 437 442.
31. Hammer, B., Moter, A., Kahl, O., Alberti, G. Gobel, U.B. (2001) Visualization of Borrelia burgdorferi sensu lato by fluorescence in situ hybridization (FISH) on whole-body sections of Ixodes ricinus ticks and gerbil skin biopsies. Microbiology 147 : 1425 1436.
32. Haupt, K., Kraiczy, P., Wallich, R., Brade, V., Skerka, C. Zipfel, P.F. (2007) Binding of human factor H-related protein 1 to serum-resistant Borrelia burgdorferi is mediated by borrelial complement regulator-acquiring surface proteins. J Infect Dis 196 : 124 133.
33. Hayashi, J., Hamada, N. Kuramitsu, H.K. (2002) The autolysin of Porphyromonas gingivalis is involved in outer membrane vesicle release. FEMS Microbiol Lett 216 : 217 222.
34. Hayes, S.F. Burgdorfer, W. (1993) Ultrastructure of Borrelia burgdorferi. In Aspects of Lyme Borreliosis. Weber, K. Burgdorfer, W. (eds). Berlin : Springer, pp. 29 43.
35. Hefty, P.S., Jolliff, S.E., Caimano, M.J., Wikel, S.K. Akins, D.R. (2002) Changes in temporal and spatial patterns of outer surface lipoprotein expression generate population heterogeneity and antigenic diversity in the Lyme disease spirochete, Borrelia burgdorferi. Infect Immun 70 : 3468 3478.
36. Hegerl, R. (1996) The EM program package: a platform for image processing in biological electron microscopy. J Struct Biol 116 : 30 34.
37. Henderson, G.P., Gan, L. Jensen, G.J. (2007) 3-D ultrastructure of O. tauri: electron cryotomography of an entire eukaryotic cell. PloS ONE 2 : e749.
38. Hoffmann, C., Leis, A., Niederweis, M., Plitzko, J.M. Engelhardt, H. (2008) 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.
39. Holt, S.C. (1978) Anatomy and chemistry of spirochetes. Microbiol Rev 42 : 114 160.
40. Holt, S.C. Ebersole, J.L. (2006) The oral spirochetes: their ecology and role in the pathogenesis of periodontal disease. In Pathogenic Treponema. Molecular and Cellular Biology, Vol. 1. Radolf, J.D. Lukenhart, S.A. (eds). Wymondham : Caister Academic Press, pp. 323 365.
41. Hovind-Hougen, K. (1976) Treponema and Borrelia morphology. In The Biology of Parasitic Spriochetes. Johnson, R.C. (ed.). New York : Academic Press, pp. 7 18.
42. Hovind-Hougen, K. (1984) Ultrastructure of spirochetes isolated from Ixodes ricinus and Ixodes dammini. Yale J Biol Med 57 : 543 548.
43. Izard, J. (2006) Cytoskeletal cytoplasmic filament ribbon of Treponema: a member of an intermediate-like filament protein family. J Mol Microbiol Biotechnol 11 : 159 166.
44. Izard, J. Limberger, R. (2006) Structural and genomic features of treponemal architecture. In Pathogenic Treponema. Molecular and Cellular Biology, Vol. 1. Radolf, J.D. Lukenhart, S.A. (eds). Wymondham : Caister Academic Press, pp. 39 60.
45. Izard, J., Samsonoff, W.A., Kinoshita, M.B. Limberger, R.J. (1999) Genetic and structural analyses of cytoplasmic filaments of wild-type Treponema phagedenis and a flagellar filament-deficient mutant. J Bacteriol 181 : 6739 6746.
46. Izard, J., Hsieh, C.E., Limberger, R.J., Mannella, C.A. Marko, M. (2008) Native cellular architecture of Treponema denticola revealed by cryo-electron tomography. J Struct Biol 163 : 10 17.
47. Jensen, G.J. Briegel, A. (2007) How electron cryotomography is opening a new window onto prokaryotic ultrastructure. Curr Opin Struct Biol 17 : 260 267.
48. Johnson, R.C., Hyde, F.W. Rumpel, C.M. (1984) Taxonomy of the Lyme disease spirochetes. Yale J Biol Med 57 : 529 537.
49. Joseph, R., Holt, S.C. Canale-Parola, E. (1973) Peptidoglycan of free-living anaerobic spirochetes. J Bacteriol 115 : 426 435.
50. Kraiczy, P., Hellwage, J., Skerka, C., Becker, H., Kirschfink, M., Simon, M.M., et al. (2004) Complement resistance of Borrelia burgdorferi correlates with the expression of BbCRASP-1, a novel linear plasmid-encoded surface protein that interacts with human factor H and FHL-1 and is unrelated to Erp proteins. J Biol Chem 279 : 2421 2429.
51. Kuehn, M.J. Kesty, N.C. (2005) Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev 19 : 2645 2655.
52. Lambrechts, A., Gevaert, K., Cossart, P., Vandekerckhove, J. Van Troys, M. (2008) Listeria comet tails: the actin-based motility machinery at work. Trends Cell Biol 18 : 220 227.
53. Li, C., Corum, L., Morgan, D., Rosey, E.L., Stanton, T.B. Charon, N.W. (2000) The spirochete FlaA periplasmic flagellar sheath protein impacts flagellar helicity. J Bacteriol 182 : 6698 6706.
54. Li, Z., Trimble, M.J., Brun, Y.V. Jensen, G.J. (2007) The structure of FtsZ filaments in vivo suggests a force-generating role in cell division. EMBO J 26 : 4694 4708.
55. Limberger, R.J. (2004) The periplasmic flagellum of spirochetes. J Mol Microbiol Biotechnol 7 : 30 40.
56. Lowe, J. Amos, L.A. (1998) Crystal structure of the bacterial cell-division protein FtsZ. Nature 391 : 203 206.
57. 2+-induced FtsZ sheets. EMBO J 18 : 2364 2371.
58. Lucic, V., Forster, F. Baumeister, W. (2005) Structural studies by electron tomography: from cells to molecules. Annu Rev Biochem 74 : 833 865.
59. Ma, X., Ehrhardt, D.W. Margolin, W. (1996) Colocalization of cell division proteins FtsZ and FtsA to cytoskeletal structures in living Escherichia coli cells by using green fluorescent protein. Proc Natl Acad Sci USA 93 : 12998 13003.
60. MacDonald, A.B. (2006) A life cycle for Borrelia spirochetes? Med Hypotheses 67 : 810 818.
61. McDowell, J.V., Sung, S.Y., Hu, L.T. Marconi, R.T. (2002) Evidence that the variable regions of the central domain of VlsE are antigenic during infection with lyme disease spirochetes. Infect Immun 70 : 4196 4203.
62. Margolin, W. (2005) FtsZ and the division of prokaryotic cells and organelles. Nat Rev Mol Cell Biol 6 : 862 871.
63. Margolin, W. Bernander, R. (2004) How do prokaryotic cells cycle? Curr Biol 14 : R768 R770.
64. Mashburn-Warren, L.M. Whiteley, M. (2006) Special delivery: vesicle trafficking in prokaryotes. Mol Microbiol 61 : 839 846.
65. Mathiesen, M.J., Holm, A., Christiansen, M., Blom, J., Hansen, K., Ostergaard, S. Theisen, M. (1998) The dominant epitope of Borrelia garinii outer surface protein C recognized by sera from patients with neuroborreliosis has a surface-exposed conserved structural motif. Infect Immun 66 : 4073 4079.
66. Medalia, O., Weber, I., Frangakis, A.S., Nicastro, D., Gerisch, G. Baumeister, W. (2002) Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography. Science 298 : 1209 1213.
67. Michie, K.A. Lowe, J. (2006) Dynamic filaments of the bacterial cytoskeleton. Annu Rev Biochem 75 : 467 492.
68. Mogilner, A. (2006) On the edge: modeling protrusion. Curr Opin Cell Biol 18 : 32 39.
69. Motaleb, M.A., Corum, L., Bono, J.L., Elias, A.F., Rosa, P., Samuels, D.S. Charon, N.W. (2000) Borrelia burgdorferi periplasmic flagella have both skeletal and motility functions. Proc Natl Acad Sci USA 97 : 10899 10904.
70. Murphy, G.E., Leadbetter, J.R. Jensen, G.J. (2006) In situ structure of the complete Treponema primitia flagellar motor. Nature 442 : 1062 1064.
71. Murphy, G.E., Matson, E.G., Leadbetter, J.R., Berg, H.C. Jensen, G.J. (2008) Novel ultrastructures of Treponema primitia and their implications for motility. Mol Microbiol 67 : 1184 1195.
72. Namba, K., Yamashita, I. Vonderviszt, F. (1989) Structure of the core and central channel of bacterial flagella. Nature 342 : 648 654.
73. Nickell, S., Forster, F., Linaroudis, A., Net, W.D., Beck, F., Hegerl, R., et al. (2005) TOM software toolbox: acquisition and analysis for electron tomography. J Struct Biol 149 : 227 234.
74. Norris, S.J. (2006) Antigenic variation with a twist - the Borrelia story. Mol Microbiol 60 : 1319 1322.
75. Pogliano, J. (2008) The bacterial cytoskeleton. Curr Opin Cell Biol 20 : 19 27.
76. Radolf, J.D., Bourell, K.W., Akins, D.R., Brusca, J.S. Norgard, M.V. (1994) Analysis of Borrelia burgdorferi membrane architecture by freeze-fracture electron microscopy. J Bacteriol 176 : 21 31.
77. Roberts, D.M., Theisen, M. Marconi, R.T. (2000) Analysis of the cellular localization of Bdr paralogs in Borrelia burgdorferi, a causative agent of lyme disease: evidence for functional diversity. J Bacteriol 182 : 4222 4226.
78. Salkinoja-Salonen, M. Nurmiaho, E.L. (1978) The effect of lipopolysaccharide composition on the ultrastructure of Pseudomonas aeruginosa. J Gen Microbiol 105 : 23 28.
79. Schroder, N.W., Eckert, J., Stubs, G. Schumann, R.R. (2008) Immune responses induced by spirochetal outer membrane lipoproteins and glycolipids. Immunobiology 213 : 329 340.
80. Shih, Y.L. Rothfield, L. (2006) The bacterial cytoskeleton. Microbiol Mol Biol Rev 70 : 729 754.
81. Skare, J.T., Shang, E.S., Foley, D.M., Blanco, D.R., Champion, C.I., Mirzabekov, T., et al. (1995) Virulent strain associated outer membrane proteins of Borrelia burgdorferi. J Clin Invest 96 : 2380 2392.
82. Smit, J., Kamio, Y. Nikaido, H. (1975) Outer membrane of Salmonella typhimurium: chemical analysis and freeze-fracture studies with lipopolysaccharide mutants. J Bacteriol 124 : 942 958.
83. Steere, A.C. (2001) Lyme disease. N Engl J Med 345 : 115 125.
84. Takayama, K., Rothenberg, R.J. Barbour, A.G. (1987) Absence of lipopolysaccharide in the Lyme disease spirochete, Borrelia burgdorferi. Infect Immun 55 : 2311 2313.
85. Thanedar, S. Margolin, W. (2004) FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr Biol 14 : 1167 1173.
86. Tilney, L.G. Portnoy, D.A. (1989) Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol 109 : 1597 1608.
87. Wachi, M., Doi, M., Tamaki, S., Park, W., Nakajima-Iijima, S. Matsuhashi, M. (1987) Mutant isolation and molecular cloning of mre genes, which determine cell shape, sensitivity to mecillinam, and amount of penicillin-binding proteins in Escherichia coli. J Bacteriol 169 : 4935 4940.
88. Wai, S.N., Lindmark, B., Soderblom, T., Takade, A., Westermark, M., Oscarsson, J., et al. (2003) Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell 115 : 25 35.
89. Wallich, R., Pattathu, J., Kitiratschky, V., Brenner, C., Zipfel, P.F., Brade, V., et al. (2005) Identification and functional characterization of complement regulator-acquiring surface protein 1 of the Lyme disease spirochetes Borrelia afzelii and Borrelia garinii. Infect Immun 73 : 2351 2359.
90. Weiss, D.S. (2004) Bacterial cell division and the septal ring. Mol Microbiol 54 : 588 597.
91. Wensink, J. Witholt, B. (1981) Identification of different forms of the murein-bound lipoprotein found in isolated outer membranes of Escherichia coli. Eur J Biochem 113 : 349 357.
92. Yang, X., Li, Y., Dunn, J.J. Luft, B.J. (2006) Characterization of a unique borreliacidal epitope on the outer surface protein C of Borrelia burgdorferi. FEMS Immunol Med Microbiol 48 : 64 74.
93. Yonekura, K., Maki, S., Morgan, D.G., DeRosier, D.J., Vonderviszt, F., Imada, K. Namba, K. (2000) The bacterial flagellar cap as the rotary promoter of flagellin self-assembly. Science 290 : 2148 2152.
94. Zhou, L., Srisatjaluk, R., Justus, D.E. Doyle, R.J. (1998) On the origin of membrane vesicles in gram-negative bacteria. FEMS Microbiol Lett 163 : 223 228.
95. Zuber, B., Chami, M., Houssin, C., Dubochet, J., Griffiths, G. Daffe, M. (2008) Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J Bacteriol 190 : 5672 5680.