Three-dimensional structures of pathogenic and saprophytic leptospira species revealed by cryo-electron tomography

Journal of Bacteriology

Volumn 194, Issue 6, 2012, Pages 1299-1306

  Raddi, Gianmarco ^a   Morado, Dustin R ^a   Yan, Jie ^c   Haake, David A ^d,e   Yang, X Frank ^b   Liu, Jun ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^d VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE;

ARTICLE; BACTERIAL MEMBRANE; BACTERIUM CULTURE; CELL STRUCTURE; CHEMORECEPTOR; CYTOPLASM; DNA PACKAGING; ELECTRON TOMOGRAPHY; FLAGELLUM; LEPTOSPIRA; LEPTOSPIRA BIFLEXA; LEPTOSPIRA INTERROGANS; NONHUMAN; PRIORITY JOURNAL;

CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; FLAGELLA; IMAGING, THREE-DIMENSIONAL; LEPTOSPIRA; MACROMOLECULAR SUBSTANCES;

LEPTOSPIRA; LEPTOSPIRA BIFLEXA; LEPTOSPIRA INTERROGANS;

EID: 84863281646     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.06474-11     Document Type: Article

References (50)

1. Beck M, et al. 2009. Visual proteomics of the human pathogen Leptospira interrogans. Nat. Methods 6:817- 823.
2. Bharti AR, et al. 2003. Leptospirosis: a zoonotic disease of global importance. Lancet Infect. Dis. 3:757-771.
3. Bloomfield VA. 1996. DNA condensation. Curr. Opin. Struct. Biol. 6:334 -341.
4. Briegel A, et al. 2009. Universal architecture of bacterial chemoreceptor arrays. Proc. Natl. Acad. Sci. U. S. A. 106:17181-17186.
5. Bromley DB, Charon NW. 1979. Axial filament involvement in the motility of Leptospira interrogans. J. Bacteriol. 137:1406 -1412.
6. Bulach DM, et al. 2006. Genome reduction in Leptospira borgpetersenii reflects limited transmission potential. Proc. Natl. Acad. Sci. U. S. A. 103: 14560-14565.
7. Charon NW, et al. 2009. The flat-ribbon configuration of the periplasmic flagella of Borrelia burgdorferi and its relationship to motility and morphology. J. Bacteriol. 191:600-607.
8. Chen S, et al. 2011. Structural diversity of bacterial flagellar motors. EMBO J. 30:2972-2981.
9. Comolli LR, Kundmann M, Downing KH. 2006. Characterization of intact subcellular bodies in whole bacteria by cryo-electron tomography and spectroscopic imaging. J. Microsc. 223:40 -52.
10. Eltsov M, Dubochet J. 2005. Fine structure of the Deinococcus radiodurans nucleoid revealed by cryoelectron microscopy of vitreous sections. J. Bacteriol. 187:8047- 8054.
11. Goldstein SF, Charon NW. 1988. Motility of the spirochete Leptospira. Cell Motil. Cytoskeleton 9:101-110.
12. Haake DA, Matsunaga J. 2010. Leptospira: a spirochete with a hybrid outer membrane. Mol. Microbiol. 77:805- 814.
13. Hud NV, Vilfan ID. 2005. Toroidal DNA condensates: unraveling the fine structure and the role of nucleation in determining size. Annu. Rev. Biophys. Biomol. Struct. 34:295-318.
14. Izard J, Hsieh CE, Limberger RJ, Mannella CA, Marko M. 2008. Native cellular architecture of Treponema denticola revealed by cryo-electron tomography. J. Struct. Biol. 163:10 -17.
15. Izard J, et al. 2009. Cryo-electron tomography elucidates the molecular architecture of Treponema pallidum, the syphilis spirochete. J. Bacteriol. 191:7566 -7580.
16. Kennedy MJ, Rosey EL, Yancey RJ, Jr. 1997. Characterization of flaAand flaB- mutants of Serpulina hyodysenteriae: both flagellin subunits, FlaA and FlaB, are necessary for full motility and intestinal colonization. FEMS Microbiol. Lett. 153:119 -128.
17. Ko AI, Goarant C, Picardeau M. 2009. Leptospira: the dawn of the molecular genetics era for an emerging zoonotic pathogen. Nat. Rev. Microbiol. 7:736 -747.
18. Kremer JR, Mastronarde DN, McIntosh JR. 1996. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116:71-76.
19. Kudryashev M, et al. 2009. Comparative cryo-electron tomography of pathogenic Lyme disease spirochetes. Mol. Microbiol. 71:1415-1434.
20. Levett PN. 2001. Leptospirosis. Clin. Microbiol. Rev. 14:296 -326.
21. Levin-Zaidman S, et al. 2003. Ringlike structure of the Deinococcus radiodurans genome: a key to radioresistance? Science 299:254 -256.
22. Li L, Ojcius DM, Yan J. 2007. Comparison of invasion of fibroblasts and macrophages by high- and low-virulence Leptospira strains: colonization of the host-cell nucleus and induction of necrosis by the virulent strain. Arch. Microbiol. 188:591-598.
23. Li Z, Jensen GJ. 2009. Electron cryotomography: a new view into microbial ultrastructure. Curr. Opin. Microbiol. 12:333-340.
24. Liu J, et al. 2010. Cellular architecture of Treponema pallidum: novel flagellum, periplasmic cone, and cell envelope as revealed by cryo electron tomography. J. Mol. Biol. 403:546 -561.
25. Liu J, et al. 2009. Intact flagellar motor of Borrelia burgdorferi revealed by cryo-electron tomography: evidence for stator ring curvature and rotor/ C-ring assembly flexion. J. Bacteriol. 191:5026 -5036.
26. Lucic V, Forster F, Baumeister W. 2005. Structural studies by electron tomography: from cells to molecules. Annu. Rev. Biochem. 74:833- 865.
27. Macnab RM. 2003. How bacteria assemble flagella. Annu. Rev. Microbiol. 57:77-100.
28. Malmstrom J, et al. 2009. Proteome-wide cellular protein concentrations of the human pathogen Leptospira interrogans. Nature 460:762-765.
29. McBride AJ, Athanazio DA, Reis MG, Ko AI. 2005. Leptospirosis. Curr. Opin. Infect. Dis. 18:376 -386.
30. Milne JL, Subramaniam S. 2009. Cryo-electron tomography of bacteria: progress, challenges and future prospects. Nat. Rev. Microbiol. 7:666-675.
31. Motaleb MA, et al. 2000. Borrelia burgdorferi periplasmic flagella have both skeletal and motility functions. Proc. Natl. Acad. Sci. U. S. A. 97: 10899-10904.
32. Murphy GE, Leadbetter JR, Jensen GJ. 2006. In situ structure of the complete Treponema primitia flagellar motor. Nature 442:1062-1064.
33. Murphy GE, Matson EG, Leadbetter JR, Berg HC, Jensen GJ. 2008. Novel ultrastructures of Treponema primitia and their implications for motility. Mol. Microbiol. 67:1184 -1195.
34. Nahori MA, et al. 2005. Differential TLR recognition of leptospiral lipid A and lipopolysaccharide in murine and human cells. J. Immunol. 175: 6022-6031.
35. Nascimento AL, et al. 2004. Comparative genomics of two Leptospira interrogans serovars reveals novel insights into physiology and pathogenesis. J. Bacteriol. 186:2164 -2172.
36. Pallen MJ, Penn CW, Chaudhuri RR. 2005. Bacterial flagellar diversity in the post-genomic era. Trends Microbiol. 13:143-149.
37. Paster BJ, et al. 1991. Phylogenetic analysis of the spirochetes. J. Bacteriol. 173:6101- 6109.
38. Pettersen EF, et al. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612.
39. Picardeau M, Brenot A, Saint Girons I. 2001. First evidence for gene replacement in Leptospira spp. Inactivation of L. biflexa flaB results in non-motile mutants deficient in endoflagella. Mol. Microbiol. 40:189-199.
40. Picardeau M, et al. 2008. Genome sequence of the saprophyte Leptospira biflexa provides insights into the evolution of Leptospira and the pathogenesis of leptospirosis. PLoS One 3:e1607.
41. Reich Z, Wachtel EJ, Minsky A. 1994. Liquid-crystalline mesophases of plasmid DNA in bacteria. Science 264:1460 -1463.
42. Ren SX, et al. 2003. Unique physiological and pathogenic features of Leptospira interrogans revealed by whole-genome sequencing. Nature 422:888-893.
43. Sadziene A, Thomas DD, Bundoc VG, Holt SC, Barbour AG. 1991. A flagella-less mutant of Borrelia burgdorferi. Structural, molecular, and in vitro functional characterization. J. Clin. Invest. 88:82-92.
44. Swulius MT, et al. 2011. Long helical filaments are not seen encircling cells in electron cryotomograms of rod-shaped bacteria. Biochem. Biophys. Res. Commun. 407:650-655.
45. Tchamedeu Kameni AP, Couture-Tosi E, Saint-Girons I, Picardeau M. 2002. Inactivation of the spirochete recA gene results in a mutant with low viability and irregular nucleoid morphology. J. Bacteriol. 184:452- 458.
46. Wadhams GH, Armitage JP. 2004. Making sense of it all: bacterial chemotaxis. Nat. Rev. Mol. Cell Biol. 5:1024 -1037.
47. Werts C, et al. 2001. Leptospiral lipopolysaccharide activates cells through a TLR2-dependent mechanism. Nat. Immunol. 2:346 -352.
48. Winkler H, Taylor KA. 2006. Accurate marker-free alignment with simultaneous geometry determination and reconstruction of tilt series in electron tomography. Ultramicroscopy 106:240 -254.
49. Xue F, Yan J, Picardeau M. 2009. Evolution and pathogenesis of Leptospira spp.: lessons learned from the genomes. Microbes Infect. 11:328-333.
50. Yonekura K, Maki-Yonekura S, Homma M. 2011. Structure of the flagellar motor protein complex PomAB: implications for the torquegenerating conformation. J. Bacteriol. 193:3863-3870.