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. 1996 Nov;178(22):6539–6545. doi: 10.1128/jb.178.22.6539-6545.1996

Structural analysis of the Leptospiraceae and Borrelia burgdorferi by high-voltage electron microscopy.

S F Goldstein 1, K F Buttle 1, N W Charon 1
PMCID: PMC178540  PMID: 8932310

Abstract

Spirochetes are an evolutionary and structurally unique group of bacteria. Outermost is a membrane sheath (OS), and within this sheath are the protoplasmic cell cylinder (PC) and periplasmic flagella (PFs). The PFs are attached at each end of the PC and, depending on the species, may or may not overlap in the center of the cell. The precise location of the PFs within the spirochetal cells is unknown. The PFs could lie along the cell axis. Alternatively, the PFs could wrap around the PC in either a right- or a left-handed sense. To understand the factors that cause the PFs to influence cell shape and allow the cells to swim, we determined the precise location of the PFs in the Leptospiraceae (Leptonema illini) and Borrelia burgdorferi. Our approach was to use high-voltage electron microscopy and analyze the three-dimensional images obtained from thick sections of embedded cells. We found that a single PF in L. illini is located in a central channel 29 nm in diameter running along the helix axis of the right-handed PC. The presence of the PFs is associated with the end being hook shaped. The results obtained agree with the current model of Leptospiraceae motility. In B. burgdorferi, which forms a flattened wave, the relationship between the PFs and the PC is more complicated. A multistrand ridge 67 nm in diameter, which was shown to be composed of PFs by cross-sectional and mutant analysis, was found to extend along the entire length of the cell. We found that the PFs wrapped around the PC in a right-handed sense. However, the PFs formed a left-handed helix in space. The wavelength of the cell body and the helix pitch of the PFs were found to be identical (2.83 microm). The results obtained were used to propose a model of B. burgdorferi motility whereby backward-propagating waves, which gyrate counterclockwise as viewed from the back of the cell, are generated by the counterclockwise rotation of the internal PFs. Concomitant with this motion, the cell is believed to rotate clockwise about the body axis as shown for the Leptospiraceae.

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Selected References

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  1. Birch-Andersen A., Hovind Hougen K., Borg-Petersen C. Electron microscopy of Leptospira. 1. Leptospira strain Pomona. Acta Pathol Microbiol Scand B Microbiol Immunol. 1973 Dec;81(6):665–676. doi: 10.1111/j.1699-0463.1973.tb02258.x. [DOI] [PubMed] [Google Scholar]
  2. Bromley D. B., Charon N. W. Axial filament involvement in the motility of Leptospira interrogans. J Bacteriol. 1979 Mar;137(3):1406–1412. doi: 10.1128/jb.137.3.1406-1412.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Carleton O., Charon N. W., Allender P., O'Brien S. Helix handedness of Leptospira interrogans as determined by scanning electron microscopy. J Bacteriol. 1979 Mar;137(3):1413–1416. doi: 10.1128/jb.137.3.1413-1416.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Charon N. W., Daughtry G. R., McCuskey R. S., Franz G. N. Microcinematographic analysis of tethered Leptospira illini. J Bacteriol. 1984 Dec;160(3):1067–1073. doi: 10.1128/jb.160.3.1067-1073.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Charon N. W., Goldstein S. F., Block S. M., Curci K., Ruby J. D., Kreiling J. A., Limberger R. J. Morphology and dynamics of protruding spirochete periplasmic flagella. J Bacteriol. 1992 Feb;174(3):832–840. doi: 10.1128/jb.174.3.832-840.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Charon N. W., Goldstein S. F., Curci K., Limberger R. J. The bent-end morphology of Treponema phagedenis is associated with short, left-handed, periplasmic flagella. J Bacteriol. 1991 Aug;173(15):4820–4826. doi: 10.1128/jb.173.15.4820-4826.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Charon N. W., Greenberg E. P., Koopman M. B., Limberger R. J. Spirochete chemotaxis, motility, and the structure of the spirochetal periplasmic flagella. Res Microbiol. 1992 Jul-Aug;143(6):597–603. doi: 10.1016/0923-2508(92)90117-7. [DOI] [PubMed] [Google Scholar]
  8. Goldstein S. F., Charon N. W., Kreiling J. A. Borrelia burgdorferi swims with a planar waveform similar to that of eukaryotic flagella. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3433–3437. doi: 10.1073/pnas.91.8.3433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Goldstein S. F., Charon N. W. Motility of the spirochete Leptospira. Cell Motil Cytoskeleton. 1988;9(2):101–110. doi: 10.1002/cm.970090202. [DOI] [PubMed] [Google Scholar]
  10. Goldstein S. F., Charon N. W. Multiple-exposure photographic analysis of a motile spirochete. Proc Natl Acad Sci U S A. 1990 Jul;87(13):4895–4899. doi: 10.1073/pnas.87.13.4895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hayes S. F., Burgdorfer W., Barbour A. G. Bacteriophage in the Ixodes dammini spirochete, etiological agent of Lyme disease. J Bacteriol. 1983 Jun;154(3):1436–1439. doi: 10.1128/jb.154.3.1436-1439.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hechemy K. E., Samsonoff W. A., Harris H. L., McKee M. Adherence and entry of Borrelia burgdorferi in Vero cells. J Med Microbiol. 1992 Apr;36(4):229–238. doi: 10.1099/00222615-36-4-229. [DOI] [PubMed] [Google Scholar]
  13. Holt S. C. Anatomy and chemistry of spirochetes. Microbiol Rev. 1978 Mar;42(1):114–160. doi: 10.1128/mr.42.1.114-160.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hovind-Hougen K. Ultrastructure of spirochetes isolated from Ixodes ricinus and Ixodes dammini. Yale J Biol Med. 1984 Jul-Aug;57(4):543–548. [PMC free article] [PubMed] [Google Scholar]
  15. Li H., Ruby J., Charon N., Kuramitsu H. Gene inactivation in the oral spirochete Treponema denticola: construction of an flgE mutant. J Bacteriol. 1996 Jun;178(12):3664–3667. doi: 10.1128/jb.178.12.3664-3667.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Limberger R. J., Charon N. W. Treponema phagedenis has at least two proteins residing together on its periplasmic flagella. J Bacteriol. 1986 Apr;166(1):105–112. doi: 10.1128/jb.166.1.105-112.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Macnab R. M. Genetics and biogenesis of bacterial flagella. Annu Rev Genet. 1992;26:131–158. doi: 10.1146/annurev.ge.26.120192.001023. [DOI] [PubMed] [Google Scholar]
  18. Nauman R. K., Holt S. C., Cox C. D. Purification, ultrastructure, and composition of axial filaments from Leptospira. J Bacteriol. 1969 Apr;98(1):264–280. doi: 10.1128/jb.98.1.264-280.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Paster B. J., Canale-Parola E. Involvement of periplasmic fibrils in motility of spirochetes. J Bacteriol. 1980 Jan;141(1):359–364. doi: 10.1128/jb.141.1.359-364.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. RITCHIE A. E., ELLINGHAUSEN H. C. ELECTRON MICROSCOPY OF LEPTOSPIRES. I. ANATOMICAL FEATURES OF LEPTOSPIRA POMONA. J Bacteriol. 1965 Jan;89:223–233. doi: 10.1128/jb.89.1.223-233.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Sadziene A., Thomas D. D., Bundoc V. G., Holt S. C., Barbour A. G. A flagella-less mutant of Borrelia burgdorferi. Structural, molecular, and in vitro functional characterization. J Clin Invest. 1991 Jul;88(1):82–92. doi: 10.1172/JCI115308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Trueba G. A., Bolin C. A., Zuerner R. L. Characterization of the periplasmic flagellum proteins of Leptospira interrogans. J Bacteriol. 1992 Jul;174(14):4761–4768. doi: 10.1128/jb.174.14.4761-4768.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Woese C. R. Bacterial evolution. Microbiol Rev. 1987 Jun;51(2):221–271. doi: 10.1128/mr.51.2.221-271.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]

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