1887

Microbiology Society logo

Volume 163, Issue 2

Editor's Choice Viscosity-dependent variations in the cell shape and swimming manner of Free

Abstract

Spirochaetes are spiral or flat-wave–shaped Gram-negative bacteria that have periplasmic flagella between the peptidoglycan layer and outer membrane. Rotation of the periplasmic flagella transforms the cell body shape periodically, allowing the cell to swim in aqueous environments. Because the virulence of motility-deficient mutants of pathogenic species is drastically attenuated, motility is thought to be an essential virulence factor in spirochaetes. However, it remains unknown how motility practically contributes to the infection process. We show here that the cell body configuration and motility of the zoonotic spirochaete changes depending on the viscosity of the medium. swim and reverse the swimming direction by transforming the cell body. Motility analysis showed that the frequency of cell shape transformation was increased by increasing the viscosity of the medium. The increased cell body transformation induced highly frequent reversal of the swimming direction. A simple kinetic model based on the experimental results shows that the viscosity-induced increase in reversal limits cell migration, resulting in the accumulation of cells in high-viscosity regions. This behaviour could facilitate the colonization of the spirochaete on host tissues covered with mucosa.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Leptospira , motility , spirochaete and viscosity
© 2017 The Authors
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000420
2017-02-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/micro/163/2/153.html?itemId=/content/journal/micro/10.1099/mic.0.000420&mimeType=html&fmt=ahah

References

  1. Li C, Motaleb A, Sal M, Goldstein SF, Charon NW. Spirochete periplasmic flagella and motility. J Mol Microbiol Biotechnol 2000; 2:345–354[PubMed]
     [Google Scholar]
  2. Picardeau M, Brenot A, Saint Girons I. First evidence for gene replacement in Leptospira spp. Inactivation of L. biflexa flaB results in non-motile mutants deficient in endoflagella. Mol Microbiol 2001; 40:189–199 [View Article][PubMed]
     [Google Scholar]
  3. Sultan SZ, Sekar P, Zhao X, Manne A, Liu J et al. Motor rotation is essential for the formation of the periplasmic flagellar ribbon, cellular morphology, and Borrelia burgdorferi persistence within Ixodes scapularis tick and murine hosts. Infect Immun 2015; 83:1765–1777 [View Article][PubMed]
     [Google Scholar]
  4. Rosey EL, Kennedy MJ, Yancey RJ. Dual flaA1 flaB1 mutant of Serpulina hyodysenteriae expressing periplasmic flagella is severely attenuated in a murine model of swine dysentery. Infect Immun 1996; 64:4154–4162[PubMed]
     [Google Scholar]
  5. Lambert A, Picardeau M, Haake DA, Sermswan RW, Srikram A et al. FlaA proteins in Leptospira interrogans are essential for motility and virulence but are not required for formation of the flagellum sheath. Infect Immun 2012; 80:2019–2025 [View Article][PubMed]
     [Google Scholar]
  6. Sultan SZ, Manne A, Stewart PE, Bestor A, Rosa PA et al. Motility is crucial for the infectious life cycle of Borrelia burgdorferi. Infect Immun 2013; 81:2012–2021 [View Article][PubMed]
     [Google Scholar]
  7. Trivett-Moore NL, Gilbert GL, Law CL, Trott DJ, Hampson DJ. Isolation of Serpulina pilosicoli from rectal biopsy specimens showing evidence of intestinal spirochetosis. J Clin Microbiol 1998; 36:261–265[PubMed]
     [Google Scholar]
  8. Kraaz W, Pettersson B, Thunberg U, Engstrand L, Fellström C. Brachyspira aalborgi infection diagnosed by culture and 16S ribosomal DNA sequencing using human colonic biopsy specimens. J Clin Microbiol 2000; 38:3555–3560[PubMed]
     [Google Scholar]
  9. Nakamura S, Adachi Y, Goto T, Magariyama Y. Improvement in motion efficiency of the spirochete Brachyspira pilosicoli in viscous environments. Biophys J 2006; 90:3019–3026 [View Article][PubMed]
     [Google Scholar]
  10. Ruby JD, Charon NW. Effect of temperature and viscosity on the motility of the spirochete Treponema denticola. FEMS Microbiol Lett 1998; 169:251–254[PubMed] [CrossRef]
     [Google Scholar]
  11. Kaiser GE, Doetsch RN. Enhanced translational motion of Leptospira in viscous environments. Nature 1975; 255:656–657 [View Article][PubMed]
     [Google Scholar]
  12. Takabe K, Nakamura S, Ashihara M, Kudo S. Effect of osmolarity and viscosity on the motility of pathogenic and saprophytic Leptospira. Microbiol Immunol 2013; 57:236–239 [View Article][PubMed]
     [Google Scholar]
  13. Adler B. Pathogenesis of leptospirosis: cellular and molecular aspects. Vet Microbiol 2014; 172:353–358 [View Article][PubMed]
     [Google Scholar]
  14. Bromley DB, Charon NW. Axial filament involvement in the motility of Leptospira interrogans. J Bacteriol 1979; 137:1406–1412[PubMed]
     [Google Scholar]
  15. Goldstein SF, Charon NW. Motility of the spirochete Leptospira. Cell Motil Cytoskeleton 1988; 9:101–110 [View Article][PubMed]
     [Google Scholar]
  16. Goldstein SF, Charon NW. Multiple-exposure photographic analysis of a motile spirochete. Proc Natl Acad Sci USA 1990; 87:4895–4899[PubMed] [CrossRef]
     [Google Scholar]
  17. Islam MS, Takabe K, Kudo S, Nakamura S. Analysis of the chemotactic behaviour of Leptospira using microscopic agar-drop assay. FEMS Microbiol Lett 2014; 356:39–44 [View Article][PubMed]
     [Google Scholar]
  18. Nakamura S, Leshansky A, Magariyama Y, Namba K, Kudo S. Direct measurement of helical cell motion of the spirochete Leptospira. Biophys J 2014; 106:47–54 [View Article][PubMed]
     [Google Scholar]
  19. Kan W, Wolgemuth CW. The shape and dynamics of the Leptospiraceae. Biophys J 2007; 93:54–61 [View Article][PubMed]
     [Google Scholar]
  20. Porter SL, Wadhams GH, Armitage JP. Signal processing in complex chemotaxis pathways. Nat Rev Microbiol 2011; 9:153–165 [View Article][PubMed]
     [Google Scholar]
  21. Fahrner KA, Ryu WS, Berg HC. Biomechanics: bacterial flagellar switching under load. Nature 2003; 423:938 [CrossRef]
     [Google Scholar]
  22. Yuan J, Fahrner KA, Berg HC. Switching of the bacterial flagellar motor near zero load. J Mol Biol 2009; 390:394–400 [View Article][PubMed]
     [Google Scholar]
  23. Bai F, Minamino T, Wu Z, Namba K, Xing J. Coupling between switching regulation and torque generation in bacterial flagellar motor. Phys Rev Lett 2012; 108:178105 [View Article][PubMed]
     [Google Scholar]
  24. Raddi G, Morado DR, Yan J, Haake DA, Yang XF et al. Three-dimensional structures of pathogenic and saprophytic Leptospira species revealed by cryo-electron tomography. J Bacteriol 2012; 194:1299–1306 [View Article][PubMed]
     [Google Scholar]
  25. Picardeau M, Bulach DM, Bouchier C, Zuerner RL, Zidane N et al. Genome sequence of the saprophyte Leptospira biflexa provides insights into the evolution of Leptospira and the pathogenesis of leptospirosis. PLoS One 2008; 3:e1607 [View Article][PubMed]
     [Google Scholar]
  26. Harman M, Vig DK, Radolf JD, Wolgemuth CW. Viscous dynamics of Lyme disease and syphilis spirochetes reveal flagellar torque and drag. Biophys J 2013; 105:2273–2280 [View Article][PubMed]
     [Google Scholar]
  27. Kimsey RB, Spielman A. Motility of Lyme disease spirochetes in fluids as viscous as the extracellular matrix. J Infect Dis 1990; 162:1205–1208[PubMed] [CrossRef]
     [Google Scholar]
  28. Petrino MG, Doetsch RN. ‘Viscotaxis’, a new behavioural response of Leptospira interrogans (biflexa) strain B16. J Gen Microbiol 1978; 109:113–117 [View Article][PubMed]
     [Google Scholar]
  29. Naresh R, Hampson DJ. Attraction of Brachyspira pilosicoli to mucin. Microbiology 2010; 156:191–197 [View Article][PubMed]
     [Google Scholar]
  30. Sze CW, Zhang K, Kariu T, Pal U, Li C. Borrelia burgdorferi needs chemotaxis to establish infection in mammals and to accomplish its enzootic cycle. Infect Immun 2012; 80:2485–2492 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000420
Loading
Viscosity-dependent variations in the cell shape and swimming manner of Leptospira
Microbiology 163, 153 (2017); https://doi.org/10.1099/mic.0.000420
/content/journal/micro/10.1099/mic.0.000420
/content/journal/micro/10.1099/mic.0.000420
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error