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Rototrichous: a new type of bacterial flagellation

  • Hayk MinasyanEmail author
Original Paper
  • 32 Downloads

Abstract

A rod-shaped microorganism with unknown type of flagellation has been accidentally discovered during phase-contrast microscopy of a sample of contaminated human donor blood. The flagellum consists of three fragments that form a complex locomotor device attached to bacterial body. The device provides bacterial motility by rotating around longitudinal axis of bacterial body and so this type of flagellation has been named “rototrichous.” This newly discovered bacterial flagellation should be included in the classification of bacterial flagellations.

Keywords

Bacteria Motility Flagellation Rototrichous 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

203_2019_1765_MOESM1_ESM.mpg (126.3 mb)
Supplementary material 1 (MPG 129302 kb)

References

  1. Abbe E (1874) A contribution to the theory of the microscope and the nature of microscopic vision. In: Proceedings of the Bristol Naturalists’ Society. I pt II, pp 200–261Google Scholar
  2. Abram D, Davis BK (1970) Structural properties and features of parasitic Bdellovibrio bacteriovorus. J Bacteriol 104:948–965PubMedPubMedCentralGoogle Scholar
  3. Abram D, Castro e Melo J, Chou D (1974) Penetration of Bdellovibrio bacteriovorus into host cells. J Bacteriol 118:663–680PubMedPubMedCentralGoogle Scholar
  4. Amann J (1911) Die direkte Zählung der Wasserbakterien mittels des Ultramikroskops. Centralbl Bakteriol II Abt 29:381–384Google Scholar
  5. Amann J, Ludwig RIW, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169PubMedPubMedCentralGoogle Scholar
  6. Armitage JP (1992) Behavioral responses in bacteria. Annu Rev Physiol 54:683–714PubMedCrossRefGoogle Scholar
  7. Armitage JP, Macnab RM (1987) Unidirectional, intermittent rotation of the flagellum of Rhodobacter sphaeroides. J Bacteriol 169:514–518PubMedPubMedCentralCrossRefGoogle Scholar
  8. Barbour AG (1998) Spirochetes come in from the cold. Nat Med 4:890–891PubMedCrossRefGoogle Scholar
  9. Beighton E, Porter AM, Stocker BAD (1958) X-ray and related studies of the flagella of non-motile bacteria. Biochim Biophys Acta 29:8–13PubMedCrossRefGoogle Scholar
  10. Belas R, Simon M, Silverman M (1986) Regulation of lateral flagella gene transcription in Vibrio parahaemolyticus. J Bacteriol 167(1):210–218PubMedPubMedCentralCrossRefGoogle Scholar
  11. Berg HC (1976) How spirochetes may swim. J Theor Biol 56:269–273PubMedCrossRefGoogle Scholar
  12. Berg HC, Anderson RA (1973) Bacteria swim by rotating their flagellar filaments. Nature 245:380–382PubMedCrossRefGoogle Scholar
  13. Berg HC, Turner L (1979) Movement of microorganisms in viscous environments. Nature 278:349–351PubMedCrossRefGoogle Scholar
  14. Berg HC, Bromley DB, Charon NW (1978) Leptospiral motility. Symp Soc Gen Microbiol 28:285–294Google Scholar
  15. Bergey’s Manual of Systematic Bacteriology (2005) US. SpringerGoogle Scholar
  16. Birch-Andersen A, Hovind-Hougen K, Borg-Petersen C (1973) Electron microscopy of Leptospira. 1. Leptospira strain Pomona. Acta Pathol Microbiol Scand B Microbiol Immunol 81(6):665–676PubMedGoogle Scholar
  17. Boucher Y, Douady CJ, Papke RT, Walsh DA, Boudreau ME, Nesbo CL, Case RJ, Doolittle WF (2003) Lateral gene transfer and the origins of prokaryotic groups. Annu Rev Genet 37:283–328PubMedCrossRefGoogle Scholar
  18. Canale-Parola E (1984) The spirochetes. In: Krieg NR, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 1. Williams and Wilkins, Baltimore, pp 38–70Google Scholar
  19. Canals R, Ramirez S, Vilches S, Horsburgh G, Shaw JG, Tomás JM, Merino S (2006) Polar flagellum biogenesis in aeromonas hydrophila. J Bacteriol 188(2):542–555PubMedPubMedCentralCrossRefGoogle Scholar
  20. Carleton O, Charon NW, Allender P, O’Brien S (1979) Helixhandedness of Leptospira interrogans as determined by scanning electronmicroscopy. J Bacteriol 137:1413–1416PubMedPubMedCentralGoogle Scholar
  21. Charon NW, Lawrence CW, O’Brien S (1981) Movement of antibody-coated latex beads attached to the spirochete Leptospira interrogans. Proc Natl Acad Sci USA 78:7166–7170PubMedCrossRefGoogle Scholar
  22. Charon NW, Goldstein SF, Curci K, Limberger RJ (1991) The bent-end morphology of Treponema phagedenis is associated with short, left-handed periplasmic flagella. J Bacteriol 173:4820–4826PubMedPubMedCentralCrossRefGoogle Scholar
  23. Charon NW, Greenberg EP, Koopman MBH, Limberger RJ (1992) Spirochete chemotaxis, motility, and the structure of the spirochetal periplasmic flagella. Res Microbiol 143:597–603PubMedCrossRefGoogle Scholar
  24. Cluzel P, Surette M, Leibler S (2000) An ultrasensitive bacterial motor revealed by monitoring signaling proteins in single cells. Science 287:1652–1655PubMedCrossRefGoogle Scholar
  25. Davis DJ (1921) The accessory factors in bacterial growth: IV. The “satellite” or symbiosis. Phenomenon of Pfeiffer’s Bacillus (B. influenzae). J Infect Dis 29:178–186Google Scholar
  26. DeLong EF (1998) Everything in moderation: archaea as ‘non-extremophiles’. Curr Opin Genet Dev 8(6):649–654PubMedCrossRefGoogle Scholar
  27. DeLong EF, Pace NR (2001) Environmental diversity of bacteria and archaea. Syst Biol 50(4):470–478PubMedCrossRefGoogle Scholar
  28. D’Onofrio AJM, Crawford EJ, Stewart K, Witt E, Gavrish S, Epstein J, Clardy B, Lewis K (2010) Siderophores from neighboring organisms promote the growth of uncultured bacteria. Chem Biol 17:254–264PubMedPubMedCentralCrossRefGoogle Scholar
  29. Fenton AK, Kanna M, Woods RD, Aizawa S-I, Sockett RE (2010) Shadowing the actions of a predator: backlit fluorescent microscopy reveals synchronous nonbinary septation of predatory bdellovibrio inside prey and exit through discrete bdelloplast pores. J Bacteriol 192:6329–6335PubMedPubMedCentralCrossRefGoogle Scholar
  30. Fildes P (1921) The nature of the effect of blood-pigment upon the growth of B. influenzæ. Br J Exp Pathol 2:16–25PubMedCentralPubMedGoogle Scholar
  31. Fosnaugh K, Greenberg EP (1988) Motility and chemotaxis of Spirochaeta aurantia: computer- assisted motion analysis. J Bacteriol 170:1678–1774CrossRefGoogle Scholar
  32. Fosnaugh K, Greenberg EP (1989) Chemotaxis mutants of Spirochaeta aurantia. J Bacteriol 171:606–611PubMedPubMedCentralCrossRefGoogle Scholar
  33. Goldstein SF, Charon NW (1988) The motility of the spirochete Leptospira. Cell Motility Cytoskel 9:101–110PubMedCrossRefGoogle Scholar
  34. Goldstein SF, Charon NW (1990) Multiple exposure photographic analysis of a motile spirochete. Proc Natl Acad Sci USA 87:4895–4899PubMedCrossRefGoogle Scholar
  35. Goldstein SF, Charon NW, Kreiling JA (1994) Borrelia burgdorferi swims with a planar waveform similar to that of eukaryotic flagella. Proc Natl Acad Sci USA 91:3433–3437PubMedCrossRefGoogle Scholar
  36. Goldstein SF, Buttle KF, Charon NW (1996) Structural analysis of Leptospiraceae and Borrelia burgdorferi using high voltage electron microscopy. J Bacteriol 178:6539–6545PubMedPubMedCentralCrossRefGoogle Scholar
  37. Grossart HP, Steward GF, Martinez J, Azam F (2000) A simple, rapid method for demonstrating bacterial flagella. Appl Environ Microbiol 66:3632–3636PubMedPubMedCentralCrossRefGoogle Scholar
  38. Helmholtz H (1876) On the limits of the optical capacity of the microscope. Mon Microsc J 16:15–39Google Scholar
  39. Holt SC (1978) Anatomy and chemistry of spirochetes. Microbiol Rev 42:114–160PubMedPubMedCentralGoogle Scholar
  40. Houwink AL, van Iterson W (1950) Electron microscopical observations on bacterial cytology. A study of flagellation. Biocim Biophys Acta 5(1):10–44CrossRefGoogle Scholar
  41. Hugenholz P, Goebel BM, Pace NR (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180(18):4765–4774Google Scholar
  42. Jarrell KF, McBride MJ (2008) The surprisingly diverse ways that prokaryotes move. Nat Rev Microbiol 6:466–476PubMedCrossRefGoogle Scholar
  43. Jordan EO, Caldwell ME, Reiter D (1934) Bacterial motility. J Bacteriol 27:165–174PubMedPubMedCentralGoogle Scholar
  44. Kaiser GE, Doetsch RN (1975) Enhanced translational motion of Leptospira in viscous environments. Nature 255:656–657PubMedCrossRefGoogle Scholar
  45. Kim YK, McCarter LL (2000) Analysis of the polar flagellar gene system of vibrio parahaemolyticus. J Bacteriol 182(13):3693–3704PubMedPubMedCentralCrossRefGoogle Scholar
  46. Kim M, Bird JC, Van Parys AJ, Breuer KS, Powers TR (2003) A macroscopic scale model of bacterial flagellar bundling. Proc Natl Acad Sci USA 100(26):15481–15485PubMedCrossRefGoogle Scholar
  47. Kojima S, Shinohara A, Terashima H, Yakushi T, Sakuma M, Homma M, Namba K, Imada K (2008) Insights into the stator assembly of the Vibrio flagellar motor from the crystal structure of MotY. Proc Natl Acad Sci USA 190:7696–7701CrossRefGoogle Scholar
  48. Leifson E (1930) A method of staining bacterial flagella and capsules together with a study of the origin of flagella. J Bacteriol 20:203–211PubMedPubMedCentralGoogle Scholar
  49. Leifson E (1951) Staining, shape and arrangement of bacterial flagella. J Bacteriol 62:377–398PubMedPubMedCentralGoogle Scholar
  50. Limberger RJ, Charon NW (1986) Treponema phagedenis has at least two proteins residing together on its periplasmic flagella. J Bacteriol 166:105–112PubMedPubMedCentralCrossRefGoogle Scholar
  51. Lowy J, Hanson J (1965) Electron microscope studies of bacterial flagella. J Mol Biol 11:293–13CrossRefGoogle Scholar
  52. Lwoff A, Lwoff M (1937) Studies on codehydrogenases. I—nature of growth factor “V”. Proc R Soc Lond Ser B Biol Sci 122:352–359CrossRefGoogle Scholar
  53. Macnab RM (1977) Bacterial flagella rotating in bundles: a study in helical geometry. Proc Natl Acad Sci USA 74(1):221–225PubMedCrossRefGoogle Scholar
  54. McCarter LL (2004) Dual flagellar systems enable motility under different circumstances. J Mol Microbiol Biotechnol 7(1–2):18–29PubMedCrossRefGoogle Scholar
  55. Merino S, Shaw JG, Tomás JM (2006) Bacterial lateral flagella: an inducible flagella system. FEMS Microbiol Lett 263(2):127–135PubMedCrossRefGoogle Scholar
  56. Mudd S, Polevitsky K, Anderson TF, Chambers LA (1941) Bacterial morphology as shown by the electron microscope. IV. Structural differentiation within the bacterial protoplasm. J Bacteriol 42(2):251–264PubMedPubMedCentralGoogle Scholar
  57. Noguchi H (1918) Morophological characteristics and nomenclature of Leptospira (Spirochaeta) icterohaemorrhagiae. J Exp Med 27:575–592PubMedPubMedCentralCrossRefGoogle Scholar
  58. Olsen GJ, Woese CR, Overbeek R (1994) The winds of (evolutionary) change: breathing new life into microbiology. J Bacteriol 176(1):1–6PubMedPubMedCentralCrossRefGoogle Scholar
  59. Paster BJ, Canale-Parola E (1980) Involvement of periplasmic fibrils in motility of spirochetes. J Bacteriol 141:359–364PubMedPubMedCentralGoogle Scholar
  60. Pietrantonio F, Noble PB, Amsel R, Chan EC (1988) Locomotory characteristics of Treponema denticola. Canad J Microbiol 34:748–752CrossRefGoogle Scholar
  61. Pijper A (1948) Bacterial flagella and motility. Nature 161:200–201PubMedCrossRefGoogle Scholar
  62. Pijper A, Abraham G (1954) Wavelength of bacterial flagella. J Gen Microbiol 10:452–456PubMedCrossRefGoogle Scholar
  63. Rendulic S, Jagtap P, Rosinus A, Eppinger M, Baar C, Lanz C, Keller H, Lambert C, Evans KJ, Goesmann A, Meyer F, Sockett RE, Schuster SC (2004) A predator unmasked: life cycle of bdellovibrio bacteriovorus from a genomic perspective. Science 303(5658):689–692PubMedCrossRefGoogle Scholar
  64. Ruby JD, Charon NW (1998) Effect of temperature and viscosity on the motility of the spirochete Treponema denticola. FEMS Mirobiol Lett 169(2):251–254CrossRefGoogle Scholar
  65. 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 88:82–92PubMedPubMedCentralCrossRefGoogle Scholar
  66. Schmitt R (2002) Sinorhizobial chemotaxis: a departure from the enterobacterial paradigm. Microbiology 148:627–631PubMedCrossRefGoogle Scholar
  67. Shunk IV (1920) A modification of Loeffler’s flagella stain. J Bacteriol 5:181–187PubMedPubMedCentralGoogle Scholar
  68. Silverman M, Simon MI (1974) Flagellar rotation and the mechanism of bacterial motility. Nature 249:73–74PubMedCrossRefGoogle Scholar
  69. Sowa Y, Berry RM (2008) Bacterial flagellar motor. Q Rev Biophys 41:103–132PubMedCrossRefGoogle Scholar
  70. Staley JT, Konopka A (1985) Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 39:321–346PubMedCrossRefGoogle Scholar
  71. Strauch E, Beck S, Appel B (2007) Bdellovibrio and like organisms: potential sources for new biochemicals and therapeutic agents? Predatory prokaryotes. Microbiol Monogr 4:131CrossRefGoogle Scholar
  72. Theron J, Cloete TE (2000) Molecular techniques for determining microbial diversity and community structure in natural environments. Crit Rev Microbiol 26(1):37–57PubMedCrossRefGoogle Scholar
  73. Thomas NA, Bardy SL, Jarrell KF (2001) The archaeal flagellum: a different kind of prokaryotic motility structure. FEMS Microbiol Rev 25(2):147–174PubMedCrossRefGoogle Scholar
  74. Turner L, Ryu WS, Berg HC (2000) Real-time imaging of fluorescent flagellar filaments. J Bacteriol 182:2793–2801PubMedPubMedCentralCrossRefGoogle Scholar
  75. Van Weelden GJ, Charon NW, Norris SJ (1990) Viscosity and the motility of Treponema phagedenis and Treponema pallidum. Abstr 90th Annu Meet Am Soc Microbiol I76:211Google Scholar
  76. Watsuji TO, Kato T, Ueda K, Beppu T (2006) CO2 supply induces the growth of Symbiobacterium thermophilum, a syntrophic bacterium. Biosci Biotechnol Biochem 70:753–756PubMedCrossRefGoogle Scholar
  77. Watsuji T, Yamada S, Yamabe T, Watanabe Y, Kato T, Saito T, Ueda K, Beppu T (2007) Identification of indole derivatives as self-growth inhibitors of symbiobacterium thermophilum, a unique bacterium whose growth depends on coculture with a Bacillus sp. Appl Environ Microbiol 73:6159–6165PubMedPubMedCentralCrossRefGoogle Scholar
  78. West M, Burdash NM, Freimuth F (1977) Simplified silver-plating stain for flagella. J Clin Microbiol 6:414–419PubMedPubMedCentralGoogle Scholar
  79. Yonekura K, Maki-Yonekura S, Namba K (2003) Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424(6949):643–650PubMedCrossRefGoogle Scholar
  80. Zuckerkandl E, Pauling L (1965) Molecules as documents of evolutionary history. J Theor Biol 8(2):357–366PubMedCrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.YerevanArmenia

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