Advertisement

Cell Motility pp 137-175 | Cite as

Molecular Mechanism of Mycoplasma Gliding - A Novel Cell Motility System

  • Makoto Miyata
Part of the Biological and Medical Physics, Biomedical Engineering book series (BIOMEDICAL)

Summary

More than ten Mycoplasma species from two independent groups bind to glass surfaces and exhibit movement while maintaining their binding, a process known as gliding motility. They form a small membrane protrusion at a cell pole and move in the direction of the protrusion. Genomic sequencing and analysis has revealed that the motility mechanism must differ from those of other bacteria and other motor protein systems. M. mobile glides at 2.0-4.5μm/s. Its gliding machinery is composed of three very large proteins and one regular-sized protein around the cell membrane. Four hundred and fifty units of this machinery are located around the base of the protrusion, an area designated the “neck” and supported by a unique cytoskeletal structure. The gliding occurs based on the energy supplied from ATP hydrolysis on a solid surface coated by sialic acid. Gli349, the plausible leg protein, has a music-note shape that is 100nm in length and a suggested flexible 50nm protrusion. Our working model suggests that the flexible legs cyclically bind and release the sialic acid, and pull the cell body via conformational changes triggered by change in tension. M. pneumoniae glides at 0.3-1.0μm/s. The protrusion, known as the attachment organelle, is a large structure into which more than 11 proteins are integrated. Recent studies by electron microscopy have revealed a detailed structure, comprised of i) a surface structure, ii) segmented paired plates, iii) a terminal button, iv) a wheel, and v) a translucent area. Structural studies suggest an inchworm model for gliding, whereas a power stroke model similar to that of M. mobile can explain the inhibitory effects caused by an antibody against the plausible leg protein, P1 adhesin.

Keywords

Solid Surface Sialic Acid Optical Tweezer Mycoplasma Species Gli349 Protein 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Razin, S, Yogev, D, & Naot., Y. (1998.) Microbiol. Mol. Biol. Rev. 62, 1094–1156.Google Scholar
  2. 2.
    Weisburg, W, Tully, J, Rose, D, Petzel, J, Oyaizu, H, Yang, D, Mandelco, L, Sechrest, J, Lawrence, T, Etten, J. V, Maniloff, J, & Woese., C. (1989.) J. Bacteriol. 171, 6455–6467.Google Scholar
  3. 3.
    Bredt, W. (1968.) Pathol. Microbiol. 32, 321–326.Google Scholar
  4. 4.
    Kirchhoff, H. (1992.) Mycoplasmas- Molecular Biology and Pathogenesis. (American Society for Microbiology, Washington, D.C.), pp. 289–306.Google Scholar
  5. 5.
    Miyata, M. (2005.) In: Mycoplasmas: pathogenesis, molecular biology, and emerging strategies for control. (Horizon Biosciene, Norfolk, U.K.), pp. 137–163.Google Scholar
  6. 6.
    Jaffe, J, Stange-Thomann, N, Smith, C, DeCaprio, D, Fisher, S, Butler, J, Calvo, S, Elkins, T, FitzGerald, M, Hafez, N, Kodira, C, Major, J, Wang, S, Wilkinson, J, Nicol, R, Nusbaum, C, Birren, B, Berg, H, & Church., G. (2004.) Genome Research 14, 1447–1461.CrossRefGoogle Scholar
  7. 7.
    Hiratsuka, Y, Miyata, M, & Uyeda., T. (2005.) Biochem. Biophys. Res. Commun. 331, 318–324.CrossRefGoogle Scholar
  8. 8.
    Rosengarten, R & Kirchhoff., H. (1987.) J. Bacteriol. 169, 1891–1898.Google Scholar
  9. 9.
    Kirchhoff, H, Beyene, P, Fischer, M, Flossdorf, J, Heitmann, J, Khattab, B, Lopatta, D, Rosengarten, R, Seidel, G, & Yousef., C. (1987.) Int. J. Syst. Bacteriol. 37, 192–197.CrossRefGoogle Scholar
  10. 10.
    Kirchhoff, H & Rosengarten., R. (1984.) J. Gen. Microbiol. 130, 2439–2445.Google Scholar
  11. 11.
    Uenoyama, A & Miyata., M. (2005.) Proc. Natl. Acad. Sci. USA 102, 12754–12758.Google Scholar
  12. 12.
    Hasselbring, B, Page, C, Sheppard, E, & Krause., D. (2006.) J. Bacteriol. 188, 6335–6345.CrossRefGoogle Scholar
  13. 13.
    Kenri, T, Seto, S, Horino, A, Sasaki, Y, Sasaki, T, & Miyata., M. (2004.) J. Bacteriol. 186, 6944–6955.CrossRefGoogle Scholar
  14. 14.
    Radestock, U & Bredt., W. (1977.) J. Bacteriol. 129, 1495–1501.Google Scholar
  15. 15.
    Seto, S, Kenri, T, Tomiyama, T, & Miyata., M. (2005.) J. Bacteriol. 187, 1875–1877.CrossRefGoogle Scholar
  16. 16.
    Krause, D & Balish., M. (2004.) Mol. Microbiol. 51, 917–924.CrossRefGoogle Scholar
  17. 17.
    McBride, M. (2001.) Annu. Rev. Microbiol. 55, 49–75.CrossRefGoogle Scholar
  18. 18.
    Mattick, J. (2002.) Annu. Rev. Microbiol. 56, 289–314.CrossRefGoogle Scholar
  19. 19.
    Mogilner, A & Oster., G. (2003.) Curr. Biol. 13, R721–733.CrossRefGoogle Scholar
  20. 20.
    Sogaard-Andersen, L. (2004.) Curr. Opin. Microbiol. 7, 587–593.CrossRefGoogle Scholar
  21. 21.
    Wolgemuth, C & Oster., G. (2004.) J. Mol. Microbiol. Biotechnol. 7, 72–7.CrossRefGoogle Scholar
  22. 22.
    Mignot, T, Shaevitz, J, Hartzell, P, & Zusman., D. (2007.) Science 315, 853–856.CrossRefADSGoogle Scholar
  23. 23.
    McBride, M. (2004.) J. Mol. Microbiol. Biotechnol. 7, 63–71.CrossRefGoogle Scholar
  24. 24.
    Hatchel, J, Balish, R, Duley, M, & Balish., M. (2006.) Microbiology 152, 2181–2189.CrossRefGoogle Scholar
  25. 25.
    Jurkovic, D, Friedberg, A. J, Hatchel, J. M, Relich, R. F, & Balish., M. F. (2006.) Adherence and gliding motility at low temperatures by tortoise-associated mycoplasmas. p. 22.Google Scholar
  26. 26.
    Vasconcelos, A, Ferreira, H, Bizarro, C, Bonatto, S, Carvalho, M, Pinto, P, Almeida, D, Almeida, L, Almeida, R, Alves-Filho, L, Assuncao, E, Azevedo, V, Bogo, M, Brigido, M, Brocchi, M, Burity, H, Camargo, A, Camargo, S, Carepo, M, Carraro, D, de Mattos Cascardo, J, Castro, L, Cavalcanti, G, Chemale, G, Collevatti, R, Cunha, C, Dallagiovanna, B, Dambros, B, Dellagostin, O, Falcao, C, Fantinatti-Garboggini, F, Felipe, M, Fiorentin, L, Franco, G, Freitas, N, Frias, D, Grangeiro, T, Grisard, E, Guimaraes, C, Hungria, M, Jardim, S, Krieger, M, Laurino, J, Lima, L, Lopes, M, Loreto, E, Madeira, H, Manfio, G, Maranhao, A, Martinkovics, C, Medeiros, S, Moreira, M, Neiva, M, Ramalho-Neto, C, Nicolas, M, Oliveira, S, Paixao, R, Pedrosa, F, Pena, S, Pereira, M, Pereira-Ferrari, L, Piffer, I, Pinto, L, Potrich, D, Salim, A, Santos, F, Schmitt, R, Schneider, M, Schrank, A, Schrank, I, Schuck, A, Seuanez, H, Silva, D, Silva, R, Silva, S, Soares, C, Souza, K, Souza, R, Staats, C, Steffens, M, Teixeira, S, Urmenyi, T, Vainstein, M, Zuccherato, L, Simpson, A, & Zaha., A. (2005.) J. Bacteriol. 187, 5568–5577.CrossRefGoogle Scholar
  27. 27.
    Uenoyama, A, Kusumoto, A, & Miyata., M. (2004.) J. Bacteriol. 186, 1537–1545.CrossRefGoogle Scholar
  28. 28.
    Uenoyama, A & Miyata., M. (2005.) J. Bacteriol. 187, 5578–5584.Google Scholar
  29. 29.
    Pich, O, Burgos, R, Ferrer-Navarro, M, Querol, E, & Pinol., J. (2006.) Mol. Microbiol. 60, 1509–1519.CrossRefGoogle Scholar
  30. 30.
    Miyata. (2005.) Tanpakushitsu Kakusan Koso 50, 239–245.Google Scholar
  31. 31.
    Bourret, R, Charon, N, Stock, A, & West., A. (2002.) J. Bacteriol. 184, 1–17.CrossRefGoogle Scholar
  32. 32.
    Kirchhoff, H, Boldt, U, Rosengarten, R, & Klein-Struckmeier., A. (1987.) Curr. Microbiol. 15, 57–60.CrossRefGoogle Scholar
  33. 33.
    Chambaud, I, Heilig, R, Ferris, S, Barbe, V, Samson, D, Galisson, F, Moszer, I, Dybvig, K, Wroblewski, H, Viari, A, Rocha, E, & Blanchard., A. (2001.) Nucleic. Acids Res. 29, 2145–2153.CrossRefGoogle Scholar
  34. 34.
    Fraser, C, Gocayne, J, White, O, Adams, M, Clayton, R, Fleischmann, R, Bult, C, Kerlavage, A, Sutton, G, Kelley, J, Fritchman, R, Weidman, J, Small, K, Sandusky, M, Fuhrmann, J, Nguyen, D, Utterback, R, Saudek, D, Phillips, C, Merrick, J, Tomb, J.-F, Dougherty, B, Bott, K, Hu, P.-C, Lucier, T, Peterson, S, Smith, H, III, C. H, & Venter., J. (1995.) Science 270, 397–403.CrossRefADSGoogle Scholar
  35. 35.
    Himmelreich, R, Hilbert, H, Plagens, H, Pirkl, E, Li, B.-C, & Herrmann., R. (1996.) Nucleic Acids Res. 24, 4420–4449.CrossRefGoogle Scholar
  36. 36.
    Papazisi, L, Gorton, T. S, Kutish, G, Markham, P. F, Browning, G. F, Nguyen, D. K, Swartzell, S, Madan, A, Mahairas, G, & Geary., S. J. (2003.) Microbiology 149, 2307–2316.CrossRefGoogle Scholar
  37. 37.
    Sasaki, Y, Ishikawa, J, Yamashita, A, Oshima, K, Kenri, T, Furuya, K, Yoshino, C, Horino, A, Shiba, T, Sasaki, T, & Hattori., M. (2002.) Nucleic Acids Res. 30, 5293–5300.CrossRefGoogle Scholar
  38. 38.
    Rosengarten, R, Fisher, M, Kirchhoff, H, Kerlen, G, & Seack., K.-H. (1988.) Curr. Microbiol. 16, 253–257.CrossRefGoogle Scholar
  39. 39.
    Stadtlander, C & Kirchhoff., H. (1990.) Vet. Microbiol. 21, 339–343.CrossRefGoogle Scholar
  40. 40.
    Stadtlander, C & Kirchhoff., H. (1995.) Br. Vet. J. 151, 89–100.CrossRefGoogle Scholar
  41. 41.
    Stadtlander, C, Lotz, W, Korting, W, & Kirchhoff., H. (1995.) J. Comp. Pathol. 112, 351–359.CrossRefGoogle Scholar
  42. 42.
    Kusumoto, A, Seto, S, Jaffe, J, & Miyata., M. (2004.) Microbiology 150, 4001–4008.CrossRefGoogle Scholar
  43. 43.
    Miyata, M & Uenoyama., A. (2002.) FEMS Microbiol. Lett. 215, 285–289.CrossRefGoogle Scholar
  44. 44.
    Miyata, M, Ryu, W, & Berg., H. (2002.) J. Bacteriol. 184, 1827–1831.CrossRefGoogle Scholar
  45. 45.
    Jordan, J, Chang, H, Balish, M, Holt, L, Bose, S, Hasselbring, B, 3rd, R. W, Krunkosky, T, & Krause., D. (2007.) Infect. Immun. 75, 518–522.Google Scholar
  46. 46.
    Krunkosky, T, Jordan, J, Chambers, E, & Krause., D. (2007.) Microb. Pathog. 42, 98–103.CrossRefGoogle Scholar
  47. 47.
    Miyata, M, Yamamoto, H, Shimizu, T, Uenoyama, A, Citti, C, & Rosengarten., R. (2000.) Microbiology 146, 1311–1320.Google Scholar
  48. 48.
    Seto, S, Uenoyama, A, & Miyata., M. (2005.) J. Bacteriol. 187, 3502–3510.CrossRefGoogle Scholar
  49. 49.
    Seto, S, Layh-Schmitt, G, Kenri, T, & Miyata., M. (2001.) J. Bacteriol. 183, 1621–1630.CrossRefGoogle Scholar
  50. 50.
    Gitai, Z. (2005.) Cell 120, 577–586.CrossRefGoogle Scholar
  51. 51.
    Miyata, M & Petersen., J. (2004.) J. Bacteriol. 186, 4382–4386.CrossRefGoogle Scholar
  52. 52.
    Metsugi, S, Uenoyama, A, Adan-Kubo, J, Miyata, M, Yura, K, Kono, H, & Go., N. (2005.) Biophysics 1, 33–43.CrossRefGoogle Scholar
  53. 53.
    Adan-Kubo, J, Uenoyama, A, Arata, T, & Miyata., M. (2006.) J. Bacteriol. 188, 2821–2828.CrossRefGoogle Scholar
  54. 54.
    Edeling, M, Smith, C, & Owen., D. (2006.) Nat. Rev. Mol. Cell Biol. 7, 32–44.CrossRefGoogle Scholar
  55. 55.
    Jaffe, J, Miyata, M, & Berg., H. (2004.) J. Bacteriol. 186, 4254–4261.CrossRefGoogle Scholar
  56. 56.
    Roberts, D, Olson, L, Barile, M, Ginsburg, V, & Krivan., H. (1989.) J. Biol. Chem. 264, 9289–9293.Google Scholar
  57. 57.
    Nagai, R & Miyata., M. (2006.) J. Bacteriol. 188, 6469–6475.CrossRefGoogle Scholar
  58. 58.
    Gibbons, B & Gibbons., I. (1972.) J. Cell. Biol. 54, 75–97.CrossRefGoogle Scholar
  59. 59.
    Ohtani, N & Miyata., M. (2006.) Biochem. J. 403, 71–77.Google Scholar
  60. 60.
    Fischer, M, Kirchhoff, H, Rosengarten, R, Kerlen, G, & Seack., K.-H. (1987.) FEMS Microbiol. Lett. 40, 321–324.CrossRefGoogle Scholar
  61. 61.
    Kawaguchi, K & Ishiwata., S. (2000.) Biochem. Biophys. Res. Commun. 272, 895–899.CrossRefGoogle Scholar
  62. 62.
    Kawai, M, Kawaguchi, K, Saito, M, & Ishiwata., S. (2000.) Biophys. J. 78, 3112–3119.CrossRefGoogle Scholar
  63. 63.
    Meister, M, Lowe, G, & Berg., H. (1987.) Cell 49, 643–650.CrossRefGoogle Scholar
  64. 64.
    Rosengarten, R & Kirchhoff., H. (1988.) Curr. Microbiol. 16, 247–252.CrossRefGoogle Scholar
  65. 65.
    Rosengarten, R, Klein-Struckmeier, A, & Kirchhoff., H. (1988.) J. Bacteriol. 170, 989–990.Google Scholar
  66. 66.
    Finer, J, Simmons, R, & Spudich., J. (1994.) Nature 368, 113–119.CrossRefADSGoogle Scholar
  67. 67.
    Svoboda, K & Block., S. (1994.) Cell 77, 773–784.CrossRefGoogle Scholar
  68. 68.
    Charon, N. (2005.) Proc. Natl. Acad. Sci. USA 102, 13713–13714.CrossRefADSGoogle Scholar
  69. 69.
    Hiratsuka, Y, Miyata, M, Tada, T, & Uyeda., T. (2006.) Proc. Natl. Acad. Sci. USA 103, 13618–13623.CrossRefADSGoogle Scholar
  70. 70.
    Balish, M & Krause., D. (2006.) J. Mol. Microbiol. Biotechnol. 11, 244–255.CrossRefGoogle Scholar
  71. 71.
    Miyata, M & Ogaki., H. (2006.) J. Mol. Microbiol. Biotechnol. 11, 256–264.CrossRefGoogle Scholar
  72. 72.
    Razin, S & Jacobs., E. (1992.) J. Gen. Microbiol. 138, 407–422.Google Scholar
  73. 73.
    Wilson, M & Collier., A. (1976.) J. Bacteriol. 125, 332–339.Google Scholar
  74. 74.
    Kenri, T, Seto, S, Horino, A, Arakawa, Y, Sasaki, T, & Miyata., M. (2006.) Mapping of localization sites of cytadherence-related and cytoskeletal proteins of Mycoplasma pneumoniae by fluorescent protein tagging. p. 137.Google Scholar
  75. 75.
    Biberfeld, G & Biberfeld., P. (1970.) J. Bacteriol. 102, 855–861.Google Scholar
  76. 76.
    Gobel, U, Speth, V, & Bredt., W. (1981.) J. Cell Biol. 91, 537–543.CrossRefGoogle Scholar
  77. 77.
    Meng, K & Pfister., R. (1980.) J. Bacteriol. 144, 390–399.Google Scholar
  78. 78.
    Hegermann, J, Herrmann, R, & Mayer., F. (2002.) Naturwissenschaften 89, 453–458.CrossRefADSGoogle Scholar
  79. 79.
    Henderson, G & Jensen., G. (2006.) Mol. Microbiol. 60, 376–385.CrossRefGoogle Scholar
  80. 80.
    Regula, J, Boguth, G, Gorg, A, Hegermann, J, Mayer, F, Frank, R, & Herrmann., R. (2001.) Microbiology 147, 1045–1057.Google Scholar
  81. 81.
    Seybert, A, Herrmann, R, & Frangakis., A. (2006.) J. Struct. Biol. 156, 342–354.CrossRefGoogle Scholar
  82. 82.
    Hu, P, Cole, R. M, Huang, Y, Graham, J, Gardner, D, Collier, A, & Jr., W. C. (1982.) Science 216, 313–315.CrossRefADSGoogle Scholar
  83. 83.
    Kirchhoff, H, Rosengarten, R, Lotz, W, Fischer, M, & Lopatta., D. (1984.) Israel J. Med. Sci. 20, 848–853.Google Scholar
  84. 84.
    Shimizu, T & Miyata., M. (2002.) Curr. Microbiol. 44, 431–434.CrossRefGoogle Scholar
  85. 85.
    Wall, F, Pfister, R, & Somerson., N. (1983.) J. Bacteriol. 154, 924–929.Google Scholar
  86. 86.
    Balish, M. (2006.) Front. Biosci. 11, 2017–2027.CrossRefGoogle Scholar
  87. 87.
    Krause, D. (1996.) Mol. Microbiol. 20, 247–253.CrossRefGoogle Scholar
  88. 88.
    Balish, M & Krause., D. (2002.) Molecular Biology and Pathogenicity of Mycoplasmas., eds. Herrmann, R & Razin, S. (Kluwer Academic / Plenum Publishers, London.), pp. 491–518.Google Scholar
  89. 89.
    Seto, S & Miyata., M. (2003.) J. Bacteriol. 185, 1082–1091.CrossRefGoogle Scholar
  90. 90.
    Balish, M, Santurri, R, Ricci, A, Lee, K, & Krause., D. (2003.) Mol. Microbiol. 47, 49–60.CrossRefGoogle Scholar
  91. 91.
    Hedreyda, C, Lee, K, & Krause., D. (1993.) Plasmid 30, 170–175.CrossRefGoogle Scholar
  92. 92.
    Krause, D, Proft, T, Hedreyda, C. T, Hilbert, H, Plagens, H, & Herrmann., R. (1997.) J. Bacteriol. 179, 2668–2677.Google Scholar
  93. 93.
    Dandekar, T, Huynen, M, Regula, J, Ueberle, B, Zimmermann, C, Andrade, M, Doerks, T, Sanchez-Pulido, L, Snel, B, Suyama, M, Yuan, Y, Herrmann, R, & Bork., P. (2000.) Nucleic Acids Res. 28, 3278–3288.CrossRefGoogle Scholar
  94. 94.
    Krivan, H, Olson, L, Barile, M, Ginsburg, V, & Roberts., D. (1989.) J. Biol. Chem. 264, 9283–9288.Google Scholar
  95. 95.
    Layh-Schmitt, G & Herrmann., R. (1994.) Infect. Immun. 62, 974–979.Google Scholar
  96. 96.
    Layh-Schmitt, G, Podtelejnikov, A, & Mann., M. (2000.) Microbiology 146, 741–747.Google Scholar
  97. 97.
    Layh-Schmitt, G, Hilbert, H, & Pirkl., E. (1995.) J. Bacteriol. 177, 843–846.Google Scholar
  98. 98.
    Romero-Arroyo, C, Jordan, J, Peacock, S, Willby, M, Farmer, M, & Krause., D. (1999.) J. Bacteriol. 181, 1079–1087.Google Scholar
  99. 99.
    Stevens, M & Krause., D. (1992.) J. Bacteriol. 174, 4265–4274.Google Scholar
  100. 100.
    Jaffe, J, Berg, H, & Church., G. (2004.) Proteomics 4, 59–77.CrossRefGoogle Scholar
  101. 101.
    Hasselbring, B & Krause., D. (2007.) Mol. Microbiol. 63, 44–53.CrossRefGoogle Scholar
  102. 102.
    Jensen, G. (2007.) Mol. Microbiol. 63, 4–6.CrossRefGoogle Scholar
  103. 103.
    Wolgemuth, C, Igoshin, O, & Oster., G. (2003.) Biophys. J. 85, 828–842.CrossRefGoogle Scholar
  104. 104.
    Krause, D. (1998.) Trends Microbiol. 6, 15–18.CrossRefGoogle Scholar
  105. 105.
    Miyata, M. (2002.) Molecular Biology and Pathogenicity of Mycoplasmas., eds. Herrmann, R & Razin, S. (Kluwer Academic / Plenum Publishers, London.), pp. 117–130.Google Scholar
  106. 106.
    Miyata, M & Seto., S. (1999.) Biochimie 81, 873–878.CrossRefGoogle Scholar
  107. 107.
    Seto, S & Miyata., M. (1998.) J. Bacteriol. 180, 256–264.Google Scholar
  108. 108.
    Seto, S & Miyata., M. (1999.) J. Bacteriol. 181, 6073–6080.Google Scholar
  109. 109.
    B.M., H, Jordan, J, Krause, R, & Krause., D. (2006.) Proc. Natl. Acad. Sci. USA 103, 16478–16483.Google Scholar
  110. 110.
    Andrewes, C & Welch., F. (1946.) J. Pathol. Bacteriol. 58, 578–580.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Makoto Miyata
    • 1
  1. 1.Department of Biology, Graduate School of ScienceOsaka City University Sumiyoshi-kuOsaka 558-8585 JAPANJAPAN

Personalised recommendations