1887

Abstract

The cluster is a clade of eight described species which all exhibit cellular polarity. Their polar attachment organelle is a hub of cellular activities including cytadherence and gliding motility, and its duplication in the species is coordinated with cell division and DNA replication. The attachment organelle houses a detergent-insoluble, electron-dense core whose presence is required for structural integrity. Although mutant analysis has led to the identification of attachment organelle proteins, the mechanistic basis for the activities of the attachment organelle remains poorly understood, with gliding motility attributed alternatively to the core or to the adhesins. In this study we investigated attachment organelle-associated phenotypes, including gliding motility characteristics and ultrastructural details, in seven species of the cluster under identical conditions, allowing direct comparison. We identified gliding ability in three species in which it has not previously been reported, , and . Across species, ultrastructural features of attachment organelles and their cores do not correlate with gliding speed, and morphological features of cores are inconsistent with predictions about how these structures are involved in the gliding process, disfavouring a prominent, direct role for the electron-dense core in gliding. In addition, we found to be an outlier in terms of cell structure with respect to its close relatives, suggesting that it has acquired a special set of adaptations during its evolution.

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2008-01-01
2020-07-09
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References

  1. Balish M. F.. 2006; Subcellular structures of mycoplasmas. Front Biosci11:2017–2027
    [Google Scholar]
  2. Balish M. F., Krause D. C.. 2005; Mycoplasma attachment organelle and cell division. In Mycoplasmas: Molecular Biology, Pathogenicity, and Strategies for Control . pp189–237 Edited by Blanchard A.. Browning G.. Norfolk, UK: Horizon Bioscience;
  3. Balish M. F., Krause D. C.. 2006; Mycoplasmas: a distinct cytoskeleton for wall-less bacteria. J Mol Microbiol Biotechnol11:244–255
    [Google Scholar]
  4. Biberfeld G., Biberfeld P.. 1970; Ultrastructural features of Mycoplasma pneumoniae . J Bacteriol102:855–861
    [Google Scholar]
  5. Bredt W.. 1979; Motility. In The Mycoplasmas vol 1 pp141–155 Edited by Barile M. F.. Razin S.. New York: Academic Press;
    [Google Scholar]
  6. Bredt W., Radestock U.. 1977; Gliding motility of Mycoplasma pulmonis . J Bacteriol130:937–938
    [Google Scholar]
  7. Cunha S., Odijk T., Süleymanoglu E., Woldringh C. L.. 2001; Isolation of the Escherichia coli nucleoid. Biochimie83:149–154
    [Google Scholar]
  8. Dhandayuthapani S., Rasmussen W. G., Baseman J. B.. 1999; Disruption of gene mg218 of Mycoplasma genitalium through homologous recombination leads to an adherence-deficient phenotype. Proc Natl Acad Sci U S A96:5227–5232
    [Google Scholar]
  9. Göbel U., Speth V., Bredt W.. 1981; Filamentous structures in adherent Mycoplasma pneumoniae cells treated with nonionic detergents. J Cell Biol91:537–543
    [Google Scholar]
  10. Gourlay R. N., Wyld S. G., Leach R. H.. 1977; Mycoplasma alvi , a new species from bovine intestinal and urogenital tracts. Int J Syst Bacteriol27:86–96
    [Google Scholar]
  11. Hall T. A.. 1999; BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser41:95–98
    [Google Scholar]
  12. Hasselbring B. M., Krause D. C.. 2007; Cytoskeletal protein P41 is required to anchor the terminal organelle of the wall-less prokaryote Mycoplasma pneumoniae . Mol Microbiol63:44–53
    [Google Scholar]
  13. Hasselbring B. M., Jordan J. L., Krause D. C.. 2005; Mutant analysis reveals a specific requirement for protein P30 in Mycoplasma pneumoniae gliding motility. J Bacteriol187:6281–6289
    [Google Scholar]
  14. Hasselbring B. M., Jordan J. L., Krause R. W., Krause D. C.. 2006a; Terminal organelle development in the cell wall-less bacterium Mycoplasma pneumoniae . Proc Natl Acad Sci U S A103:16478–16483
    [Google Scholar]
  15. Hasselbring B. M., Page C. A., Sheppard E. S., Krause D. C.. 2006b; Transposon mutagenesis identifies genes associated with Mycoplasma pneumoniae gliding motility. J Bacteriol188:6335–6345
    [Google Scholar]
  16. Hatchel J. M., Balish R. S., Duley M. L., Balish M. F.. 2006; Ultrastructure and gliding motility of Mycoplasma amphoriforme , a possible human respiratory pathogen. Microbiology152:2181–2189
    [Google Scholar]
  17. Hegermann J., Herrmann R., Mayer F.. 2002; Cytoskeletal elements in the bacterium Mycoplasma pneumoniae . Naturwissenschaften89:453–458
    [Google Scholar]
  18. Henderson G. P., Jensen G. J.. 2006; Three-dimensional structure of Mycoplasma pneumoniae 's attachment organelle and a model for its role in gliding motility. Mol Microbiol60:376–385
    [Google Scholar]
  19. Johansson K. E., Pettersson B.. 2002; Taxonomy of Mollicutes . In Molecular Biology and Pathogenicity of Mycoplasmas . pp1–29 Edited by Razin S.. Herrmann R.. New York: Kluwer Academic/Plenum Publishers;
  20. Jordan J. L., Chang H. Y., Balish M. F., Holt L. S., Bose S. R., Hasselbring B. M., Waldo R. H. III, Krunkosky T. M., Krause D. C.. 2007; Protein P200 is dispensable for Mycoplasma pneumoniae hemadsorption but not gliding motility or colonization of differentiated bronchial epithelium. Infect Immun75:518–522
    [Google Scholar]
  21. Krause D. C., Balish M. F.. 2004; Cellular engineering in a minimal microbe: structure and assembly of the terminal organelle of Mycoplasma pneumoniae . Mol Microbiol51:917–924
    [Google Scholar]
  22. Lind K., Lindhardt B. Ø., Schütten H. J., Blom J., Christiansen C.. 1984; Serological cross-reactions between Mycoplasma genitalium and Mycoplasma pneumoniae . J Clin Microbiol20:1036–1043
    [Google Scholar]
  23. Maniloff J., Quinlan D. C.. 1974; Partial purification of a membrane-associated deoxyribonucleic acid complex from Mycoplasma gallisepticum . J Bacteriol120:495–501
    [Google Scholar]
  24. Meng K. E., Pfister R. M.. 1980; Intracellular structures of Mycoplasma pneumoniae revealed after membrane removal. J Bacteriol144:390–399
    [Google Scholar]
  25. Miyata M.. 2005; Gliding motility of mycoplasmas: the mechanism cannot be explained by current biology. In Mycoplasmas: Molecular Biology, Pathogenicity, and Strategies for Control . pp137–163 Edited by Blanchard A.. Browning G. Norfolk, UK: Horizon Bioscience;
  26. Nagai R., Miyata M.. 2006; Gliding motility of Mycoplasma mobile can occur by repeated binding to N -acetylneuraminyllactose (sialyllactose) fixed on solid surfaces. J Bacteriol188:6469–6475
    [Google Scholar]
  27. Papazisi L., Frasca S. Jr, Gladd M., Liao X., Yogev D., Geary S. J.. 2002; GapA and CrmA coexpression is essential for Mycoplasma gallisepticum cytadherence and virulence. Infect Immun70:6839–6845
    [Google Scholar]
  28. Perrière G., Gouy M.. 1996; WWW-Query: an on-line retrieval system for biological sequence banks. Biochimie78:364–369
    [Google Scholar]
  29. Pich O. Q., Burgos R., Ferrer-Navarro M., Querol E., Piñol J.. 2006; Mycoplasma genitalium mg200 and mg386 genes are involved in gliding motility but not in cytadherence. Mol Microbiol60:1509–1519
    [Google Scholar]
  30. Pitcher D. G., Windsor D., Windsor H., Bradbury J. M., Yavari C., Jensen J. S., Ling C., Webster D.. 2005; Mycoplasma amphoriforme sp. nov., isolated from a patient with chronic bronchopneumonia. Int J Syst Evol Microbiol55:2589–2594
    [Google Scholar]
  31. Regula J. T., Boguth G., Görg A., Hegermann J., Mayer F., Frank R., Herrmann R.. 2001; Defining the mycoplasma 'cytoskeleton': the protein composition of the Triton X-100 insoluble fraction of the bacterium Mycoplasma pneumoniae determined by 2-D gel electrophoresis and mass spectrometry. Microbiology147:1045–1057
    [Google Scholar]
  32. Seto S., Layh-Schmitt G., Kenri T., Miyata M.. 2001; Visualization of the attachment organelle and cytadherence proteins of Mycoplasma pneumoniae by immunofluorescence microscopy. J Bacteriol183:1621–1630
    [Google Scholar]
  33. Seto S., Kenri T., Tomiyama T., Miyata M.. 2005a; Involvement of P1 adhesin in gliding motility of Mycoplasma pneumoniae as revealed by the inhibitory effects of antibody under optimized gliding conditions. J Bacteriol187:1875–1877
    [Google Scholar]
  34. Seto S., Uenoyama A., Miyata M.. 2005b; Identification of a 521-kilodalton protein (Gli521) involved in force generation or force transmission for Mycoplasma mobile gliding. J Bacteriol187:3502–3510
    [Google Scholar]
  35. Seybert A., Herrmann R., Frangakis A. S.. 2006; Structural analysis of Mycoplasma pneumoniae by cryo-electron tomography. J Struct Biol156:342–354
    [Google Scholar]
  36. Shimizu T., Miyata M.. 2002; Electron microscopic studies of three gliding mycoplasmas, Mycoplasma mobile, M. pneumoniae , and M. gallisepticum , by using the freeze-substitution technique. Curr Microbiol44:431–434
    [Google Scholar]
  37. Tham T. N., Ferris S., Bahraoui E., Canarelli S., Montagnier L., Blanchard A.. 1994; Molecular characterization of the P1-like adhesin gene from Mycoplasma pirum . J Bacteriol176:781–788
    [Google Scholar]
  38. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G.. 1997; The clustal_x Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res25:4876–4882
    [Google Scholar]
  39. Tully J. G., Rose D. L., Whitcomb R. F., Wenzel R. P.. 1979; Enhanced isolation of Mycoplasma pneumoniae from throat washings with a newly-modified culture medium. J Infect Dis139:478–482
    [Google Scholar]
  40. Uenoyama A., Kusumoto A., Miyata M.. 2004; Identification of a 349-kilodalton protein (Gli349) responsible for cytadherence and glass binding during gliding of Mycoplasma mobile . J Bacteriol186:1537–1545
    [Google Scholar]
  41. Waites K. B., Talkington D. F.. 2004; Mycoplasma pneumoniae and its role as a human pathogen. Clin Microbiol Rev17:697–728
    [Google Scholar]
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