Skip to main content
SpringerLink
Log in

“Mycoplasmal Antigen Modulation,” a Novel Surface Variation Suggested for a Lipoprotein Specifically Localized on Mycoplasma mobile

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Mycoplasma mobile, a pathogen of freshwater fish, glides easily across surfaces, colonizes on the fish gill, and causes necrosis. The cell surface is differentiated into three parts: the head, neck, and body. Mobile variable surface proteins (Mvsps) localizing at each of these parts may be involved in surface variation including phase variation and antigenic variation, although no proof exists. In this study, we examined this possibility by focusing on MvspI, the largest Mvsp. Immunofluorescence microscopy showed that MvspI is expressed on the surfaces of all cells. When anti-MvspI antibody was added at concentrations over 0.8 nM, MvspI was observed to decrease over time. After 72 h of cultivation with the antibody, the fluorescence intensity and amount of MvspI decreased up to 13 and 39%, respectively, compared to those of cells grown without antibody. These changes were reversed by the removal of the antibody. Such effects were not observed when another antibody targeting other Mvsps was used, suggesting that the decrease is specific to the relationship between MvspI and the antibody. Cell growth was also inhibited by the antibody, but the decrease in MvspI could not be explained by the selective growth of MvspI-negative variants or by the inhibition of growth with other conditions. The decrease in MvspI caused by the antibody binding may suggest a novel type of surface variation, designated here as “mycoplasmal antigen modulation.”

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Adan-Kubo J, Uenoyama A, Arata T, Miyata M (2006) Morphology of isolated Gli349, a leg protein responsible for glass binding of Mycoplasma mobile gliding revealed by rotary-shadowing electron microscopy. J Bacteriol 188:2821–2828

    Article  PubMed  CAS  Google Scholar 

  2. Aluotto BB, Wittler RG, Williams CO, Faber JE (1970) Standardized bacteriologic techniques for the characterization of Mycoplasma species. Int J Syst Bacteriol 20:35–58

    Article  Google Scholar 

  3. Avakian AP, Ley DH (1993) Inhibition of Mycoplasma gallisepticum growth and attachment to chick tracheal rings by antibodies to a 64-kilodalton membrane protein of M. gallisepticum. Avian Dis 37:706–714

    Article  PubMed  CAS  Google Scholar 

  4. Bhugra B, Voelker LL, Zou N, Yu H, Dybvig K (1995) Mechanism of antigenic variation in Mycoplasma pulmonis: interwoven, site-specific DNA inversions. Mol Microbiol 18:703–714

    Article  PubMed  CAS  Google Scholar 

  5. Chambaud I, Heilig R, Ferris S, Barbe V, Samson D, Galisson F, Moszer I, Dybvig K, Wroblewski H, Viari A, Rocha EP, Blanchard A (2001) The complete genome sequence of the murine respiratory pathogen Mycoplasma pulmonis. Nucleic Acids Res 29:2145–2153

    Article  PubMed  CAS  Google Scholar 

  6. Citti C, Nouvel LX, Baranowski E (2010) Phase and antigenic variation in mycoplasmas. Future Microbiol 5:1073–1085

    Article  PubMed  CAS  Google Scholar 

  7. Duffy MF, Moormohammadi AH, Baseggio N, Browning GF, Markham PF (1998) Immunological and biochemical characterization of membrane proteins. In: Miles RJ, Nicholas RAJ (eds) Methods in molecular biology, vol 104. Hamana Press, Totowa, pp 279–298

    Google Scholar 

  8. Jaffe JD, Stange-Thomann N, Smith C, DeCaprio D, Fisher S, Butler J, Calvo S, Elkins T, FitzGerald MG, Hafez N, Kodira CD, Major J, Wang S, Wilkinson J, Nicol R, Nusbaum C, Birren B, Berg HC, Church GM (2004) The complete genome and proteome of Mycoplasma mobile. Genome Res 14:1447–1461

    Article  PubMed  CAS  Google Scholar 

  9. Kirchhoff H, Rosengarten R (1984) Isolation of a motile mycoplasma from fish. J Gen Microbiol 130:2439–2445

    PubMed  CAS  Google Scholar 

  10. Kusumoto A, Seto S, Jaffe JD, Miyata M (2004) Cell surface differentiation of Mycoplasma mobile visualized by surface protein localization. Microbiology 150:4001–4008

    Article  PubMed  CAS  Google Scholar 

  11. Lluch-Senar M, Vallmitjana M, Querol E, Pinol J (2007) A new promoterless reporter vector reveals antisense transcription in Mycoplasma genitalium. Microbiology 153:2743–2752

    Article  PubMed  CAS  Google Scholar 

  12. Markham PF, Glew MD, Browning GF, Whithear KG, Walker ID (1998) Expression of two members of the pMGA gene family of Mycoplasma gallisepticum oscillates and is influenced by pMGA-specific antibodies. Infect Immun 66:2845–2853

    PubMed  CAS  Google Scholar 

  13. Miyata M, Seto S (1999) Cell reproduction cycle of mycoplasma. Biochimie 81:873–878

    Article  PubMed  CAS  Google Scholar 

  14. Miyata M, Yamamoto H, Shimizu T, Uenoyama A, Citti C, Rosengarten R (2000) Gliding mutants of Mycoplasma mobile: relationships between motility and cell morphology, cell adhesion and microcolony formation. Microbiology 146:1311–1320

    PubMed  CAS  Google Scholar 

  15. Miyata M (2002) Cell division. In: Herrmann R, Razin S (eds) Molecular biology and pathogenicity of mycoplasmas. Kluwer Academic/Plenum Publishers, London, pp 117–130

    Chapter  Google Scholar 

  16. Miyata M, Ryu WS, Berg HC (2002) Force and velocity of Mycoplasma mobile gliding. J Bacteriol 184:1827–1831

    Article  PubMed  CAS  Google Scholar 

  17. Miyata M, Uenoyama A (2002) Movement on the cell surface of the gliding bacterium, Mycoplasma mobile, is limited to its head-like structure. FEMS Microbiol Lett 215:285–289

    Article  PubMed  CAS  Google Scholar 

  18. Miyata M, Ogaki H (2006) Cytoskeleton of mollicutes. J Mol Microbiol Biotechnol 11:256–264

    Article  PubMed  CAS  Google Scholar 

  19. Miyata M (2008) Centipede and inchworm models to explain Mycoplasma gliding. Trends Microbiol 16:6–12

    Article  PubMed  CAS  Google Scholar 

  20. Miyata M (2010) Unique centipede mechanism of Mycoplasma gliding. Annu Rev Microbiol 64:519–537

    Article  PubMed  CAS  Google Scholar 

  21. Nakane D, Miyata M (2007) Cytoskeletal “jellyfish” structure of Mycoplasma mobile. Proc Natl Acad Sci USA 104(49):19518–19523

    Article  PubMed  CAS  Google Scholar 

  22. Nakane D, Adan-Kubo J, Kenri T, Miyata M (2011) Isolation and characterization of P1 adhesin, a leg protein of the gliding bacterium Mycoplasma pneumoniae. J Bacteriol 193:715–722

    Article  PubMed  CAS  Google Scholar 

  23. Nonaka T, Adan-Kubo J, Miyata M (2010) Triskelion structure of the Gli521 protein, involved in the gliding mechanism of Mycoplasma mobile. J Bacteriol 192:636–642

    Article  PubMed  CAS  Google Scholar 

  24. Oshima K, Nishida H (2007) Phylogenetic relationships among mycoplasmas based on the whole genomic information. J Mol Evol 65:249–258

    Article  PubMed  CAS  Google Scholar 

  25. Razin S, Yogev D, Naot Y (1998) Molecular biology and pathogenicity of mycoplasmas. Microbiol Mol Biol Rev 62:1094–1156

    PubMed  CAS  Google Scholar 

  26. Robertson JAR, Stemke GW (1995) Measurement of mollicute growth by ATP-dependent luminometry. In: Razin S, Tully JG (eds) Molecular and diagnostic procedures in mycoplasmology, vol 1. Academic Press, San Diego, pp 65–71

  27. Rodriguez F, Fernandez A, Ball HJ (1997) Detection of Mycoplasma mycoides subspecies mycoides by growth-inhibition using monoclonal antibodies. Res Vet Sci 63:91–92

    Article  PubMed  CAS  Google Scholar 

  28. Rosengarten R, Kirchhoff H (1987) Gliding motility of Mycoplasma sp. nov. Strain 163 K. J Bacteriol 169:1891–1898

    PubMed  CAS  Google Scholar 

  29. Rosengarten R, Wise KS (1990) Phenotypic switching in mycoplasmas: phase variation of diverse surface lipoproteins. Science 247:315–318

    Article  PubMed  CAS  Google Scholar 

  30. 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 Bacteriol 183:1621–1630

    Article  PubMed  CAS  Google Scholar 

  31. Seto S, Uenoyama A, Miyata M (2005) Identification of 521-kilodalton protein (Gli521) involved in force generation or force transmission for Mycoplasma mobile gliding. J Bacteriol 187:3502–3510

    Article  PubMed  CAS  Google Scholar 

  32. Shen X, Gumulak J, Yu H, French CT, Zou N, Dybvig K (2000) Gene rearrangements in the vsa locus of Mycoplasma pulmonis. J Bacteriol 182:2900–2908

    Article  PubMed  CAS  Google Scholar 

  33. Sirand-Pugnet P, Lartigue C, Marenda M, Jacob D, Barre A, Barbe V, Schenowitz C, Mangenot S, Couloux A, Segurens B, de Daruvar A, Blanchard A, Citti C (2007) Being pathogenic, plastic, and sexual while living with a nearly minimal bacterial genome. PLoS Genet 3:e75

    Article  PubMed  Google Scholar 

  34. Sitaraman R, Denison AM, Dybvig K (2002) A unique, bifunctional site-specific DNA recombinase from Mycoplasma pulmonis. Mol Microbiol 46:1033–1040

    Article  PubMed  CAS  Google Scholar 

  35. Stadtlander CT, Kirchhoff H (1995) Attachment of Mycoplasma mobile 163 K to piscine gill arches and rakers–light, scanning and transmission electron microscopic findings. Br Vet J 151:89–100

    Article  PubMed  CAS  Google Scholar 

  36. Stadtlander CT, Lotz W, Korting W, Kirchhoff H (1995) Piscine gill epithelial cell necrosis due to Mycoplasma mobile strain 163 K: comparison of in vivo and in vitro infection. J Comp Pathol 112:351–359

    Article  CAS  Google Scholar 

  37. 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 Bacteriol 186:1537–1545

    Article  PubMed  CAS  Google Scholar 

  38. Uenoyama A, Miyata M (2005) Identification of a 123-kilodalton protein (Gli123) involved in machinery for gliding motility of Mycoplasma mobile. J Bacteriol 187:5578–5584

    Article  PubMed  CAS  Google Scholar 

  39. van der Woude MW, Baumler AJ (2004) Phase and antigenic variation in bacteria. Clin Microbiol Rev 17:581–611

    Article  PubMed  Google Scholar 

  40. Weisburg WG, Tully JG, Rose DL, Petzel JP, Oyaizu H, Yang D, Mandelco L, Sechrest J, Lawrence TG, Van Etten J, Maniloff J, Woese CR (1989) A phylogenetic analysis of the mycoplasmas: basis for their classification. J Bacteriol 171:6455–6467

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Mr. Adan-Kubo Jun for helpful discussions. This study was supported by a Grant-in-Aid for Scientific Research (A) (to Makoto Miyata) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan, and by a grant from the Institution for Fermentation Osaka (to Makoto Miyata).

Author information

Authors and Affiliations

  1. Department of Biology, Graduate School of Science, Osaka City University, Sumiyoshi-ku, Osaka, 558-8585, Japan

    Heng Ning Wu, Chie Kawaguchi, Daisuke Nakane & Makoto Miyata

Authors
  1. Heng Ning Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chie Kawaguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daisuke Nakane
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Makoto Miyata
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Makoto Miyata.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wu, H.N., Kawaguchi, C., Nakane, D. et al. “Mycoplasmal Antigen Modulation,” a Novel Surface Variation Suggested for a Lipoprotein Specifically Localized on Mycoplasma mobile . Curr Microbiol 64, 433–440 (2012). https://doi.org/10.1007/s00284-012-0090-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-012-0090-y

Keywords

Search

Navigation