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. 1995 Oct;177(19):5636–5643. doi: 10.1128/jb.177.19.5636-5643.1995

Increased structural and combinatorial diversity in an extended family of genes encoding Vlp surface proteins of Mycoplasma hyorhinis.

D Yogev 1, R Watson-McKown 1, R Rosengarten 1, J Im 1, K S Wise 1
PMCID: PMC177375  PMID: 7559353

Abstract

Variable lipoproteins (Vlp) constitute the major coat protein of Mycoplasma hyorhinis. They are products of multiple, divergent, single-copy genes organized in a chromosomal cluster. Three genes, vlpA, vlpB, and vlpC, have been previously identified in clonal isolates of M. hyorhinis SK76. Each is linked to a characteristic promoter region containing a homopolymeric tract of adenine residues [poly(A) tract], subject to hypermutation, that transcriptionally controls phase variation of vlp genes and leads to combinatorial surface mosaics of distinct Vlp products. The size of the natural vlp gene repertoire is unknown but may critically determine the degree of structural and combinatorial diversity available in this species. In this study, the vlp repertoire of M. hyorhinis GDL-1 was characterized and shown to contain three additional genes, vlpD, vlpE, and vlpF, clustered with other known vlp genes in the order 5'-vlpD-vlpE-vlpF-IS-vlpA-IS-vlpB-vlpC+ ++-3', where IS represents copies of the IS1221 element of M. hyorhinis. The 5' boundary of this expanded family was identical to that of the more limited family 5'-vlpA-IS-vlpB-vlpC-3' previously described in a clonal isolate of strain SK76. A recombinant construct containing vlpD, vlpE, and vlpF expressed antigenically distinguishable products corresponding to each gene. These genes encode characteristic C-terminal repetitive regions that are subject to size variation by insertion or deletion of intragenic repeats but maintain an extended, charged structure. Each vlp gene also contained characteristic alternative open reading frames, which provide a potential reservoir of coding sequence for Vlp diversity, possibly recruited through insertion and/or deletion mutations. These findings demonstrate a vastly expanded potential for structural diversity and combinatorial display of surface mosaics on this organism and suggest that modulation of the vlp repertoire, possibly in conjunction with mobile elements, may determine the capacity for surface variation in natural populations and laboratory strains of this mycoplasma species.

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Selected References

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  1. Behrens A., Heller M., Kirchhoff H., Yogev D., Rosengarten R. A family of phase- and size-variant membrane surface lipoprotein antigens (Vsps) of Mycoplasma bovis. Infect Immun. 1994 Nov;62(11):5075–5084. doi: 10.1128/iai.62.11.5075-5084.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bhugra B., Dybvig K. Identification and characterization of IS1138, a transposable element from Mycoplasma pulmonis that belongs to the IS3 family. Mol Microbiol. 1993 Feb;7(4):577–584. doi: 10.1111/j.1365-2958.1993.tb01148.x. [DOI] [PubMed] [Google Scholar]
  3. Boyer M. J., Wise K. S. Lipid-modified surface protein antigens expressing size variation within the species Mycoplasma hyorhinis. Infect Immun. 1989 Jan;57(1):245–254. doi: 10.1128/iai.57.1.245-254.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Christiansen G., Mathiesen S. L., Nyvold C., Birkelund S. Analysis of a Mycoplasma hominis membrane protein, P120. FEMS Microbiol Lett. 1994 Aug 1;121(1):121–127. doi: 10.1111/j.1574-6968.1994.tb07085.x. [DOI] [PubMed] [Google Scholar]
  5. Cleavinger C. M., Kim M. F., Wise K. S. Processing and surface presentation of the Mycoplasma hyorhinis variant lipoprotein VlpC. J Bacteriol. 1994 Apr;176(8):2463–2467. doi: 10.1128/jb.176.8.2463-2467.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dramsi S., Dehoux P., Cossart P. Common features of gram-positive bacterial proteins involved in cell recognition. Mol Microbiol. 1993 Sep;9(5):1119–1121. doi: 10.1111/j.1365-2958.1993.tb01241.x. [DOI] [PubMed] [Google Scholar]
  8. Dybvig K. DNA rearrangements and phenotypic switching in prokaryotes. Mol Microbiol. 1993 Nov;10(3):465–471. doi: 10.1111/j.1365-2958.1993.tb00919.x. [DOI] [PubMed] [Google Scholar]
  9. Dybvig K., Simecka J. W., Watson H. L., Cassell G. H. High-frequency variation in Mycoplasma pulmonis colony size. J Bacteriol. 1989 Sep;171(9):5165–5168. doi: 10.1128/jb.171.9.5165-5168.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dybvig K., Yu H. Regulation of a restriction and modification system via DNA inversion in Mycoplasma pulmonis. Mol Microbiol. 1994 May;12(4):547–560. doi: 10.1111/j.1365-2958.1994.tb01041.x. [DOI] [PubMed] [Google Scholar]
  11. Engelberg-Kulka H., Schoulaker-Schwarz R. Regulatory implications of translational frameshifting in cellular gene expression. Mol Microbiol. 1994 Jan;11(1):3–8. doi: 10.1111/j.1365-2958.1994.tb00283.x. [DOI] [PubMed] [Google Scholar]
  12. Gourlay R. N., Wyld S. G., Poulton M. E. Some characteristics of mycoplasma virus Hr 1, isolated from and infecting Mycoplasma hyorhinis. Brief report. Arch Virol. 1983;77(1):81–85. doi: 10.1007/BF01314867. [DOI] [PubMed] [Google Scholar]
  13. Lenski R. E., Mittler J. E. The directed mutation controversy and neo-Darwinism. Science. 1993 Jan 8;259(5092):188–194. doi: 10.1126/science.7678468. [DOI] [PubMed] [Google Scholar]
  14. Markham P. F., Glew M. D., Sykes J. E., Bowden T. R., Pollocks T. D., Browning G. F., Whithear K. G., Walker I. D. The organisation of the multigene family which encodes the major cell surface protein, pMGA, of Mycoplasma gallisepticum. FEBS Lett. 1994 Oct 3;352(3):347–352. doi: 10.1016/0014-5793(94)00991-0. [DOI] [PubMed] [Google Scholar]
  15. Moxon E. R., Rainey P. B., Nowak M. A., Lenski R. E. Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr Biol. 1994 Jan 1;4(1):24–33. doi: 10.1016/s0960-9822(00)00005-1. [DOI] [PubMed] [Google Scholar]
  16. Osawa S., Muto A., Ohama T., Andachi Y., Tanaka R., Yamao F. Prokaryotic genetic code. Experientia. 1990 Dec 1;46(11-12):1097–1106. doi: 10.1007/BF01936919. [DOI] [PubMed] [Google Scholar]
  17. Relf W. A., Martin D. R., Sriprakash K. S. Antigenic diversity within a family of M proteins from group A streptococci: evidence for the role of frameshift and compensatory mutations. Gene. 1994 Jun 24;144(1):25–30. doi: 10.1016/0378-1119(94)90198-8. [DOI] [PubMed] [Google Scholar]
  18. Robertson B. D., Meyer T. F. Genetic variation in pathogenic bacteria. Trends Genet. 1992 Dec;8(12):422–427. doi: 10.1016/0168-9525(92)90325-x. [DOI] [PubMed] [Google Scholar]
  19. Rosengarten R., Behrens A., Stetefeld A., Heller M., Ahrens M., Sachse K., Yogev D., Kirchhoff H. Antigen heterogeneity among isolates of Mycoplasma bovis is generated by high-frequency variation of diverse membrane surface proteins. Infect Immun. 1994 Nov;62(11):5066–5074. doi: 10.1128/iai.62.11.5066-5074.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rosengarten R., Theiss P. M., Yogev D., Wise K. S. Antigenic variation in Mycoplasma hyorhinis: increased repertoire of variable lipoproteins expanding surface diversity and structural complexity. Infect Immun. 1993 May;61(5):2224–2228. doi: 10.1128/iai.61.5.2224-2228.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rosengarten R., Wise K. S. Phenotypic switching in mycoplasmas: phase variation of diverse surface lipoproteins. Science. 1990 Jan 19;247(4940):315–318. doi: 10.1126/science.1688663. [DOI] [PubMed] [Google Scholar]
  22. Rosengarten R., Wise K. S. The Vlp system of Mycoplasma hyorhinis: combinatorial expression of distinct size variant lipoproteins generating high-frequency surface antigenic variation. J Bacteriol. 1991 Aug;173(15):4782–4793. doi: 10.1128/jb.173.15.4782-4793.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sleytr U. B., Messner P. Crystalline surface layers in procaryotes. J Bacteriol. 1988 Jul;170(7):2891–2897. doi: 10.1128/jb.170.7.2891-2897.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sutcliffe I. C., Russell R. R. Lipoproteins of gram-positive bacteria. J Bacteriol. 1995 Mar;177(5):1123–1128. doi: 10.1128/jb.177.5.1123-1128.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tabor S., Richardson C. C. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1074–1078. doi: 10.1073/pnas.82.4.1074. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Wise K. S. Adaptive surface variation in mycoplasmas. Trends Microbiol. 1993 May;1(2):59–63. doi: 10.1016/0966-842X(93)90034-O. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wise K. S., Watson R. K. Mycoplasma hyorhinis GDL surface protein antigen p120 defined by monoclonal antibody. Infect Immun. 1983 Sep;41(3):1332–1339. doi: 10.1128/iai.41.3.1332-1339.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Yogev D., Menaker D., Strutzberg K., Levisohn S., Kirchhoff H., Hinz K. H., Rosengarten R. A surface epitope undergoing high-frequency phase variation is shared by Mycoplasma gallisepticum and Mycoplasma bovis. Infect Immun. 1994 Nov;62(11):4962–4968. doi: 10.1128/iai.62.11.4962-4968.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Yogev D., Rosengarten R., Watson-McKown R., Wise K. S. Molecular basis of Mycoplasma surface antigenic variation: a novel set of divergent genes undergo spontaneous mutation of periodic coding regions and 5' regulatory sequences. EMBO J. 1991 Dec;10(13):4069–4079. doi: 10.1002/j.1460-2075.1991.tb04983.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Yogev D., Watson-McKown R., McIntosh M. A., Wise K. S. Sequence and TnphoA analysis of a Mycoplasma hyorhinis protein with membrane export function. J Bacteriol. 1991 Mar;173(6):2035–2044. doi: 10.1128/jb.173.6.2035-2044.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Zheng J., McIntosh M. A. Characterization of IS1221 from Mycoplasma hyorhinis: expression of its putative transposase in Escherichia coli incorporates a ribosomal frameshift mechanism. Mol Microbiol. 1995 May;16(4):669–685. doi: 10.1111/j.1365-2958.1995.tb02429.x. [DOI] [PubMed] [Google Scholar]
  33. Zheng X., Teng L. J., Watson H. L., Glass J. I., Blanchard A., Cassell G. H. Small repeating units within the Ureaplasma urealyticum MB antigen gene encode serovar specificity and are associated with antigen size variation. Infect Immun. 1995 Mar;63(3):891–898. doi: 10.1128/iai.63.3.891-898.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]

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