1887

Abstract

Lipooligosaccharide (LOS) is a major virulence factor of the pathogenic . Nine genes at three chromosomal loci (, , ) encoding the glycosyltransferases responsible for the biosynthesis of LOS oligosaccharide chains were examined in 26 , 51 and 18 commensal strains. DNA hybridization, PCR and nucleotide sequence data were compared to previously reported genes. Analysis of the genetic organization of the loci revealed that in , the and loci were hypervariable genomic regions, whereas the locus was conserved. In , no variability in the composition or organization of the three loci was observed. genes were detected only in some commensal species. The genetic organization of the locus was classified into eight types and the locus was classified into four types. Two types of arrangement at (II and IV) and one type of arrangement at (IV) were novel genetic organizations reported in this study. Based on the three loci, 10 LOS genotypes of were distinguished. Phylogenetic analysis revealed a gene cluster, , which separated from the homologous genes and . The and genes were mutually exclusive and were located at the same position in . The data demonstrated that pathogenic and commensal share a common gene pool and horizontal gene transfer appears to contribute to the genetic diversity of the loci in .

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2002-06-01
2019-12-13
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References

  1. Arking, D., Tong, Y. & Stein, D. C. ( 2001; ). Analysis of lipooligosaccharide biosynthesis in the neisseriaceae. J Bacteriol 183, 934-941.[CrossRef]
    [Google Scholar]
  2. Banerjee, A., Wang, R., Uljon, S. N., Rice, P. A., Gotschlich, E. C. & Stein, D. C. ( 1998; ). Identification of the gene (lgtG) encoding the lipooligosaccharide β chain synthesizing glucosyl transferase from Neisseria gonorrhoeae. Proc Natl Acad Sci USA 95, 10872-10877.[CrossRef]
    [Google Scholar]
  3. Burch, C. L., Danaher, R. J. & Stein, D. C. ( 1997; ). Antigenic variation in Neisseria gonorrhoeae: production of multiple lipooligosaccharides. J Bacteriol 179, 982-986.
    [Google Scholar]
  4. Danaher, R. J., Levin, J. C., Arking, D., Burch, C. L., Sandlin, R. & Stein, D. C. ( 1995; ). Genetic basis of Neisseria gonorrhoeae lipooligosaccharide antigenic variation. J Bacteriol 177, 7275-7279.
    [Google Scholar]
  5. Devereux, J., Haeberli, P. & Smithies, O. ( 1984; ). A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12, 387-395.[CrossRef]
    [Google Scholar]
  6. Erwin, A. L., Haynes, P. A., Rice, P. A. & Gotschlich, E. C. ( 1996; ). Conservation of the lipooligosaccharide synthesis locus lgt among strains of Neisseria gonorrhoeae: requirement for lgtE in synthesis of the 2C7 epitope and of the β chain of strain 15253. J Exp Med 184, 1233-1241.[CrossRef]
    [Google Scholar]
  7. Gotschlich, E. C. ( 1994; ). Genetic locus for the biosynthesis of the variable portion of Neisseria gonorrhoeae lipooligosaccharide. J Exp Med 180, 2181-2190.[CrossRef]
    [Google Scholar]
  8. Harvey, H. A., Porat, N., Campbell, C. A., Jennings, M., Gibson, B. W., Phillips, N. J., Apicella, M. A. & Balke, M. S. ( 2000; ). Gonococcal lipooligosaccharide is a ligand for the asialoglycoprotein receptor on human sperm. Mol Microbiol 36, 1059-1070.[CrossRef]
    [Google Scholar]
  9. Jennings, M. P., Hood, D. W., Peak, I. R., Virji, M. & Moxon, E. R. ( 1995; ). Molecular analysis of a locus for the biosynthesis and phase-variable expression of the lacto-N-neotetraose terminal lipopolysaccharide structure in Neisseria meningitidis. Mol Microbiol 18, 729-740.[CrossRef]
    [Google Scholar]
  10. Jennings, M. P., Srikhanta, Y. N., Moxon, E. R., Kramer, M., Poolman, J. T., Kuipers, B. & van der Ley, P. ( 1999; ). The genetic basis of the phase variation repertoire of lipopolysaccharide immunotypes in Neisseria meningitidis. Microbiology 145, 3013-3021.
    [Google Scholar]
  11. Kahler, C. M. & Stephens, D. S. ( 1998; ). Genetic bases for biosynthesis, structure and function of meningococcal lipooligosaccharide. Crit Rev Microbiol 24, 281-334.
    [Google Scholar]
  12. Kahler, C. M., Carlson, R. W., Rahman, M. M., Martin, L. E. & Stephens, D. S. ( 1996a; ). Two glycosyltransferase genes, lgtF and rfaK, constitute the lipooligosaccharide ice (inner core extension) biosynthesis operon of Neisseria meningitidis. J Bacteriol 178, 6677-6684.
    [Google Scholar]
  13. Kahler, C. M., Carlson, R. W., Rahman, M. M., Martin, L. E. & Stephens, D. S. ( 1996b; ). Inner core biosynthesis of lipooligosaccharide (LOS) in Neisseria meningitidis serogroup B: identification and role in LOS assembly of the α1,2 N-acetylglucosamine transferase (RfaK). J Bacteriol 178, 1265-1273.
    [Google Scholar]
  14. Kumar, S., Tamura, K. & Nei, M. ( 1994; ). MEGA: Molecular Evolutionary Genetics Analysis software for microcomputers. Comput Appl Biosci 10, 189-191.
    [Google Scholar]
  15. Li, W. H. ( 1993; ). Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol 36, 96-99.[CrossRef]
    [Google Scholar]
  16. Li, W. H., Wu, C. I. & Luo, C. C. ( 1985; ). A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol 2, 150-174.
    [Google Scholar]
  17. Linz, B., Schenker, M., Zhu, P. & Achtman, M. ( 2000; ). Frequent interspecific genetic exchange between commensal neisseriae and Neisseria meningitidis. Mol Microbiol 36, 1049-1058.[CrossRef]
    [Google Scholar]
  18. Mandrell, R. E. & Zollinger, W. D. ( 1977; ). Lipopolysaccharide serotyping of Neisseria meningitidis by hemagglutination inhibition. Infect Immun 16, 471-475.
    [Google Scholar]
  19. Minor, S. Y., Banerjee, A. & Gotschlich, E. C. ( 2000; ). Effect of α-oligosaccharide phenotype of Neisseria gonorrhoeae strain MS11 on invasion of Chang conjunctival, HEC-1-B endometrial, and ME-180 cervical cells. Infect Immun 68, 6526-6534.[CrossRef]
    [Google Scholar]
  20. O’Brien, J. P., Goldenberg, D. L. & Rice, P. A. ( 1983; ). Disseminated gonococcal infection: a prospective analysis of 49 patients and a review of pathophysiology and immune mechanisms. Medicine 62, 395-406.[CrossRef]
    [Google Scholar]
  21. Olyhoek, A. J. M., Sarkari, J., Bopp, M., Morelli, G. & Achtman, M. ( 1991; ). Cloning and expression in Escherichia coli of opc, the gene for an unusual class 5 outer membrane protein from Neisseria meningitidis (meningococci/surface antigen). Microb Pathog 11, 249-257.[CrossRef]
    [Google Scholar]
  22. Parkhill, J., Achtman, M., James, K. D. & 25 other authors ( 2000; ). Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491. Nature 404, 502–506.[CrossRef]
    [Google Scholar]
  23. Preston, A., Mandrell, R. E., Gibson, B. W. & Apicella, M. A. ( 1996; ). The lipooligosaccharides of pathogenic Gram-negative bacteria. Crit Rev Microbiol 22, 139-180.[CrossRef]
    [Google Scholar]
  24. Saitou, N. & Nei, M. ( 1987; ). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406-425.
    [Google Scholar]
  25. Sarkari, J., Pandit, N., Moxon, E. R. & Achtman, M. ( 1994; ). Variable expression of the Opc outer membrane protein in Neisseria meningitidis is caused by size variation of promoter containing poly-cytidine. Mol Microbiol 13, 207-217.[CrossRef]
    [Google Scholar]
  26. Spratt, B. G., Bowler, L. D., Zhang, Q. Y., Zhou, J. & Smith, J. M. ( 1992; ). Role of interspecies transfer of chromosomal genes in the evolution of penicillin resistance in pathogenic and commensal Neisseria species. J Mol Evol 34, 115-125.
    [Google Scholar]
  27. Tettelin, H., Saunders, N. J., Heidelberg, J. & 39 other authors ( 2000; ). Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science 278, 1809–1815.
    [Google Scholar]
  28. van der Ley, P., Kramer, M., Martin, A., Richards, J. C. & Poolman, J. T. ( 1997; ). Analysis of the icsBA locus required for biosynthesis of the inner core region from Neisseria meningitidis lipopolysaccharide. FEMS Microbiol 146, 247-253.[CrossRef]
    [Google Scholar]
  29. Verheul, A. F. M., Snippe, H. & Poolman, J. T. ( 1993; ). Meningococcal lipopolysaccharides: virulence factor and potential vaccine component. Microbiol Rev 57, 34-39.
    [Google Scholar]
  30. Wakarchuk, W., Martin, A., Jennings, M. P., Moxon, E. R. & Richards, J. C. ( 1996; ). Functional relationships of the genetic locus encoding the glycosyltransferase enzymes involved in expression of the lacto-N-neotetraose terminal lipopolysaccharide structure in Neisseria meningitidis. J Biol Chem 271, 19166-19173.[CrossRef]
    [Google Scholar]
  31. Yang, Q. L. & Gotschlich, E. C. ( 1996; ). Variation of gonococcal lipooligosaccharide structure is due to alterations in poly-G tracts in lgt genes encoding glycosyltransferases. J Exp Med 183, 323-327.[CrossRef]
    [Google Scholar]
  32. Zhu, P., Klutch, M. J. & Tsai, C. M. ( 2001; ). Genetic analysis of conservation and variation of lipooligosaccharide expression in two L8-immunotype strains of Neisseria meningitidis. FEMS Microbiol Lett 203, 173-177.[CrossRef]
    [Google Scholar]
  33. Zollinger, W. D. & Mandrell, R. E. ( 1977; ). Outer-membrane protein and lipopolysaccharide serotyping of Neisseria meningitidis by inhibition of a solid-phase radioimmunoassay. Infect Immun 18, 424-433.
    [Google Scholar]
  34. Zollinger, W. D. & Mandrell, R. E. ( 1980; ). Type-specific antigens of group A Neisseria meningitidis: lipopolysaccharide and heat-modifiable outer membrane proteins. Infect Immun 28, 451-458.
    [Google Scholar]
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