1887

Abstract

Summary: The nucleotide sequences of two gene clusters, and involved in the synthesis of type 5 and type 8 capsular polysaccharides (CPs), respectively, were determined. Each gene cluster contained 16 ORFs, which were named through for type 5 CP and through for type 8 CP. The and loci were allelic and were mapped to the l-G fragment in the standard l map of strain NCTC 8325. The predicted gene products of through and through are essentially identical to those of through and through respectively, with very few amino acid substitutions. Four ORFs located in the central region of each locus are type-specific. A comparison of the predicted amino acid sequences of and with sequences found in the databases allowed tentative assignment of functions to 15 of the 16 ORFs. The majority of the capsule genes are likely to be involved in amino sugar synthesis; the remainder are likely to be involved in sugar transfer, capsule chain-length regulation, polymerization and transport.

Funding
This study was supported by the:
  • NIH, and by the Health Research Board of Ireland (Award AI29040 and AI37027)
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1997-07-01
2024-03-29
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References

  1. Albus A., Fournier J. M., Wolz C., Boutonnier A., Ranke M., Hoiby N., Hochkeppel H., Doring G. 1988; Staphylococcus aureus capsular types and antibody response to lung infection in patients with cystic fibrosis. J Clin Microbiol 26:2205–2209
    [Google Scholar]
  2. Albus A., Arbeit R. D., Lee J. C. 1991; Virulence of Staphylococcus aureus mutants altered in type 5 capsule production. Infect Immun 59:1008–1014
    [Google Scholar]
  3. Allen A., Maskell D. 1996; The identification, cloning and mutagenesis of a genetic locus required for lipopolysaccharide biosynthesis in Bordetella pertussis . Mol Microbiol 19:37–52
    [Google Scholar]
  4. Altschul A. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410
    [Google Scholar]
  5. Arbeit R. D., Karakawa W. W., Vann., W. F. & Robbins J. B. 1984; Predominance of two newly described capsular polysaccharide types among clinical isolates of Staphylococcus aureus . Diagn Microbiol Infect Dis 2:85–91
    [Google Scholar]
  6. Ardourel M., Lortet G., Maillet F., Roche P., Truchet G., Promé, J. C. & Rosenberg C. 1995; In Rhizobium meliloti, the operon associated with the nod box n5 comprises nodL, noeA and noeB, three host-range genes specifically required for the nodulation of particular Medicago species. Mol Microbiol 17:687–699
    [Google Scholar]
  7. Baddour L. M., Lowrance C., Albus A., Lowrance J. H., Anderson S. K., Lee J. C. 1992; Staphylococcus aureus microcapsule expression attenuates bacterial virulence in a rat model of experimental endocarditis. J Infect Dis 165:749–753
    [Google Scholar]
  8. Bastin D. A., Stevenson G., Brown P. K., Haase A., Reeves P. 1993; Repeat unit polysaccharides of bacteria: a model for polymerization resembling that of ribosomes and fatty acid synthetase, with a novel mechanism for determining chain length. Mol Microbiol 7:725–734
    [Google Scholar]
  9. Batchelor R. A., Alifano P., Biffali E., Hull S., Hull R. 1992; Nucleotide sequences of the genes regulating O-polysaccharide antigen chain length (rol) from Escherichia coli and Salmonella typhimurium: protein homology and functional complementation. J Bacteriol 174:5228–5236
    [Google Scholar]
  10. Becker A., Niehaus K., Pühler A. 1995; Low-molecular-weight succinoglycan is predominantly produced by Rhizobium meliloti strains carrying a mutated ExoP protein characterized by a periplasmic N-terminal domain and a missing C-terminal domain. Mol Microbiol 16:191–203
    [Google Scholar]
  11. Birnboim H. C. 1983; A rapid alkaline extraction method for the isolation of plasmid DNA. Methods Enzymol 100:243–255
    [Google Scholar]
  12. Bult C. J., White O., Olsen G. J. & 37 other authors 1996; Complete genome sequence of the methanogenic Archaeon, Methanococcus jannaschii . Science 273:1058–1073
    [Google Scholar]
  13. Comstock L. E., Johnson J. A., Michalski J. M., Morris J. G., Jr & Kaper J. B. 1996; Cloning and sequence of a region encoding a surface polysaccharide of Vibrio cholerae O139 and characterization of the insertion site in the chromosome of Vibrio cholerae O1. Mol Microbiol 19:815–826
    [Google Scholar]
  14. Daniels D., L, Plunkett G., III, Burland V., Blattner F. R. 1992; Analysis of the Escherichia coli genome: DNA sequence of the region from 84.5 to 86.5 minutes. Science 257:771–778
    [Google Scholar]
  15. Deretic V., Gill J. F., Chakrabarty A. M. 1987a; Pseudomonas aeruginosa infection in cystic fibrosis: nucleotide sequence and transcriptional regulation of the algD gene. Nucleic Acids Res 15:4567–4581
    [Google Scholar]
  16. Deretic V., Gill J. F., Chakrabarty A. M. 1987b; Gene algD coding for GDP-mannose dehydrogenase is transcriptionally activated in mucoid Pseudomonas aeruginosa . J Bacteriol 169:351–358
    [Google Scholar]
  17. Downie J. A. 1989; The nodL gene from Rhizobium leguminosarum is homologous to the acetyl transferases encoded by lacA and cysE . Mol Microbiol 3:1649–1651
    [Google Scholar]
  18. Fath M., Kolter R. 1993; ABC transporters: bacterial exporters. Microbiol Rev 57:995–1017
    [Google Scholar]
  19. Fattom A. I., Sarwar J., Ortiz A., Naso R. 1996; A Staphylococcus aureus capsular polysaccharide (CP) vaccine and CP-specific antibodies protect mice against bacterial challenge. Infect Immun 64:1659–1665
    [Google Scholar]
  20. Fournier J. M., Vann W. F., Karakawa W. W. 1984; Purification and characterization of Staphylococcus aureus type 8 capsular polysaccharide. Infect Immun 45:87–93
    [Google Scholar]
  21. Goering R. V., Winters M. A. 1992; Rapid method for epidemiological evaluation of gram-positive cocci by field inversion gel electrophoresis. J Clin Microbiol 30:577–580
    [Google Scholar]
  22. Guidolin A., Morona J. K., Morona R., Hansman D., Paton J. 1994; Nucleotide sequence analysis of genes essential for capsular polysaccharide biosynthesis in Streptococcus pneumoniae type 19F. Infect Immun 62:5384–5396
    [Google Scholar]
  23. Hanessian S., Haskell T. H. 1964; Structural studies on staphylococcal polysaccharide antigens. J Biol Chem 239:2758–2764
    [Google Scholar]
  24. Hediger M., A, Johnson D. F., Nierlich D. P., Zabin I. 1985; DNA sequence of the lactose operon: the lacA gene and the transcriptional termination region. Proc Natl Acad Sci USA 82:6414–6418
    [Google Scholar]
  25. Higgins D. G., Sharp P. M. 1988; clustal: a package for performing multiple sequence alignments on a microcomputer. Gene 73:237–244
    [Google Scholar]
  26. Hochkeppel H. K., Braun D. G., Vischer W., Imm A., Sutter S., Staeubli, U” Guggenheim R., Kaplan E. L., Boutonnier A., Fournier J. M. 1987; Serotyping and electron microscopy studies of Staphylococcus aureus clinical isolates with monoclonal antibodies to capsular polysaccharide type 5 and type 8. J Clin Microbiol 25:526–530
    [Google Scholar]
  27. Houng H. H.-S., Kopecko D., Baron L. S. 1990; Molecular cloning and physical and functional characterization of the Salmonella typhimurium and Salmonella typhi galactose utilization operons. J Bacteriol 172:4392–4398
    [Google Scholar]
  28. Huang J., Schell M. 1995; Molecular characterization of the eps gene cluster of Pseudomonas solanacearum and its transcriptional regulation at a single promoter. Mol Microbiol 16:977–989
    [Google Scholar]
  29. Ielpi L., Couso R. O., Dankert M. A. 1993; Sequential assembly and polymerization of the polyprenol-linked pentasaccharide repeat unit of the xanthan polysaccharide in Xanthomonas campestris . J Bacteriol 175:2490–2500
    [Google Scholar]
  30. Jiang X.-M., Santiago N. R., Lee S. L., Romana L. K., Reeves P. R. 1991; Structure and sequence of the rfb (O antigen) gene cluster of Salmonella serovar typhimurium (strain LT2). Mol Microbiol 5:695–713
    [Google Scholar]
  31. Karakawa W. W., Vann W. F. 1982; Capsular polysaccharides of Staphylococcus aureus . Semin Infect Dis 4:285–293
    [Google Scholar]
  32. Karakawa W. W., Fournier J. M., Vann W., F” Arbeit R., Schneerson R., Robbins J. B. 1985; Method for the serological typing of the capsular polysaccharides of Staphylococcus aureus . J Clin Microbiol 22:445–447
    [Google Scholar]
  33. Karakawa W. W., Sutton A., Schneerson R., Karpas A., Vann W. F. 1988; Capsular antibodies induce type-specific phagocytosis of Staphylococcus aureus by human polymorphonuclear leukocytes. Infect Immun 56:1090–1095
    [Google Scholar]
  34. Keenleyside W. J., Whitfield C. 1996; A novel pathway for O-polysaccharide biosynthesis in Salmonella enterica serovar Borreze. J Biol Chem 271:28581–28592
    [Google Scholar]
  35. Kido N., Torgov V. I., Sugiyama T., Uchiya K., Sugihara H., Komatsu T., Kato N., Jann K. 1995; Expression of the O9 polysaccharide of Escherichia coli: sequencing of the E. coli O9 rfb gene cluster, characterization of mannosyl transferases, and evidence for an ATP-binding cassette transport system. J Bacteriol 177:2178–2187
    [Google Scholar]
  36. Klein P., Kanehisa M., Delisi C. 1985; The detection and classification of membrane-spanning proteins. Biochim Biophys Acta 815:468–476
    [Google Scholar]
  37. Kyte J., Doolittle R. F. 1982; A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132
    [Google Scholar]
  38. Lee C. Y. 1992; Cloning of genes affecting capsule expression in Staphylococcus aureus strain M . Mol Microbiol 6:1515–1522
    [Google Scholar]
  39. Lee C. Y., Buranen S. L., Ye Z. H. 1991; Construction of single-copy integration vectors for Staphylococcus aureus . Gene 103:101–105
    [Google Scholar]
  40. Lee J. C., Betley M. J., Hopkins C. A., Perez N. E., Pier G. B. 1987; Virulence studies, in mice, of transposon-induced mutants of Staphylococcus aureus differing in capsule size. J Infect Dis 156:741–750
    [Google Scholar]
  41. Lee J. C., Xu S., Albus A., Livoisi P. J. 1994; Genetic analysis of type 5 capsular polysaccharide expression by Staphylococcus aureus . J Bacteriol 176:4883–4889
    [Google Scholar]
  42. Lee J. C., Albus A., Livoisi P. J. 1995 Identification of a gene essential for O-acetylation of the Staphylococcus aureus type 5 capsular polysaccharide.. In Abstracts of the 95th Annual Meeting of the American Society for Microbiology , abstract no. B453 Washington, DC: American Society for Microbiology;
    [Google Scholar]
  43. Lee J. C., Park J.-S., Shepherd S. E., Fattom A. 1996 Protective efficacy of antibodies to the Staphylococcus aureus capsular polysaccharides to a rat model of endocarditis. . In Abstracts of the 96th Annual Meeting of the American Society for Microbiology , abstract no. B328 Washington, DC: American Society for Microbiology;
    [Google Scholar]
  44. Lemaire H.-G., Müller-Hill B. 1986; Nucleotide sequences of the galE gene and the galT gene of E. coli . Nucleic Acids Res 14:7705–7711
    [Google Scholar]
  45. Lin W. S., Cunneen T., Lee C. Y. 1994; Sequence analysis and molecular characterization of genes required for the biosynthesis of type 1 capsular polysaccharide in Staphylococcus aureus . J Bacteriol 176:7005–7016
    [Google Scholar]
  46. Liu D., Cole R. A., Reeves P. R. 1996; An O-antigen processing function for Wzx (RfbX): a promising candidate for O-unit flippase. J Bacteriol 178:2102–2107
    [Google Scholar]
  47. Macpherson D. F., Manning P. A., Morona R. 1994; Characterization of the dTDP-rhamnose biosynthetic genes encoded in the rfb locus of Shigella flexneri . Mol Microbiol 11:281–292
    [Google Scholar]
  48. Marolda C. L., Valvano M. A. 1995; Genetic analysis of the dTDP-rhamnose biosynthesis region of the Escherichia coli VW187 (O7:K1) rfb gene cluster: identification of functional homologs of rfbB and rfbA in the rff cluster and correct location of the rffE gene. J Bacteriol 177:5539–5546
    [Google Scholar]
  49. Meier-Dieter U., Starman R., Barr K., Mayer H., Rick P. D. 1990; Biosynthesis of enterobacterial common antigen in Escherichia coli . J Biol Chem 265:13490–13497
    [Google Scholar]
  50. Melly M. A., Duke L. J., Liau D. F., Hash J. H. 1974; Biological properties of the encapsulated Staphylococcus aureus M. Infect Immun 10:389–397
    [Google Scholar]
  51. Moreau M., Richards J. C., Fournier J. M., Byrd R. A., Karakawa W. W., Vann W. F. 1990; Structure of the type-5 capsular polysaccharide of Staphylococcus aureus . Carbohydr Res 201:285–297
    [Google Scholar]
  52. Morona R., Mavris M., Faliarino A., Manning P. A. 1994; Characterization of the rfc region of Shigella flexneri . J Bacteriol 176:733–747
    [Google Scholar]
  53. Morona R., van den Bosch L., Manning P. A. 1995; Molecular, genetic, and topological characterization of O-antigen chain length regulation in Shigella flexneri . J Bacteriol 177:1059–1068
    [Google Scholar]
  54. Murthy S. V. K., N., Melly M. A., Harris T. M., Hellerqvist C. G., Hash J. H. 1983; The repeating sequence of the capsular polysaccharide of Staphylococcus aureus . Carbohydr Res 117:113–123
    [Google Scholar]
  55. Nemeth J., Lee J. C. 1995; Antibodies to capsular polysaccharides are not protective against experimental Staphylococcus aureus endocarditis. Infect Immun 63:375–380
    [Google Scholar]
  56. Oeding P. 1983 Taxonomy and identification. . In Staphylococci and Staphylococcal Infections , pp. 1–32 . Edited by Easmon C. S. G., Adlam G. New York: Academic Press;
    [Google Scholar]
  57. Parent R., Roy P. H. 1992; The chloramphenicol acetyltransferase gene of Tn2424: a new breed of cat. J Bacteriol 174:2891–2897
    [Google Scholar]
  58. Pattee P. A., Lee H. C., Bannantine J. P. 1992 Genetic and physical mapping of the chromosome of Staphylococcus aureus. . In Molecular Biology of the Staphylococci , pp. 41–67 . Edited by Novick R. P. New York: VCH;
    [Google Scholar]
  59. Peterson P. K., Wilkinson B. J., Kim Y., Schmeling D., Quie P. G. 1978; Influence of encapsulation on staphylococcal opsonization and phagocytosis by human polymorphonuclear leukocytes. Infect Immun 19:943–949
    [Google Scholar]
  60. Poutrel B., Boutonnier A., Sutra L., Fournier J. M. 1988; Prevalence of capsular polysaccharide types 5 and 8 among Staphylococcus aureus isolates from cow, goat, and ewe milk. J Clin Microbiol 26:38–40
    [Google Scholar]
  61. Rubens C. E., Heggen L. M., Haft R. G., Wessels M. R. 1993; Identification of cpsD, a gene essential for type III capsule expression in group B streptococci. Mol Microbiol 8:844–855
    [Google Scholar]
  62. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor; NY: Cold Spring Harbor Laboratory:
    [Google Scholar]
  63. Sanger F., Nicklen S., Coulson A. R. 1977; DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467
    [Google Scholar]
  64. Sau S., Lee C. Y. 1996; Cloning of type 8 capsule genes and analysis of gene clusters for the production of different capsular polysaccharides in Staphylococcus aureus . J Bacteriol 178:2118–2126
    [Google Scholar]
  65. Sau S., Sun J., Lee C. Y. 1997; Molecular characterization and transcriptional analysis of type 8 genes in Staphylococcus aureus . J Bacteriol 179:1614–1621
    [Google Scholar]
  66. Skurnik M., Venho R., Toivanen P., Al-Hendy A. 1995; A novel locus of Yersinia enterocolitica serotype O:3 involved in lipopolysaccharide outer core biosynthesis. Mol Microbiol 17:575–594
    [Google Scholar]
  67. Soldo B., Lazarevic V., Margot P., Karamata D. 1993; Sequencing and analysis of the divergon comprising gtaB, the structural gene of UDP-glucose pyrophosphorylase of Bacillus subtilis 168. J Gen Microbiol 139:3185–3195
    [Google Scholar]
  68. Sompolinsky E., Samra, Z” Karakawa W. W., Vann W. F., Schneerson R., Malik Z. 1985; Encapsulation and capsular types in isolates of Staphylococcus aureus from different sources and relationship to phage types. J Clin Microbiol 22:828–834
    [Google Scholar]
  69. Stevenson G., Andrianopoulos K., Hobbs M., Reeves P. R. 1996; Organization of the Escherichia coli K-12 gene cluster responsible for production of the extracellular polysaccharide colanic acid. J Bacteriol 178:4885–4893
    [Google Scholar]
  70. Stingele F., Neeser J.-R., Mollet B. 1996; Identification and characterization of the eps (exopolysaccharide) gene cluster from Streptococcus thermophilus Sfi6. J Bacteriol 178:1680–1690
    [Google Scholar]
  71. Vanderslice R. W., Doherty D. H., Capage M. A., Betlach M. R., Hassler R. A., Henderson N. M., Ryan-Graniera J., Techlenberg M. 1989 Genetic engineering of polysaccharide structure in Xanthomonas campestris. . In Biomedical and Biotechnological Advances in Industrial Polysaccharides , pp. 145–156 Edited by Crescenzi V., Dea I. C. M., Paoletti S., Stivala S., Sutherland I. New York: Godon & Breach Science Publishers;
    [Google Scholar]
  72. Wang L., Liu D., Reeves P. R. 1996; C-terminal half of Salmonella enterica WbaP (RfbP) is the galactosyl-1-phosphate transferase domain catalyzing the first step of O-antigen synthesis. J Bacteriol 178:2598–2604
    [Google Scholar]
  73. Whitfield C. 1995; Biosynthesis of lipopolysaccharide O antigens. Trends Microbiol 3:178–185
    [Google Scholar]
  74. Wierenga R. K., Terpstra P., Hoi W. G. J. 1986; Prediction of the occurrence of the ADP-binding βαβ-fold in proteins, using an amino acid sequence fingerprint. J Mol Biol 187:101–107
    [Google Scholar]
  75. Wilkinson B. J. 1983 Staphylococcal capsules and slime. . In Staphylococci and Staphylococcal Infections , pp. 481–523 . Edited by Easmon C. S. G., Adlam G. New York: Academic Press;
    [Google Scholar]
  76. Xu S., Arbeit R. D., Lee J. C. 1992; Phagocytic killing of encapsulated and microencapsulated Staphylococcus aureus by human polymorphonuclear leukocytes. Infect Immun 60:1358–1362
    [Google Scholar]
  77. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mpl8 and pUC19 vectors. Gene 33:103–119
    [Google Scholar]
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