1887

Abstract

is a major human and animal pathogen, most notable as a cause of life-threatening disease in neonates. is also called the Group B in reference to the diagnostically significant Lancefield Group B typing antigen. Although the structure of this complex carbohydrate antigen has been solved, little is known of its biosynthesis beyond the identification of a relevant locus in sequenced genomes. Analysis of the sugar linkages present in the Group B carbohydrate (GBC) structure has allowed us to deduce the minimum enzymology required to complete its biosynthesis. Most of the enzymes required to complete this biosynthesis can be identified within the putative biosynthetic locus. Surprisingly, however, three crucial -acetylglucosamine transferases and enzymes required for activated precursor synthesis are not apparently located in this locus. A model for GBC biosynthesis wherein the complete polymer is assembled at the cytoplasmic face of the plasma membrane before translocation to the cell surface is proposed. These analyses also suggest that GBC is the major teichoic acid-like polymer in the cell wall of , whereas lipoteichoic acid is the dominant poly(glycerophosphate) antigen. Genomic analysis has allowed us to predict the pathway leading to the biosynthesis of GBC of .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/014522-0
2008-05-01
2019-08-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/5/1354.html?itemId=/content/journal/micro/10.1099/mic.0.2007/014522-0&mimeType=html&fmt=ahah

References

  1. Alaimo, C., Catrein, I., Morf, L., Marolda, C. L., Callewaert, N., Valvano, M. A., Feldman, M. F. & Aebi, M. ( 2006; ). Two distinct but interchangeable mechanisms for flipping of lipid-linked oligosaccharides. EMBO J 25, 967–976.[CrossRef]
    [Google Scholar]
  2. Almeida, M. S., Herrmann, T., Peti, W., Wilson, I. A. & Wüthrich, K. ( 2005; ). NMR structure of the conserved hypothetical protein TM0487 from Thermotoga maritima: implications for 216 homologous DUF59 proteins. Protein Sci 14, 2880–2886.[CrossRef]
    [Google Scholar]
  3. Anthony, B. F., Concepcion, N. F. & Concepcion, K. F. ( 1985; ). Human-antibody to the group-specific polysaccharide of Group-B Streptococcus. J Infect Dis 151, 221–226.[CrossRef]
    [Google Scholar]
  4. Barabote, R. D. & Saier, M. H. ( 2005; ). Comparative genomic analysis of the bacterial phosphotransferase system. Microbiol Mol Biol Rev 69, 608–634.[CrossRef]
    [Google Scholar]
  5. Bentley, S. D., Aanensen, D. M., Mavroidi, A., Saunders, D., Rabbinowitsch, E., Collins, M., Donohoe, K., Harris, D., Murphy, L. & other authors ( 2006; ). Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet 2, e31 [CrossRef]
    [Google Scholar]
  6. Bhavsar, A. P. & Brown, E. D. ( 2006; ). Cell wall assembly in Bacillus subtilis: how spirals and spaces challenge paradigms. Mol Microbiol 60, 1077–1090.[CrossRef]
    [Google Scholar]
  7. Bourgoin, F., Pluvinet, A., Gintz, B., Decaris, B. & Guedon, G. ( 1999; ). Are horizontal transfers involved in the evolution of the Streptococcus thermophilus exopolysaccharide synthesis loci? Gene 233, 151–161.[CrossRef]
    [Google Scholar]
  8. Bradley, A. J. ( 2002; ). Bovine mastitis: an evolving disease. Vet J 164, 116–124.[CrossRef]
    [Google Scholar]
  9. Brooks, S., Apostol, M., Nadle, J., Wymore, K., Haubert, N., Burnite, S., Daniels, A., Hadler, J. L., Farley, M. M. & other authors ( 2006; ). Early-onset and late-onset neonatal Group B streptococcal disease – United States, 1996–2004. JAMA 295, 1371–1372.[CrossRef]
    [Google Scholar]
  10. Cieslewicz, M. J., Chaffin, D., Glusman, G., Kasper, D., Madan, A., Rodrigues, S., Fahey, J., Wessels, M. R. & Rubens, C. E. ( 2005; ). Structural and genetic diversity of Group B Streptococcus capsular polysaccharides. Infect Immun 73, 3096–3103.[CrossRef]
    [Google Scholar]
  11. Coutinho, P. M. & Henrissat, B. ( 1999; ). Carbohydrate-active enzymes: an integrated database approach. In Recent Advances in Carbohydrate Bioengineering, pp. 3–12. Edited by H. J. Gilbert, G. Davies, B. Henrissat & B. Svensson. Cambridge: The Royal Society of Chemistry.
  12. D'Elia, M. A., Millar, K. E., Beveridge, T. J. & Brown, E. D. ( 2006; ). Wall teichoic acid polymers are dispensable for cell viability in Bacillus subtilis. J Bacteriol 188, 8313–8316.[CrossRef]
    [Google Scholar]
  13. Damjanovic, M., Kharat, A. S., Eberhardt, A., Tomasz, A. & Vollmer, W. ( 2007; ). The essential tacF gene is responsible for the choline-dependent growth phenotype of Streptococcus pneumoniae. J Bacteriol 189, 7105–7111.[CrossRef]
    [Google Scholar]
  14. Davies, S., Gear, J. E., Mason, C. M. & McIntyre, S. M. ( 2003; ). Streptococcus grouping latex kits: evaluation of five commercially available examples. Br J Biomed Sci 60, 136–140.
    [Google Scholar]
  15. Deng, L. Y., Kasper, D. L., Krick, T. P. & Wessels, M. R. ( 2000; ). Characterization of the linkage between the type III capsular polysaccharide and the bacterial cell wall of Group B Streptococcus. J Biol Chem 275, 7497–7504.[CrossRef]
    [Google Scholar]
  16. Doran, K. S., Engelson, E. J., Khosravi, A., Maisey, H. C., Fedtke, I., Equils, O., Michelsen, K. S., Arditi, M., Peschel, A. & Nizet, V. ( 2005; ). Blood–brain barrier invasion by Group B Streptococcus depends upon proper cell-surface anchoring of lipoteichoic acid. J Clin Invest 115, 2499–2507.[CrossRef]
    [Google Scholar]
  17. Edwards, M. S. & Baker, C. J. ( 2005; ). Group B streptococcal infections in elderly adults. Clin Infect Dis 41, 839–847.[CrossRef]
    [Google Scholar]
  18. Erbing, B., Kenne, L., Lindberg, B., Helting, T. & Hammerschmid, F. ( 1986; ). Structural studies of a teichoic acid from Streptococcus agalactiae Type III. Carbohydr Res 156, 145–155.
    [Google Scholar]
  19. Finn, R. D., Mistry, J., Schuster-Böckler, B., Griffiths-Jones, S., Hollich, V., Lassmann, T., Moxon, S., Marshall, M., Khanna, A. & other authors ( 2006; ). Pfam: clans, web tools and services. Nucleic Acids Res 34, D247–D251.[CrossRef]
    [Google Scholar]
  20. Follens, A., Veiga-Da-Cunha, M., Merckx, R., Van Schaftingen, E. & Van Eldere, J. ( 1999; ). acs1 of Haemophilus influenzae type a capsulation locus region II encodes a bifunctional ribulose 5-phosphate reductase-CDP-ribitol pyrophosphorylase. J Bacteriol 181, 2001–2007.
    [Google Scholar]
  21. Glaser, P., Rusniok, C., Buchrieser, C., Chevalier, F., Frangeul, L., Msadek, T., Zouine, M., Couve, E., Lalioui, L. & other authors ( 2002; ). Genome sequence of Streptococcus agalactiae, a pathogen causing invasive neonatal disease. Mol Microbiol 45, 1499–1513.[CrossRef]
    [Google Scholar]
  22. Goldschmidt, J. C. & Panos, C. ( 1984; ). Teichoic acids of Streptococcus agalactiae: chemistry, cytotoxicity, and effect on bacterial adherence to human cells in tissue culture. Infect Immun 43, 670–677.
    [Google Scholar]
  23. Gray, K. J., Bennett, S. L., French, N., Phiri, A. J. & Graham, S. M. ( 2007; ). Invasive group B streptococcal infection in infants, Malawi. Emerg Infect Dis 13, 223–229.[CrossRef]
    [Google Scholar]
  24. Greenberg, D. N., Ascher, D. P., Yoder, B. A., Hensley, D. M., Heiman, H. S. & Keith, J. F. ( 1995; ). Sensitivity and specificity of rapid diagnostic tests for detection of Group B streptococcal antigen in bacteremic neonates. J Clin Microbiol 33, 193–198.
    [Google Scholar]
  25. Gutekunst, H., Eikmanns, B. J. & Reinscheid, D. J. ( 2003; ). Analysis of RogB-controlled virulence mechanisms and gene expression in Streptococcus agalactiae. Infect Immun 71, 5056–5064.[CrossRef]
    [Google Scholar]
  26. Heath, P. T., Balfour, G., Weisner, A. M., Esfratiou, A., Lamagni, T. L., Tighe, H., O'Connell, L. A. F., Cafferkey, M., Verlander, N. Q. & other authors ( 2004; ). Group B streptococcal disease in UK and Irish infants younger than 90 days. Lancet 363, 292–294.[CrossRef]
    [Google Scholar]
  27. Henneke, P. & Berner, R. ( 2006; ). Interaction of neonatal phagocytes with Group B Streptococcus: recognition and response. Infect Immun 74, 3085–3095.[CrossRef]
    [Google Scholar]
  28. Hofmann, K. & Stoffel, W. ( 1993; ). TMbase – a database of membrane spanning protein segments. Biol Chem Hoppe Seyler 374, 166
    [Google Scholar]
  29. Johri, A. K., Paoletti, L. C., Glaser, P., Dua, M., Sharma, P. K., Grandi, G. & Rappuoli, R. ( 2006; ). Group B Streptococcus: global incidence and vaccine development. Nat Rev Microbiol 4, 932–942.[CrossRef]
    [Google Scholar]
  30. Käll, L., Krogh, A. & Sonnhammer, E. L. L. ( 2004; ). A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338, 1027–1036.[CrossRef]
    [Google Scholar]
  31. Kogan, G., Uhrin, D., Brisson, J. R., Paoletti, L. C., Blodgett, A. E., Kasper, D. L. & Jennings, H. J. ( 1996; ). Structural and immunochemical characterization of the type VIII Group B Streptococcus capsular polysaccharide. J Biol Chem 271, 8786–8790.[CrossRef]
    [Google Scholar]
  32. Krogh, A., Larsson, B., von Heijne, G. & Sonnhammer, E. L. L. ( 2001; ). Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305, 567–580.[CrossRef]
    [Google Scholar]
  33. Lancefield, R. C. ( 1934; ). A serological differentiation of specific types of bovine hemolytic streptococci (Group B). J Exp Med 59, 441–458.[CrossRef]
    [Google Scholar]
  34. Lancefield, R. C., McCarty, M. & Everly, W. N. ( 1975; ). Multiple mouse-protective antibodies directed against group B streptococci. Special reference to antibodies effective against protein antigens. J Exp Med 142, 165 [CrossRef]
    [Google Scholar]
  35. Lehrer, J., Vigeant, K. A., Tatar, L. D. & Valvano, M. A. ( 2007; ). Functional characterization and membrane topology of Escherichia coli WecA, a sugar-phosphate transferase initiating the biosynthesis of enterobacterial common antigen and O-antigen lipopolysaccharide. J Bacteriol 189, 2618–2628.[CrossRef]
    [Google Scholar]
  36. Lindahl, G., Stålhammar-Carlemalm, M. & Areschoug, T. ( 2005; ). Surface proteins of Streptococcus agalactiae and related proteins in other bacterial pathogens. Clin Microbiol Rev 18, 102–127.[CrossRef]
    [Google Scholar]
  37. 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]
  38. Lysenko, E., Richards, J. C., Cox, A. D., Stewart, A., Martin, A., Kapoor, M. & Weiser, J. N. ( 2000; ). The position of phosphorylcholine on the lipopolysaccharide of Haemophilus influenzae affects binding and sensitivity to C-reactive protein-mediated killing. Mol Microbiol 35, 234–245.[CrossRef]
    [Google Scholar]
  39. Makarova, K., Slesarev, A., Wolf, Y., Sorokin, A., Mirkin, B., Koonin, E., Pavlov, A., Pavlova, N., Karamychev, V. & other authors ( 2006; ). Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci U S A 103, 15611–15616.[CrossRef]
    [Google Scholar]
  40. Marolda, C. L., Tatar, L. D., Alaimo, C., Aebi, M. & Valvano, M. A. ( 2006; ). Interplay of the Wzx translocase and the corresponding polymerase and chain length regulator proteins in the translocation and periplasmic assembly of lipopolysaccharide O antigen. J Bacteriol 188, 5124–5135.[CrossRef]
    [Google Scholar]
  41. Marques, M. B., Kasper, D. L., Schroff, A., Michon, F., Jennings, H. J. & Wessels, M. R. ( 1994; ). Functional activity of antibodies to the group B polysaccharide of Group B streptococci elicited by a polysaccharide-protein conjugate vaccine. Infect Immun 62, 1593–1599.
    [Google Scholar]
  42. Mattingly, S. J. & Johnston, B. P. ( 1987; ). Comparative analysis of the localisation of lipotechoic acid in Streptococcus agalactiae and Streptococcus pyogenes. Infect Immun 55, 2383–2386.
    [Google Scholar]
  43. McGinnis, S. & Madden, T. L. ( 2004; ). blast: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res 32, W20–W25.[CrossRef]
    [Google Scholar]
  44. Michon, F., Katzenellenbogen, E., Kasper, D. L. & Jennings, H. J. ( 1987; ). Structure of the complex group-specific polysaccharide of group B Streptococcus. Biochemistry 26, 476–486.[CrossRef]
    [Google Scholar]
  45. Michon, F., Brisson, J. R., Dell, A., Kasper, D. L. & Jennings, H. J. ( 1988; ). Multiantennary group-specific polysaccharide of Group B Streptococcus. Biochemistry 27, 5341–5351.[CrossRef]
    [Google Scholar]
  46. Michon, F., Chalifour, R., Feldman, R., Wessels, M., Kasper, D. L., Gamian, A., Pozsgay, V. & Jennings, H. J. ( 1991; ). The α-l-(1→2)-trirhamnopyranoside epitope on the group-specific polysaccharide of Group B Streptococci. Infect Immun 59, 1690–1696.
    [Google Scholar]
  47. Michon, F., Moore, S. L., Kim, J., Blake, M. S., Auzanneau, F. I., Johnston, B. D., Johnson, M. A. & Pinto, B. M. ( 2005; ). Doubly branched hexasaccharide epitope on the cell wall polysaccharide of group A streptococci recognized by human and rabbit antisera. Infect Immun 73, 6383–6389.[CrossRef]
    [Google Scholar]
  48. Neuhaus, F. C. & Baddiley, J. ( 2003; ). A continuum of anionic charge: structures and functions of d-alanyl-teichoic acids in Gram-positive bacteria. Microbiol Mol Biol Rev 67, 686–723.[CrossRef]
    [Google Scholar]
  49. Pincus, S. H., Cole, R. L., Wessels, M. R., Corwin, M. D., Kamangasollo, E., Hayes, S. F., Cieplak, W. & Swanson, J. ( 1992; ). Group B Streptococcal opacity variants. J Bacteriol 174, 3739–3749.
    [Google Scholar]
  50. Pincus, S. H., Cole, R. L., Kamangasollo, E. & Fischer, S. H. ( 1993; ). Interaction of Group B Streptococcal opacity variants with the host-defense system. Infect Immun 61, 3761–3768.
    [Google Scholar]
  51. Poyart, C., Lamy, M. C., Boumaila, C., Fiedler, F. & Trieu-Cuot, P. ( 2001; ). Regulation of d-alanyl-lipoteichoic acid biosynthesis in Streptococcus agalactiae involves a novel two-component regulatory system. J Bacteriol 183, 6324–6334.[CrossRef]
    [Google Scholar]
  52. Pritchard, D. G., Gray, B. M. & Dillon, H. C. ( 1984; ). Characterization of the group-specific polysaccharide of group B Streptococcus. Arch Biochem Biophys 235, 385–392.[CrossRef]
    [Google Scholar]
  53. Rosini, R., Rinaudo, C. D., Soriani, M., Lauer, P., Mora, M., Maione, D., Taddei, A., Santi, I., Ghezzo, C. & other authors ( 2006; ). Identification of novel genomic islands coding for antigenic pilus-like structures in Streptococcus agalactiae. Mol Microbiol 61, 126–141.[CrossRef]
    [Google Scholar]
  54. Sabharwal, H., Michon, F., Nelson, D., Dong, W. L., Fuchs, K., Manjarrez, R. C., Sarkar, A., Uitz, C., Viteri-Jackson, A. & other authors ( 2006; ). Group A Streptococcus (GAS) carbohydrate as an immunogen for protection against GAS infection. J Infect Dis 193, 129–135.[CrossRef]
    [Google Scholar]
  55. Shibata, Y., Yamashita, Y., Ozaki, K., Nakano, Y. & Koga, T. ( 2002; ). Expression and characterization of streptococcal rgp genes required for rhamnan synthesis in Escherichia coli. Infect Immun 70, 2891–2898.[CrossRef]
    [Google Scholar]
  56. Soldo, B., Lazarevic, V. & Karamata, D. ( 2002; ). tagO is involved in the synthesis of all anionic cell-wall polymers in Bacillus subtilis 168. Microbiology 148, 2079–2087.
    [Google Scholar]
  57. Sutcliffe, I. C. & Harrington, D. J. ( 2004; ). Putative lipoproteins of Streptococcus agalactiae identified by bioinformatic genome analysis. Antonie van Leeuwenhoek 85, 305–315.[CrossRef]
    [Google Scholar]
  58. Takamatsu, D., Bensing, B. A. & Sullam, P. M. ( 2004; ). Four proteins encoded in the gspB-secY2A2 operon of Streptococcus gordonii mediate the intracellular glycosylation of the platelet-binding protein GspB. J Bacteriol 186, 7100–7111.[CrossRef]
    [Google Scholar]
  59. Tettelin, H., Masignani, V., Cieslewicz, M. J., Eisen, J. A., Peterson, S., Wessels, M. R., Paulsen, I. T., Nelson, K. E., Margarit, I. & other authors ( 2002; ). Complete genome sequence and comparative genomic analysis of an emerging human pathogen, serotype V Streptococcus agalactiae. Proc Natl Acad Sci U S A 99, 12391–12396.[CrossRef]
    [Google Scholar]
  60. Tettelin, H., Masignani, V., Cieslewicz, M. J., Donati, C., Medini, D., Ward, N. L., Angiuoli, S. V., Crabtree, J., Jones, A. L. & other authors ( 2005; ). Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial ‘pan-genome’. Proc Natl Acad Sci U S A 102, 13950–13955.[CrossRef]
    [Google Scholar]
  61. Trotman, H. & Bell, Y. ( 2006; ). Neonatal group B streptococcal infection at the University Hospital of the West Indies, Jamaica: a 10-year experience. Ann Trop Paediatr 26, 53–57.[CrossRef]
    [Google Scholar]
  62. Tsukioka, Y., Yamashita, Y., Nakano, Y., Oho, T. & Koga, T. ( 1997; ). Identification of a fourth gene involved in dTDP-rhamnose synthesis in Streptococcus mutans. J Bacteriol 179, 4411–4414.
    [Google Scholar]
  63. UniProt Consortium ( 2007; ). The universal protein resource (UniProt). Nucleic Acids Res 35, D193–D197.[CrossRef]
    [Google Scholar]
  64. Vallejo, J. G., Baker, C. J. & Edwards, M. S. ( 1996; ). Role of the bacterial cell wall and capsule in induction of tumor necrosis factor alpha by Type III Group B streptococci. Infect Immun 64, 5042–5046.
    [Google Scholar]
  65. Wegmann, U., O'Connell-Motherwy, M., Zomer, A., Buist, G., Shearman, C., Canchaya, C., Ventura, M., Goesmann, A., Gasson, M. J. & other authors ( 2007; ). Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis subsp cremoris MG1363. J Bacteriol 189, 3256–3270.[CrossRef]
    [Google Scholar]
  66. Whitfield, C. ( 2006; ). Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75, 39–68.[CrossRef]
    [Google Scholar]
  67. Yamashita, Y., Tsukioka, Y., Tomihisa, K., Nakano, Y. & Koga, T. ( 1998; ). Genes involved in cell wall localization and side chain formation of rhamnose-glucose polysaccharide in Streptococcus mutans. J Bacteriol 180, 5803–5807.
    [Google Scholar]
  68. Yamashita, Y., Sibata, Y., Nakano, Y., Tsuda, H., Kido, N., Ohta, M. & Koga, T. ( 1999; ). A novel gene required for rhamnose-glucose polysaccharide synthesis in Streptococcus mutans. J Bacteriol 181, 6556–6559.
    [Google Scholar]
  69. Yoshida, Y., Ganguly, S., Bush, C. A. & Cisar, J. O. ( 2006; ). Molecular basis of l-rhamnose branch formation in streptococcal coaggregation receptor polysaccharides. J Bacteriol 188, 4125–4130.[CrossRef]
    [Google Scholar]
  70. Zhang, J. R., Idanpaan-Heikkila, I., Fischer, W. & Tuomanen, E. I. ( 1999; ). Pneumococcal licD2 gene is involved in phosphorylcholine metabolism. Mol Microbiol 31, 1477–1488.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/014522-0
Loading
/content/journal/micro/10.1099/mic.0.2007/014522-0
Loading

Data & Media loading...

A step-wise model for the biosynthesis of the GBC is available hereas a PDF file.

PDF

. Analysis of the G+C content in the coding regions of the GBC locus and comparison of the GBC locus polysaccharide biosynthesis locus in subsp. (LACR_0200- LACR_0222 and LLMG_0206- LLMG_0227).

PDF

. Pairwise sequence inter-relationships of the putative α-RhaT encoded in the GBC locus.

PDF

. Glycosyltransferases encoded in the strain 2603/V genome.

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error