1887

Abstract

The capsule polysaccharide locus () is the site of the capsule biosynthesis gene cluster in encapsulated . A set of pneumococcal samples and non-pneumococcal streptococci from Denmark, the Gambia, the Netherlands, Thailand, the UK and the USA were sequenced at the locus to elucidate serologically mistyped or non-typable isolates. We identified a novel serotype 33B/33C mosaic capsule cluster and previously unseen serotype 22F capsule genes, disrupted and deleted clusters, the presence of and genes that are unrelated to capsule production, and similar genes in the non-pneumococcal samples. These data provide greater understanding of diversity at a locus which is crucial to the antigenic diversity of the pathogen and current vaccine strategies.

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2012-06-01
2024-03-28
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References

  1. Aanensen D. M., Mavroidi A., Bentley S. D., Reeves P. R., Spratt B. G. ( 2007). Predicted functions and linkage specificities of the products of the Streptococcus pneumoniae capsular biosynthetic loci. J Bacteriol 189:7856–7876 [View Article][PubMed]
    [Google Scholar]
  2. Ansaldi F., Canepa P., de Florentiis D., Bandettini R., Durando P., Icardi G. ( 2011). Increasing incidence of Streptococcus pneumoniae serotype 19A and emergence of two vaccine escape recombinant ST695 strains in Liguria, Italy, 7 years after implementation of the 7-valent conjugated vaccine. Clin Vaccine Immunol 18:343–345 [View Article][PubMed]
    [Google Scholar]
  3. Beall B. W., Gertz R. E., Hulkower R. L., Whitney C. G., Moore M. R., Brueggemann A. B. ( 2011). Shifting genetic structure of invasive serotype 19A pneumococci in the United States. J Infect Dis 203:1360–1368 [View Article][PubMed]
    [Google Scholar]
  4. Bentley S. D., Aanensen D. M., Mavroidi A., Saunders D., Rabbinowitsch E., Collins M., Donohoe K., Harris D., Murphy L. et al. ( 2006). Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet 2:e31 [View Article][PubMed]
    [Google Scholar]
  5. Bonfield J. K., Smith K. F., Staden R. A. ( 1995). A new DNA sequence assembly program. Nucleic Acids Res 23:4992–4999 [View Article][PubMed]
    [Google Scholar]
  6. Brueggemann A. B., Peto T. E. A., Crook D. W., Butler J. C., Kristinsson K. G., Spratt B. G. ( 2004). Temporal and geographic stability of the serogroup-specific invasive disease potential of Streptococcus pneumoniae in children. J Infect Dis 190:1203–1211 [View Article][PubMed]
    [Google Scholar]
  7. Brueggemann A. B., Pai R., Crook D. W., Beall B. ( 2007). Vaccine escape recombinants emerge after pneumococcal vaccination in the United States. PLoS Pathog 3:e168 [View Article][PubMed]
    [Google Scholar]
  8. Brugger S. D. F., Frey P., Aebi S., Hinds J., Mühlemann K. ( 2010). Multiple colonization with S. pneumoniae before and after introduction of the seven-valent conjugated pneumococcal polysaccharide vaccine. PLoS ONE 5:e11638 [View Article][PubMed]
    [Google Scholar]
  9. Cole J. R., Chai B., Farris R. J., Wang Q., Kulam-Syed-Mohideen A. S., McGarrell D. M., Bandela A. M., Cardenas E., Garrity G. M., Tiedje J. M. ( 2007). The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res 35:Database issueD169–D172 [View Article][PubMed]
    [Google Scholar]
  10. Croucher N. J., Harris S. R., Fraser C., Quail M. A., Burton J., van der Linden M., McGee L., von Gottberg A., Song J. H. et al. ( 2011). Rapid pneumococcal evolution in response to clinical interventions. Science 331:430–434 [View Article][PubMed]
    [Google Scholar]
  11. Dagan R., Givon-Lavi N., Leibovitz E., Greenberg D., Porat N. ( 2009). Introduction and proliferation of multidrug-resistant Streptococcus pneumoniae serotype 19A clones that cause acute otitis media in an unvaccinated population. J Infect Dis 199:776–785 [View Article][PubMed]
    [Google Scholar]
  12. Delcher A. L., Harmon D., Kasif S., White O., Salzberg S. L. ( 1999). Improved microbial gene identification with glimmer . Nucleic Acids Res 27:4636–4641 [View Article][PubMed]
    [Google Scholar]
  13. Donati C., Hiller N. L., Tettelin H., Muzzi A., Croucher N. J., Angiuoli S. V., Oggioni M., Dunning Hotopp J. C., Hu F. Z. et al. ( 2010). Structure and dynamics of the pan-genome of Streptococcus pneumoniae and closely related species. Genome Biol 11:R107 [View Article][PubMed]
    [Google Scholar]
  14. Edgar R. C. ( 2004). muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797 [View Article][PubMed]
    [Google Scholar]
  15. Elm C., Braathen R., Bergmann S., Frank R., Vaerman J.-P., Kaetzel C. S., Chhatwal G. S., Johansen F.-E., Hammerschmidt S. ( 2004). Ectodomains 3 and 4 of human polymeric immunoglobulin receptor (hpIgR) mediate invasion of Streptococcus pneumoniae into the epithelium. J Biol Chem 279:6296–6304 [View Article][PubMed]
    [Google Scholar]
  16. Gouy M., Guindon S., Gascuel O. ( 2010). SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224 [View Article][PubMed]
    [Google Scholar]
  17. Hammerschmidt S., Wolff S., Hocke A., Rosseau S., Müller E., Rohde M. ( 2005). Illustration of pneumococcal polysaccharide capsule during adherence and invasion of epithelial cells. Infect Immun 73:4653–4667 [View Article][PubMed]
    [Google Scholar]
  18. Hanage W. P., Kaijalainen T. H., Syrjänen R. K., Auranen K., Leinonen M., Mäkelä P. H., Spratt B. G. ( 2005). Invasiveness of serotypes and clones of Streptococcus pneumoniae among children in Finland. Infect Immun 73:431–435 [View Article][PubMed]
    [Google Scholar]
  19. Hanage W. P., Kaijalainen T., Saukkoriipi A., Rickcord J. L., Spratt B. G. ( 2006). A successful, diverse disease-associated lineage of nontypeable pneumococci that has lost the capsular biosynthesis locus. J Clin Microbiol 44:743–749 [View Article][PubMed]
    [Google Scholar]
  20. Hathaway L. J., Stutzmann Meier P., Bättig P., Aebi S., Mühlemann K. ( 2004). A homologue of aliB is found in the capsule region of nonencapsulated Streptococcus pneumoniae . J Bacteriol 186:3721–3729 [View Article][PubMed]
    [Google Scholar]
  21. Hathaway L. J., Bättig P., Aebi S., Reber S., Brewin H., Kadioglu A., Mühlemann K. ( 2010). aliB-like ORF 1 aids growth by playing a role in the uptake of glutamic acid. 7th International Symposium on Pneumococci and Pneumococcal Diseases
    [Google Scholar]
  22. Hulo N., Bairoch A., Bulliard V., Cerutti L., Cuche B. A., de Castro E., Lachaize C., Langendijk-Genevaux P. S., Sigrist C. J. A. ( 2008). The 20 years of prosite . Nucleic Acids Res 36:Database issueD245–D249 [View Article][PubMed]
    [Google Scholar]
  23. Johnson H. L., Deloria-Knoll M., Levine O. S., Stoszek S. K., Freimanis Hance L., Reithinger R., Muenz L. R., O’Brien K. L. ( 2010). Systematic evaluation of serotypes causing invasive pneumococcal disease among children under five: the pneumococcal global serotype project. PLoS Med 7:e1000348 [View Article][PubMed]
    [Google Scholar]
  24. Kerr A. R., Adrian P. V., Estevão S., de Groot R., Alloing G., Claverys J.-P., Mitchell T. J., Hermans P. W. M. ( 2004). The Ami-AliA/AliB permease of Streptococcus pneumoniae is involved in nasopharyngeal colonization but not in invasive disease. Infect Immun 72:3902–3906 [View Article][PubMed]
    [Google Scholar]
  25. Kim J. O., Romero-Steiner S., Sørensen U. B., Blom J., Carvalho M., Barnard S., Carlone G., Weiser J. N. ( 1999). Relationship between cell surface carbohydrates and intrastrain variation on opsonophagocytosis of Streptococcus pneumoniae . Infect Immun 67:2327–2333[PubMed]
    [Google Scholar]
  26. Kirkham L.-A. S., Jefferies J. M. C., Kerr A. R., Jing Y., Clarke S. C., Smith A., Mitchell T. J. ( 2006). Identification of invasive serotype 1 pneumococcal isolates that express nonhemolytic pneumolysin. J Clin Microbiol 44:151–159 [View Article][PubMed]
    [Google Scholar]
  27. Llull D., Muñoz R., López R., García E. ( 1999). A single gene (tts) located outside the cap locus directs the formation of Streptococcus pneumoniae type 37 capsular polysaccharide. Type 37 pneumococci are natural, genetically binary strains. J Exp Med 190:241–252 [View Article][PubMed]
    [Google Scholar]
  28. Marsh R., Smith-Vaughan H., Hare K. M., Binks M., Kong F., Warning J., Gilbert G. L., Morris P., Leach A. J. ( 2010). The nonserotypeable pneumococcus: phenotypic dynamics in the era of anticapsular vaccines. J Clin Microbiol 48:831–835 [View Article][PubMed]
    [Google Scholar]
  29. McMurray A. A., Sulston J. E., Quail M. A. ( 1998). Short-insert libraries as a method of problem solving in genome sequencing. Genome Res 8:562–566[PubMed]
    [Google Scholar]
  30. Melin M., Trzciński K., Meri S., Käyhty H., Väkeväinen M. ( 2010). The capsular serotype of Streptococcus pneumoniae is more important than the genetic background for resistance to complement. Infect Immun 78:5262–5270 [View Article][PubMed]
    [Google Scholar]
  31. Mizrachi Nebenzahl Y., Porat N., Lifshitz S., Novick S., Levi A., Ling E., Liron O., Mordechai S., Sahu R. K., Dagan R. ( 2004). Virulence of Streptococcus pneumoniae may be determined independently of capsular polysaccharide. FEMS Microbiol Lett 233:147–152 [View Article][PubMed]
    [Google Scholar]
  32. Moore M. R., Gertz R. E. Jr, Woodbury R. L., Barkocy-Gallagher G. A., Schaffner W., Lexau C., Gershman K., Reingold A., Farley M. et al. ( 2008). Population snapshot of emergent Streptococcus pneumoniae serotype 19A in the United States, 2005. J Infect Dis 197:1016–1027 [View Article][PubMed]
    [Google Scholar]
  33. Muñoz R., Mollerach M., López R., García E. ( 1997). Molecular organization of the genes required for the synthesis of type 1 capsular polysaccharide of Streptococcus pneumoniae: formation of binary encapsulated pneumococci and identification of cryptic dTDP-rhamnose biosynthesis genes. Mol Microbiol 25:79–92 [View Article][PubMed]
    [Google Scholar]
  34. Muñoz-Almagro C., Esteva C., de Sevilla M. F., Selva L., Gene A., Pallares R. ( 2009). Emergence of invasive pneumococcal disease caused by multidrug-resistant serotype 19A among children in Barcelona. J Infect 59:75–82 [View Article][PubMed]
    [Google Scholar]
  35. O’Brien K. L., Wolfson L. J., Watt J. P., Henkle E., Deloria-Knoll M., McCall N., Lee E., Mulholland K., Levine O. S., Cherian T. Hib and Pneumococcal Global Burden of Disease Study Team ( 2009). Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 374:893–902 [View Article][PubMed]
    [Google Scholar]
  36. Oggioni M. R., Claverys J.-P. ( 1999). Repeated extragenic sequences in prokaryotic genomes: a proposal for the origin and dynamics of the RUP element in Streptococcus pneumoniae . Microbiology 145:2647–2653[PubMed]
    [Google Scholar]
  37. Paton J. C., Morona J. K. ( 2007). Pneumococcal capsular polysaccharides: biosynthesis and regulation. Molecular Biology of Streptococci119–140 Hakenbeck R., Chhatwal G. S. Wymondham, UK: Horizon Bioscience;
    [Google Scholar]
  38. Rutherford K., Parkhill J., Crook J., Horsnell T., Rice P., Rajandream M. A., Barrell B. ( 2000). Artemis: sequence visualization and annotation. Bioinformatics 16:944–945 [View Article][PubMed]
    [Google Scholar]
  39. Sanger F., Nicklen S., Coulson A. R. ( 1977). DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 74:5463–5467 [View Article][PubMed]
    [Google Scholar]
  40. Shin J., Baek J. Y., Kim S. H., Song J.-H., Ko K. S. ( 2011). Predominance of ST320 among Streptococcus pneumoniae serotype 19A isolates from 10 Asian countries. J Antimicrob Chemother 66:1001–1004 [View Article][PubMed]
    [Google Scholar]
  41. Siguier P., Perochon J., Lestrade L., Mahillon J., Chandler M. ( 2006). ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34:Database issueD32–D36 [View Article][PubMed]
    [Google Scholar]
  42. Temime L., Boelle P.-Y., Opatowski L., Guillemot D. ( 2008). Impact of capsular switch on invasive pneumococcal disease incidence in a vaccinated population. PLoS ONE 3:e3244 [View Article][PubMed]
    [Google Scholar]
  43. Turner P. H., Hinds J., Turner C., Jankhot A., Gould K., Bentley S. D., Nosten F., Goldblatt D. ( 2011). Improved detection of nasopharyngeal co-colonization by multiple pneumococcal serotypes by use of latex agglutination or molecular serotyping by microarray. J Clin Microbiol 49:1784–1789 [View Article][PubMed]
    [Google Scholar]
  44. van Selm S., van Cann L. M., Kolkman M. A., van der Zeijst B. A. M., van Putten J. P. M. ( 2003). Genetic basis for the structural difference between Streptococcus pneumoniae serotype 15B and 15C capsular polysaccharides. Infect Immun 71:6192–6198 [View Article][PubMed]
    [Google Scholar]
  45. Waite R. D., Penfold D. W., Struthers J. K., Dowson C. G. ( 2003). Spontaneous sequence duplications within capsule genes cap8E and tts control phase variation in Streptococcus pneumoniae serotypes 8 and 37. Microbiology 149:497–504 [View Article][PubMed]
    [Google Scholar]
  46. Weinberger D. M., Trzciński K., Lu Y.-J., Bogaert D., Brandes A., Galagan J., Anderson P. W., Malley R., Lipsitch M. ( 2009). Pneumococcal capsular polysaccharide structure predicts serotype prevalence. PLoS Pathog 5:e1000476 [View Article][PubMed]
    [Google Scholar]
  47. Yang J., Ritchey M., Yoshida Y., Bush C. A., Cisar J. O. ( 2009). Comparative structural and molecular characterization of ribitol-5-phosphate-containing Streptococcus oralis coaggregation receptor polysaccharides. J Bacteriol 191:1891–1900 [View Article][PubMed]
    [Google Scholar]
  48. 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 [View Article][PubMed]
    [Google Scholar]
  49. Yu J., Lin J., Kim K.-H., Benjamin W. H. Jr, Nahm M. H. ( 2011). Development of an automated and multiplexed serotyping assay for Streptococcus pneumoniae . Clin Vaccine Immunol 18:1900–1907 [View Article][PubMed]
    [Google Scholar]
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