1887

Abstract

Serotype III group B (GBS) is the major cause of neonatal meningitis, but the risk of infection in the colonized neonates is variable. Capsular sialic acid (Sia), whose synthesis is encoded by genes, appears to be a major virulence factor in several bacterial species able to reach the cerebrospinal fluid. Therefore, variations of Sia expression related to the genetic diversity of strains may have an impact on the risk of meningitis in colonized neonates. We characterized by MLST the phylogenetic diversity of 64 serotype III GBS strains isolated from vaginal flora and randomly selected. These strains mostly belonged to three major sequence types (STs): ST1 (11 %), ST17 (39 %) and ST19 (31 %). The genetic diversity of strains of these lineages, characterized by PFGE, allowed the selection of 17 representative strains, three ST1, six ST17 and eight ST19, with NEM316 as reference, in order to evaluate (i) by quantitative RT-PCR, the level of transcription of the gene as a marker for the transcription of genes and (ii) by enzymological analysis, the expression of Sia. The mean transcription level of was higher for ST17 strains than for ST1 and ST19 strains in the early, mid- and late exponential growth phases, and was maximum in the early exponential growth phase for ST17 strains and in the mid-exponential growth phase for ST1 and ST19 strains. Mean Sia concentration was higher for ST17 than for ST1 and ST9 strains in all three growth phases. For the total population, Sia concentration varied notably in the stationary phase, from 0.38 to 9.30 nmol per 10 viable bacteria, with a median value of 2.99 nmol per 10 bacteria. All ST17 strains, only one-third of the ST19 strains and none of the ST1 strains had Sia concentrations higher than the median Sia concentration. Therefore, differences in the level of expression of Sia by strains of the major serotype III GBS phylogenetic lineages might be one of the factors that explain the leading role of ST17 strains in neonatal meningitis.

Funding
This study was supported by the:
  • Ministère de l’Enseignement Supérieur et de la Recherche
  • Centre Hospitalier Universitaire de Tours
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.050013-0
2011-12-01
2024-12-08
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/12/3282.html?itemId=/content/journal/micro/10.1099/mic.0.050013-0&mimeType=html&fmt=ahah

References

  1. Al Safadi R., Amor S., Hery-Arnaud G., Spellerberg B., Lanotte P., Mereghetti L., Gannier F., Quentin R., Rosenau A. ( 2010). Enhanced expression of lmb gene encoding laminin-binding protein in Streptococcus agalactiae strains harboring IS1548 in scpB–lmb intergenic region. PLoS ONE 5:e10794 [View Article][PubMed]
    [Google Scholar]
  2. Al Safadi R., Mereghetti L., Salloum M., Lartigue M. F., Virlogeux-Payant I., Quentin R., Rosenau A. ( 2011). Two-component system RgfA/C activates the fbsB gene encoding major fibrinogen-binding protein in highly virulent CC17 clone group B Streptococcus . PLoS ONE 6:e14658 [View Article][PubMed]
    [Google Scholar]
  3. Amin A., Abdulrazzaq Y. M., Uduman S. ( 2002). Group B streptococcal serotype distribution of isolates from colonized pregnant women at the time of delivery in United Arab Emirates. J Infect 45:42–46 [CrossRef]
    [Google Scholar]
  4. Bisharat N., Jones N., Marchaim D., Block C., Harding R. M., Yagupsky P., Peto T., Crook D. W. ( 2005). Population structure of group B streptococcus from a low-incidence region for invasive neonatal disease. Microbiology 151:1875–1881 [View Article][PubMed]
    [Google Scholar]
  5. Brochet M., Couvé E., Zouine M., Vallaeys T., Rusniok C., Lamy M. C., Buchrieser C., Trieu-Cuot P., Kunst F. et al. & other authors ( 2006). Genomic diversity and evolution within the species Streptococcus agalactiae . Microbes Infect 8:1227–1243 [View Article][PubMed]
    [Google Scholar]
  6. Brochet M., Couvé E., Bercion R., Sire J. M., Glaser P. ( 2009). Population structure of human isolates of Streptococcus agalactiae from Dakar and Bangui.. J Clin Microbiol 47:800–803 [CrossRef]
    [Google Scholar]
  7. Chaffin D. O., Beres S. B., Yim H. H., Rubens C. E. ( 2000). The serotype of type Ia and III group B streptococci is determined by the polymerase gene within the polycistronic capsule operon. J Bacteriol 182:4466–4477 [View Article][PubMed]
    [Google Scholar]
  8. Daines D. A., Wright L. F., Chaffin D. O., Rubens C. E., Silver R. P. ( 2000). NeuD plays a role in the synthesis of sialic acid in Escherichia coli K1. FEMS Microbiol Lett 189:281–284 [View Article][PubMed]
    [Google Scholar]
  9. Davies H. D., Jones N., Whittam T. S., Elsayed S., Bisharat N., Baker C. J. ( 2004). Multilocus sequence typing of serotype III group B streptococcus and correlation with pathogenic potential. J Infect Dis 189:1097–1102 [View Article][PubMed]
    [Google Scholar]
  10. Deng L., 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 [View Article][PubMed]
    [Google Scholar]
  11. Edwards U., Müller A., Hammerschmidt S., Gerardy-Schahn R., Frosch M. ( 1994). Molecular analysis of the biosynthesis pathway of the α-2,8-polysialic acid capsule by Neisseria meningitidis serogroup B. Mol Microbiol 14:141–149 [View Article][PubMed]
    [Google Scholar]
  12. Ferrieri P., Burke B., Nelson J. ( 1980). Production of bacteremia and meningitis in infant rats with group B streptococcal serotypes. Infect Immun 27:1023–1032[PubMed]
    [Google Scholar]
  13. Gherardi G., Imperi M., Baldassarri L., Pataracchia M., Alfarone G., Recchia S., Orefici G., Dicuonzo G., Creti R. ( 2007). Molecular epidemiology and distribution of serotypes, surface proteins, and antibiotic resistance among group B streptococci in Italy. J Clin Microbiol 45:2909–2916 [View Article][PubMed]
    [Google Scholar]
  14. Gibbs R. S., Schrag S., Schuchat A. ( 2004). Perinatal infections due to group B streptococci. Obstet Gynecol 104:1062–1076 [View Article][PubMed]
    [Google Scholar]
  15. Glaser P., Rusniok C., Buchrieser C., Chevalier F., Frangeul L., Msadek T., Zouine M., Couvé E., Lalioui L. et al. & other authors ( 2002). Genome sequence of Streptococcus agalactiae, a pathogen causing invasive neonatal disease. Mol Microbiol 45:1499–1513 [View Article][PubMed]
    [Google Scholar]
  16. Gutekunst H., Eikmanns B. J., Reinscheid D. J. ( 2003). Analysis of RogB-controlled virulence mechanisms and gene repression in Streptococcus agalactiae . Infect Immun 71:5056–5064 [View Article][PubMed]
    [Google Scholar]
  17. Haft R. F., Wessels M. R., Mebane M. F., Conaty N., Rubens C. E. ( 1996). Characterization of cpsF and its product CMP-N-acetylneuraminic acid synthetase, a group B streptococcal enzyme that can function in K1 capsular polysaccharide biosynthesis in Escherichia coli . Mol Microbiol 19:555–563 [View Article][PubMed]
    [Google Scholar]
  18. Hansen S. M., Uldbjerg N., Kilian M., Sørensen U. B. ( 2004). Dynamics of Streptococcus agalactiae colonization in women during and after pregnancy and in their infants. J Clin Microbiol 42:83–89 [View Article][PubMed]
    [Google Scholar]
  19. Héry-Arnaud G., Bruant G., Lanotte P., Brun S., Rosenau A., van der Mee-Marquet N., Quentin R., Mereghetti L. ( 2005). Acquisition of insertion sequences and the GBSi1 intron by Streptococcus agalactiae isolates correlates with the evolution of the species. J Bacteriol 187:6248–6252 [View Article][PubMed]
    [Google Scholar]
  20. Johnson L. P., Schlievert P. M. ( 1983). A physical map of the group A streptococcal pyrogenic exotoxin bacteriophage T12 genome. Mol Gen Genet 189:251–255 [View Article][PubMed]
    [Google Scholar]
  21. Join-Lambert O., Morand P. C., Carbonnelle E., Coureuil M., Bille E., Bourdoulous S., Nassif X. ( 2010). Mechanisms of meningeal invasion by a bacterial extracellular pathogen, the example of Neisseria meningitidis . Prog Neurobiol 91:130–139 [View Article][PubMed]
    [Google Scholar]
  22. Jones N., Bohnsack J. F., Takahashi S., Oliver K. A., Chan M. S., Kunst F., Glaser P., Rusniok C., Crook D. W. M. et al. & other authors ( 2003). Multilocus sequence typing system for group B streptococcus. J Clin Microbiol 41:2530–2536 [View Article][PubMed]
    [Google Scholar]
  23. Jones N., Oliver K. A., Barry J., Harding R. M., Bisharat N., Spratt B. G., Peto T., Crook D. W. Oxford Group B Streptococcus Consortium ( 2006). Enhanced invasiveness of bovine-derived neonatal sequence type 17 group B streptococcus is independent of capsular serotype. Clin Infect Dis 42:915–924 [View Article][PubMed]
    [Google Scholar]
  24. Kaneko J., Kimura T., Narita S., Tomita T., Kamio Y. ( 1998). Complete nucleotide sequence and molecular characterization of the temperate staphylococcal bacteriophage phiPVL carrying Panton–Valentine leukocidin genes. Gene 215:57–67 [View Article][PubMed]
    [Google Scholar]
  25. Kong F., Gowan S., Martin D., James G., Gilbert G. L. ( 2002). Serotype identification of group B streptococci by PCR and sequencing. J Clin Microbiol 40:216–226 [View Article][PubMed]
    [Google Scholar]
  26. Lewis A. L., Nizet V., Varki A. ( 2004). Discovery and characterization of sialic acid O-acetylation in group B Streptococcus. Proc Natl Acad Sci U S A 101:11123–11128 [View Article][PubMed]
    [Google Scholar]
  27. Lin F. Y., Philips J. B. III, Azimi P. H., Weisman L. E., Clark P., Rhoads G. G., Regan J., Concepcion N. F., Frasch C. E. et al. & other authors ( 2001). Level of maternal antibody required to protect neonates against early-onset disease caused by group B Streptococcus type Ia: a multicenter, seroepidemiology study. J Infect Dis 184:1022–1028 [View Article][PubMed]
    [Google Scholar]
  28. Lin F. Y., Whiting A., Adderson E., Takahashi S., Dunn D. M., Weiss R., Azimi P. H., Philips J. B. III, Weisman L. E. et al. & other authors ( 2006). Phylogenetic lineages of invasive and colonizing strains of serotype III group B streptococci from neonates: a multicenter prospective study. J Clin Microbiol 44:1257–1261 [View Article][PubMed]
    [Google Scholar]
  29. Loulergue J., Couhé C., Grasmick C., Laudat P., Quentin R. ( 2004). Sensitivity to antibiotics of vaginal carriage isolates of group B streptococci obtained in France, 2003. Bull Epidemiol Hebd 18:69–70
    [Google Scholar]
  30. Luan S. L., Granlund M., Sellin M., Lagergård T., Spratt B. G., Norgren M. ( 2005). Multilocus sequence typing of Swedish invasive group B streptococcus isolates indicates a neonatally associated genetic lineage and capsule switching. J Clin Microbiol 43:3727–3733 [View Article][PubMed]
    [Google Scholar]
  31. Manning S. D., Springman A. C., Lehotzky E., Lewis M. A., Whittam T. S., Davies H. D. ( 2009). Multilocus sequence types associated with neonatal group B streptococcal sepsis and meningitis in Canada. J Clin Microbiol 47:1143–1148 [View Article][PubMed]
    [Google Scholar]
  32. Marques M. B., Kasper D. L., Pangburn M. K., Wessels M. R. ( 1992). Prevention of C3 deposition by capsular polysaccharide is a virulence mechanism of type III group B streptococci. Infect Immun 60:3986–3993[PubMed]
    [Google Scholar]
  33. Martins E. R., Pessanha M. A., Ramirez M., Melo-Cristino J. Portuguese Group for the Study of Streptococcal Infections ( 2007). Analysis of group B streptococcal isolates from infants and pregnant women in Portugal revealing two lineages with enhanced invasiveness. J Clin Microbiol 45:3224–3229 [View Article][PubMed]
    [Google Scholar]
  34. Moyo S. R., Maeland J. A., Bergh K. ( 2002).Streptococcus agalactiae J Med Microbiol 51:595–600
    [Google Scholar]
  35. Phares C. R., Lynfield R., Farley M. M., Mohle-Boetani J., Harrison L. H., Petit S., Craig A. S., Schaffner W., Zansky S. M. et al. & other authors ( 2008). Epidemiology of invasive group B streptococcal disease in the United States, 1999–2005. JAMA 299:2056–2065 [View Article][PubMed]
    [Google Scholar]
  36. Rosenau A., Martins K., Amor S., Gannier F., Lanotte P., van der Mee-Marquet N., Mereghetti L., Quentin R. ( 2007). Evaluation of the ability of Streptococcus agalactiae strains isolated from genital and neonatal specimens to bind to human fibrinogen and correlation with characteristics of the fbsA and fbsB genes. Infect Immun 75:1310–1317 [View Article][PubMed]
    [Google Scholar]
  37. Rubens C. E., Wessels M. R., Heggen L. M., Kasper D. L. ( 1987). Transposon mutagenesis of type III group B Streptococcus: correlation of capsule expression with virulence. Proc Natl Acad Sci U S A 84:7208–7212 [View Article][PubMed]
    [Google Scholar]
  38. Seifert K. N., Adderson E. E., Whiting A. A., Bohnsack J. F., Crowley P. J., Brady L. J. ( 2006). A unique serine-rich repeat protein (Srr-2) and novel surface antigen (ϵ) associated with a virulent lineage of serotype III Streptococcus agalactiae . Microbiology 152:1029–1040 [View Article][PubMed]
    [Google Scholar]
  39. Shaikh N., Tarr P. I. ( 2003). Escherichia coli O157 : H7 Shiga toxin-encoding bacteriophages: integrations, excisions, truncations, and evolutionary implications. J Bacteriol 185:3596–3605 [View Article][PubMed]
    [Google Scholar]
  40. Spellerberg B., Rozdzinski E., Martin S., Weber-Heynemann J., Lütticken R. ( 2002). rgf encodes a novel two-component signal transduction system of Streptococcus agalactiae . Infect Immun 70:2434–2440 [View Article][PubMed]
    [Google Scholar]
  41. Straková L., Musílek M., Motlová J. ( 2010). Multilocus sequence types in Czech neonatal GBS strains from 2004 to 2008. Epidemiol Mikrobiol Imunol 59:45–47[PubMed]
    [Google Scholar]
  42. Suryanti V., Nelson A., Berry A. ( 2003). Cloning, over-expression, purification, and characterisation of N-acetylneuraminate synthase from Streptococcus agalactiae . Protein Expr Purif 27:346–356 [View Article][PubMed]
    [Google Scholar]
  43. Tazi A., Disson O., Bellais S., Bouaboud A., Dmytruk N., Dramsi S., Mistou M. Y., Khun H., Mechler C. et al. ( 2010). The surface protein HvgA mediates group B streptococcus hypervirulence and meningeal tropism in neonates. J Exp Med 207:2313–2322 [View Article][PubMed]
    [Google Scholar]
  44. van der Mee-Marquet N., Jouannet C., Domelier A. S., Arnault L., Lartigue M. F., Quentin R. ( 2009). Genetic diversity of Streptococcus agalactiae strains and density of vaginal carriage. J Med Microbiol 58:169–173 [CrossRef]
    [Google Scholar]
  45. Vann W. F., Daines D. A., Murkin A. S., Tanner M. E., Chaffin D. O., Rubens C. E., Vionnet J., Silver R. P. ( 2004). The NeuC protein of Escherichia coli K1 is a UDP N-acetylglucosamine 2-epimerase. J Bacteriol 186:706–712 [View Article][PubMed]
    [Google Scholar]
  46. Vimr E., Lichtensteiger C. ( 2002). To sialylate, or not to sialylate: that is the question. Trends Microbiol 10:254–257 [View Article][PubMed]
    [Google Scholar]
  47. Waldor M. K., Mekalanos J. J. ( 1996). Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272:1910–1914 [View Article][PubMed]
    [Google Scholar]
  48. Weiman S., Dahesh S., Carlin A. F., Varki A., Nizet V., Lewis A. L. ( 2009). Genetic and biochemical modulation of sialic acid O-acetylation on group B Streptococcus: phenotypic and functional impact. Glycobiology 19:1204–1213 [View Article][PubMed]
    [Google Scholar]
  49. Weiman S., Uchiyama S., Lin F. Y., Chaffin D., Varki A., Nizet V., Lewis A. L. ( 2010). O-Acetylation of sialic acid on Group B Streptococcus inhibits neutrophil suppression and virulence. Biochem J 428:163–168 [View Article][PubMed]
    [Google Scholar]
  50. Wessels M. R., Rubens C. E., Benedí V. J., Kasper D. L. ( 1989). Definition of a bacterial virulence factor: sialylation of the group B streptococcal capsule. Proc Natl Acad Sci U S A 86:8983–8987 [View Article][PubMed]
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.050013-0
Loading
/content/journal/micro/10.1099/mic.0.050013-0
Loading

Data & Media loading...

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