1887

Abstract

Countries of the African ‘meningitis belt’ are susceptible to meningococcal meningitis outbreaks. While in the past major epidemics have been primarily caused by serogroup A meningococci, W strains are currently responsible for most of the cases. After an epidemic in Mecca in 2000, W:ST-11 strains have caused many outbreaks worldwide. An unrelated W:ST-2881 clone was described for the first time in 2002, with the first meningitis cases caused by these bacteria reported in 2003. Here we describe results of a comparative whole-genome analysis of 74 W:ST-2881 strains isolated within the framework of two longitudinal colonization and disease studies conducted in Ghana and Burkina Faso. Genomic data indicate that the W:ST-2881 clone has emerged from Y:ST-175(CC175) bacteria by capsule switching. The circulating W:ST-2881 populations were composed of a variety of closely related but distinct genomic variants with no systematic differences between colonization and disease isolates. Two distinct and geographically clustered phylogenetic clonal variants were identified in Burkina Faso and a third in Ghana. On the basis of the presence or absence of 17 recombination fragments, the Ghanaian variant could be differentiated into five clusters. All 25 Ghanaian disease isolates clustered together with 23 out of 40 Ghanaian isolates associated with carriage within one cluster, indicating that W:ST-2881 clusters differ in virulence. More than half of the genes affected by horizontal gene transfer encoded proteins of the ‘cell envelope’ and the ‘transport/binding protein’ categories, which indicates that exchange of non-capsular antigens plays an important role in immune evasion.

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2017-06-21
2024-03-28
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References

  1. Caugant DA, Maiden MC. Meningococcal carriage and disease—population biology and evolution. Vaccine 2009; 27:B64–B70 [View Article][PubMed]
    [Google Scholar]
  2. Rosenstein NE, Perkins BA, Stephens DS, Popovic T, Hughes JM et al. Meningococcal disease. N Engl J Med 2001; 344:1378–1388 [View Article][PubMed]
    [Google Scholar]
  3. Crum-Cianflone N, Sullivan E. Meningococcal vaccinations. Infect Dis Ther 2016; 5:89–112 [View Article][PubMed]
    [Google Scholar]
  4. Pizza M, Rappuoli R. Neisseria meningitidis: pathogenesis and immunity. Curr Opin Microbiol 2015; 23:68–72 [View Article][PubMed]
    [Google Scholar]
  5. Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE et al. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci USA 1998; 95:3140–3145 [View Article][PubMed]
    [Google Scholar]
  6. Jolley KA, Brehony C, Maiden MC. Molecular typing of meningococci: recommendations for target choice and nomenclature. FEMS Microbiol Rev 2007; 31:89–96 [View Article][PubMed]
    [Google Scholar]
  7. Smith JM, Smith NH, O'Rourke M, Spratt BG. How clonal are bacteria?. Proc Natl Acad Sci USA 1993; 90:4384–4388 [View Article][PubMed]
    [Google Scholar]
  8. Tibayrenc M, Ayala FJ. How clonal are Neisseria species? The epidemic clonality model revisited. Proc Natl Acad Sci USA 2015; 112:8909–8913 [View Article][PubMed]
    [Google Scholar]
  9. Bambini S, Muzzi A, Olcen P, Rappuoli R, Pizza M et al. Distribution and genetic variability of three vaccine components in a panel of strains representative of the diversity of serogroup B meningococcus. Vaccine 2009; 27:2794–2803 [View Article][PubMed]
    [Google Scholar]
  10. Lamelas A, Harris SR, Röltgen K, Dangy JP, Hauser J et al. Emergence of a new epidemic Neisseria meningitidis serogroup A clone in the African meningitis belt: high-resolution picture of genomic changes that mediate immune evasion. MBio 2014; 5:e01974-14 [View Article][PubMed]
    [Google Scholar]
  11. Zhu P, van der Ende A, Falush D, Brieske N, Morelli G et al. Fit genotypes and escape variants of subgroup III Neisseria meningitidis during three pandemics of epidemic meningitis. Proc Natl Acad Sci USA 2001; 98:5234–5239 [View Article][PubMed]
    [Google Scholar]
  12. Greenwood B. Manson Lecture. Meningococcal meningitis in Africa. Trans R Soc Trop Med Hyg 1999; 93:341–353[PubMed]
    [Google Scholar]
  13. Tiffay K, Jodar L, Kieny MP, Socquet M, Laforce FM. The evolution of the meningitis vaccine project. Clin Infect Dis 2015; 61:S396–S403 [View Article][PubMed]
    [Google Scholar]
  14. Evans JR, Artenstein MS, Hunter DH. Prevalence of meningococcal serogroups and description of three new groups. Am J Epidemiol 1968; 87:643–646 [View Article][PubMed]
    [Google Scholar]
  15. Griffiss JM, Brandt BL. Disease due to serogroup W135 Neisseria meningitidis . Pediatrics 1979; 64:218–221[PubMed]
    [Google Scholar]
  16. Taha MK, Achtman M, Alonso JM, Greenwood B, Ramsay M et al. Serogroup W135 meningococcal disease in Hajj pilgrims. Lancet 2000; 356:2159 [View Article][PubMed]
    [Google Scholar]
  17. Mustapha MM, Marsh JW, Krauland MG, Fernandez JO, de Lemos AP et al. Genomic epidemiology of hypervirulent serogroup W, ST-11 Neisseria meningitidis . EBioMedicine 2015; 2:1447–1455 [View Article][PubMed]
    [Google Scholar]
  18. Lucidarme J, Hill DM, Bratcher HB, Gray SJ, du Plessis M et al. Genomic resolution of an aggressive, widespread, diverse and expanding meningococcal serogroup B, C and W lineage. J Infect 2015; 71:544–552 [View Article][PubMed]
    [Google Scholar]
  19. Mustapha MM, Marsh JW, Krauland MG, Fernandez JO, De Lemos AP et al. Genomic investigation reveals highly conserved, mosaic, recombination events associated with capsular switching among invasive Neisseria meningitidis serogroup W sequence type (ST)-11 strains. Genome Biol Evol 2016; 8:2065–2075 [View Article][PubMed]
    [Google Scholar]
  20. Whitney AM, Coulson GB, von Gottberg A, Block C, Keller N et al. Genotypic comparison of invasive Neisseria meningitidis serogroup Y isolates from the United States, South Africa, and Israel, isolated from 1999 through 2002. J Clin Microbiol 2009; 47:2787–2793 [View Article][PubMed]
    [Google Scholar]
  21. Nicolas P, Djibo S, Moussa A, Tenebray B, Boisier P et al. Molecular epidemiology of meningococci isolated in Niger in 2003 shows serogroup A sequence type (ST)-7 and serogroup W135 ST-11 or ST-2881 strains. J Clin Microbiol 2005; 43:1437–1438 [View Article][PubMed]
    [Google Scholar]
  22. Nicolas P, Norheim G, Garnotel E, Djibo S, Caugant DA. Molecular epidemiology of Neisseria meningitidis isolated in the African Meningitis Belt between 1988 and 2003 shows dominance of sequence type 5 (ST-5) and ST-11 complexes. J Clin Microbiol 2005; 43:5129–5135 [View Article][PubMed]
    [Google Scholar]
  23. Boisier P, Nicolas P, Djibo S, Hamidou AA, Tenebray B et al. Carriage of Neisseria meningitidis serogroup W135 ST-2881. Emerg Infect Dis 2006; 12:1421–1423 [View Article][PubMed]
    [Google Scholar]
  24. Mueller JE, Sangaré L, Njanpop-Lafourcade BM, Tarnagda Z, Traoré Y et al. Molecular characteristics and epidemiology of meningococcal carriage, Burkina Faso, 2003. Emerg Infect Dis 2007; 13:847–854 [View Article][PubMed]
    [Google Scholar]
  25. Massenet D, Birguel J, Azowé F, Ebong C, Gake B et al. Epidemiologic pattern of meningococcal meningitis in northern Cameroon in 2007-2010: contribution of PCR-enhanced surveillance. Pathog Glob Health 2013; 107:15–20 [View Article][PubMed]
    [Google Scholar]
  26. Leimkugel J, Forgor AA, Dangy JP, Pflüger V, Gagneux S et al. Genetic diversification of Neisseria meningitidis during waves of colonization and disease in the meningitis belt of sub-Saharan Africa. Vaccine 2007; 25:A18–A23 [View Article][PubMed]
    [Google Scholar]
  27. Sié A, Louis VR, Gbangou A, Müller O, Niamba L et al. The Health and Demographic Surveillance System (HDSS) in Nouna, Burkina Faso, 1993–2007. Glob Health Action 2010; 3: [View Article][PubMed]
    [Google Scholar]
  28. Gagneux S, Hodgson A, Ehrhard I, Morelli G, Genton B et al. Microheterogeneity of serogroup A (subgroup III) Neisseria meningitidis during an outbreak in northern Ghana. Trop Med Int Health 2000; 5:280–287 [View Article][PubMed]
    [Google Scholar]
  29. Sié A, Pflüger V, Coulibaly B, Dangy JP, Kapaun A et al. ST2859 serogroup A meningococcal meningitis outbreak in Nouna Health District, Burkina Faso: a prospective study. Trop Med Int Health 2008; 13:861–868 [View Article][PubMed]
    [Google Scholar]
  30. Marri PR, Paniscus M, Weyand NJ, Rendón MA, Calton CM et al. Genome sequencing reveals widespread virulence gene exchange among human Neisseria species. PLoS One 2010; 5:e11835 [View Article][PubMed]
    [Google Scholar]
  31. Seifert HS, Ajioka RS, Paruchuri D, Heffron F, So M. Shuttle mutagenesis of Neisseria gonorrhoeae: pilin null mutations lower DNA transformation competence. J Bacteriol 1990; 172:40–46 [View Article][PubMed]
    [Google Scholar]
  32. Chin CS, Alexander DH, Marks P, Klammer AA, Drake J et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 2013; 10:563–569 [View Article][PubMed]
    [Google Scholar]
  33. Otto TD, Dillon GP, Degrave WS, Berriman M. RATT: rapid annotation transfer tool. Nucleic Acids Res 2011; 39:e57 [View Article][PubMed]
    [Google Scholar]
  34. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article][PubMed]
    [Google Scholar]
  35. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 2011; 12:402 [View Article][PubMed]
    [Google Scholar]
  36. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article][PubMed]
    [Google Scholar]
  37. Croucher NJ, Harris SR, Fraser C, Quail MA, Burton J et al. Rapid pneumococcal evolution in response to clinical interventions. Science 2011; 331:430–434 [View Article][PubMed]
    [Google Scholar]
  38. Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 1997; 13:555–556 [View Article][PubMed]
    [Google Scholar]
  39. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 2015; 43:e15 [View Article][PubMed]
    [Google Scholar]
  40. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008; 18:821–829 [View Article][PubMed]
    [Google Scholar]
  41. Assefa S, Keane TM, Otto TD, Newbold C, Berriman M. ABACAS: algorithm-based automatic contiguation of assembled sequences. Bioinformatics 2009; 25:1968–1969 [View Article][PubMed]
    [Google Scholar]
  42. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG et al. ACT: the Artemis comparison tool. Bioinformatics 2005; 21:3422–3423 [View Article][PubMed]
    [Google Scholar]
  43. Stamatakis A. Using RAxML to infer phylogenies. Curr Protoc Bioinformatics 2015; 51:1–14 [View Article][PubMed]
    [Google Scholar]
  44. Fall S, Mercier A, Bertolla F, Calteau A, Gueguen L et al. Horizontal gene transfer regulation in bacteria as a "spandrel" of DNA repair mechanisms. PLoS One 2007; 2:e1055 [View Article][PubMed]
    [Google Scholar]
  45. Hey J. What's so hot about recombination hotspots?. PLoS Biol 2004; 2:e190 [View Article][PubMed]
    [Google Scholar]
  46. Bratcher HB, Corton C, Jolley KA, Parkhill J, Maiden MC. A gene-by-gene population genomics platform: de novo assembly, annotation and genealogical analysis of 108 representative Neisseria meningitidis genomes. BMC Genomics 2014; 15:1138 [View Article][PubMed]
    [Google Scholar]
  47. Bryant D, Moulton V. Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 2004; 21:255–265 [View Article][PubMed]
    [Google Scholar]
  48. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 2006; 23:254–267 [View Article][PubMed]
    [Google Scholar]
  49. Parkhill J, Achtman M, James KD, Bentley SD, Churcher C et al. Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491. Nature 2000; 404:502–506 [View Article][PubMed]
    [Google Scholar]
  50. Caugant DA, Tzanakaki G, Kriz P. Lessons from meningococcal carriage studies. FEMS Microbiol Rev 2007; 31:52–63 [View Article][PubMed]
    [Google Scholar]
  51. Yazdankhah SP, Kriz P, Tzanakaki G, Kremastinou J, Kalmusova J et al. Distribution of serogroups and genotypes among disease-associated and carried isolates of Neisseria meningitidis from the Czech Republic, Greece, and Norway. J Clin Microbiol 2004; 42:5146–5153 [View Article][PubMed]
    [Google Scholar]
  52. Bhattacharjee AK, Jennings HJ. Determination of the linkages in some methylated, sialic acid-containing, meningococcal polysaccharides by mass spectrometry. Carbohydr Res 1976; 51:253–261 [View Article][PubMed]
    [Google Scholar]
  53. Harrison OB, Claus H, Jiang Y, Bennett JS, Bratcher HB et al. Description and nomenclature of Neisseria meningitidis capsule locus. Emerg Infect Dis 2013; 19:566–573 [View Article][PubMed]
    [Google Scholar]
  54. Whitney AM, Coulson GB, von Gottberg A, Block C, Keller N et al. Genotypic comparison of invasive Neisseria meningitidis serogroup Y isolates from the United States, South Africa, and Israel, isolated from 1999 through 2002. J Clin Microbiol 2009; 47:2787–2793 [View Article][PubMed]
    [Google Scholar]
  55. Mulcahy ME, Mcloughlin RM. Host–bacterial crosstalk determines Staphylococcus aureus nasal colonization. Trends Microbiol 2016; 24:872–886 [View Article][PubMed]
    [Google Scholar]
  56. Nicolas P, Norheim G, Garnotel E, Djibo S, Caugant DA. Molecular epidemiology of Neisseria meningitidis isolated in the African Meningitis Belt between 1988 and 2003 shows dominance of sequence type 5 (ST-5) and ST-11 complexes. J Clin Microbiol 2005; 43:5129–5135 [View Article][PubMed]
    [Google Scholar]
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