1887

Abstract

Only approximately 40 cases of invasive meningococcal diseases are reported annually in Japan, and the dominant strains are serogroup Y meningococci (MenY) followed by serogroup B meningococci (MenB). Within the last 10 years, strains belonging to clonal complex (cc)2057 have become dominant among Japanese MenB and have not been identified in countries other than Japan.

The uniqueness of cc2057 strains was considered to be epidemiologically of importance, and some genetic features could be hidden in the genome of cc2057 meningococci.

We investigated 22 cc2057 MenB and one cc2057 MenY using whole genome sequencing (WGS) and also predicted the potential coverage of 4CMenB and bivalent rLP2086 vaccines .

cc2057 strains were phylogenetically assigned to two clades. Three hypothetical genes homologous to those in and sequences related to a new CRISPR Cas9 system were found only in the genome of cc2057 strains. Moreover, one cc2057 MenY strain was presumed to be capsular-switched at the capsule synthesis () locus. The potential coverage of 4CMenB and rLP2086 for cc2057 MenB strains was estimated to be very low.

To the best of our knowledge, this is the first study to provide genetic insights from epidemiologically unique cc2057 strains isolated only in Japan, an island country.

Funding
This study was supported by the:
  • Ministry of Health, Labour and Welfare (Award JPMH19HA100)
    • Principle Award Recipient: HideyukiTakahashi
  • Japan Society for the Promotion of Science (Award 19KO7550)
    • Principle Award Recipient: HideyukiTakahashi
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001504
2022-03-03
2024-04-25
Loading full text...

Full text loading...

References

  1. Fukusumi M, Kamiya H, Takahashi H, Kanai M, Hachisu Y et al. National surveillance for meningococcal disease in Japan, 1999-2014. Vaccine 2016; 34:4068–4071 [View Article] [PubMed]
    [Google Scholar]
  2. Borrow R, Lee J-S, Vázquez JA, Enwere G, Taha M-K et al. Meningococcal disease in the Asia-Pacific region: Findings and recommendations from the Global Meningococcal Initiative. Vaccine 2016; 34:5855–5862 [View Article] [PubMed]
    [Google Scholar]
  3. Takahashi H, Haga M, Sunagawa T, Saitoh T, Kitahara T et al. Meningococcal carriage rates in healthy individuals in Japan determined using Loop-Mediated Isothermal Amplification and oral throat wash specimens. J Infect Chemother 2016; 22:501–504 [View Article] [PubMed]
    [Google Scholar]
  4. Tanaka H, Kuroki T, Watanabe Y, Asai Y, Ootani K et al. Isolation of Neisseria meningitidis from healthy persons in Japan. Kansenshogaku Zasshi 2005; 79:527–533 [View Article] [PubMed]
    [Google Scholar]
  5. Tzeng YL, Thomas J, Stephens DS. Regulation of capsule in Neisseria meningitidis. Crit Rev Microbiol 2016; 42:759–772 [View Article] [PubMed]
    [Google Scholar]
  6. 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 U S A 1998; 95:3140–3145 [View Article] [PubMed]
    [Google Scholar]
  7. Kesanopoulos K, Bratcher HB, Hong E, Xirogianni A, Papandreou A et al. Characterization of meningococcal carriage isolates from Greece by whole genome sequencing: Implications for 4CMenB vaccine implementation. PLoS One 2018; 13:e0209919 [View Article] [PubMed]
    [Google Scholar]
  8. Stefanelli P, Fazio C, Vacca P, Palmieri A, Ambrosio L et al. An outbreak of severe invasive meningococcal disease due to a capsular switched Neisseria meningitidis hypervirulent strain B:cc11. Clin Microbiol Infect 2019; 25:111 [View Article] [PubMed]
    [Google Scholar]
  9. Muzzi A, Brozzi A, Serino L, Bodini M, Abad R et al. Genetic Meningococcal Antigen Typing System (gMATS): A genotyping tool that predicts 4CMenB strain coverage worldwide. Vaccine 2019; 37:991–1000 [View Article] [PubMed]
    [Google Scholar]
  10. Rodrigues CMC, Jolley KA, Smith A, Cameron JC, Feavers IM et al. Meningococcal Deduced Vaccine Antigen Reactivity (MenDeVAR) index: a rapid and accessible tool that exploits genomic data in public health and clinical microbiology applications. J Clin Microbiol 2020; 59:e02161–02120 [View Article] [PubMed]
    [Google Scholar]
  11. Mowlaboccus S, Mullally CA, Richmond PC, Howden BP, Stevens K et al. Differences in the population structure of Neisseria meningitidis in two Australian states: Victoria and Western Australia. PLoS One 2017; 12:e0186839 [View Article] [PubMed]
    [Google Scholar]
  12. Bodini M, Brozzi A, Giuliani M, Nohynek H, Vainio A et al. Genomic Characterization of Invasive Meningococcal Serogroup B Isolates and Estimation of 4CMenB Vaccine Coverage in Finland. mSphere 2020; 5:e00376–00320 [View Article] [PubMed]
    [Google Scholar]
  13. Tsang RSW, Law DKS, De Paola R, Giuliani M, Stella M et al. Culture-Confirmed Invasive Meningococcal Disease in Canada, 2010 to 2014: Characterization of Serogroup B Neisseria meningitidis Strains and Their Predicted Coverage by the 4CMenB Vaccine. mSphere 2020; 5:e00883–00819 [View Article] [PubMed]
    [Google Scholar]
  14. Leo S, Lazarevic V, Girard M, Getaz-Jimenez Velasco GC, Gaïa N et al. Strain coverage of Bexsero vaccine assessed by whole-genome sequencing over a cohort of invasive meningococci of serogroups B and W isolated in Switzerland. Vaccine 2020; 38:5324–5331 [View Article] [PubMed]
    [Google Scholar]
  15. Mulhall RM, Bennett D, Cunney R, Borrow R, Lucidarme J et al. Potential Coverage of the 4CMenB Vaccine against Invasive Serogroup B Neisseria meningitidis Isolated from 2009 to 2013 in the Republic of Ireland. mSphere 2018; 3:e00196–00118 [View Article] [PubMed]
    [Google Scholar]
  16. Rouphael NG, Stephens DS. Neisseria meningitidis: biology, microbiology, and epidemiology. Methods Mol Biol 2012; 799:1–20 [View Article] [PubMed]
    [Google Scholar]
  17. Takahashi H, Kuroki T, Watanabe Y, Tanaka H, Inouye H et al. Characterization of Neisseria meningitidis isolates collected from 1974 to 2003 in Japan by multilocus sequence typing. J Med Microbiol 2004; 53:657–662 [View Article] [PubMed]
    [Google Scholar]
  18. Taha MK. Simultaneous approach for nonculture PCR-based identification and serogroup prediction of Neisseria meningitidis. J Clin Microbiol 2000; 38:855–857 [View Article] [PubMed]
    [Google Scholar]
  19. Takahashi H, Watanabe H, Kim KS, Yokoyama S, Yanagisawa T. The meningococcal cysteine transport system plays a crucial role in Neisseria meningitidis survival in human brain microvascular endothelial cells. mBio 2018; 9:e02332–02318 [View Article] [PubMed]
    [Google Scholar]
  20. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  21. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M et al. Versatile and open software for comparing large genomes. Genome Biol 2004; 5:R12 [View Article] [PubMed]
    [Google Scholar]
  22. Clarke J, Wu H-C, Jayasinghe L, Patel A, Reid S et al. Continuous base identification for single-molecule nanopore DNA sequencing. Nat Nanotechnol 2009; 4:265–270 [View Article] [PubMed]
    [Google Scholar]
  23. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
    [Google Scholar]
  24. Karimi Z, Ahmadi A, Najafi A, Ranjbar R. Bacterial CRISPR regions: general features and their potential for epidemiological molecular typing studies. Open Microbiol J 2018; 12:59–70 [View Article] [PubMed]
    [Google Scholar]
  25. 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]
  26. Shao Z, Li W, Ren J, Liang X, Xu L et al. Identification of a new Neisseria meningitidis serogroup C clone from Anhui province, China. Lancet 2006; 367:419–423 [View Article] [PubMed]
    [Google Scholar]
  27. Zhang X, Shao Z, Yang E, Xu L, Xu X et al. Molecular characterization of serogroup C Neisseria meningitidis isolated in China. J Med Microbiol 2007; 56:1224–1229 [View Article] [PubMed]
    [Google Scholar]
  28. Zhu B, Xu Z, Du P, Xu L, Sun X et al. Sequence Type 4821 Clonal Complex Serogroup B Neisseria meningitidis in China, 1978-2013. Emerg Infect Dis 2015; 21:925–932 [View Article] [PubMed]
    [Google Scholar]
  29. Lucidarme J, Zhu B, Xu L, Bai X, Gao Y et al. Genomic analysis of the meningococcal ST-4821 complex-Western clade, potential sexual transmission and predicted antibiotic susceptibility and vaccine coverage. PLoS One 2020; 15:e0243426 [View Article] [PubMed]
    [Google Scholar]
  30. Tsang RS, Law DK, Tyler SD, Stephens GS, Bigham M et al. Potential capsule switching from serogroup Y to B: The characterization of three such Neisseria meningitidis isolates causing invasive meningococcal disease in Canada. Can J Infect Dis Med Microbiol 2005; 16:171–174 [View Article] [PubMed]
    [Google Scholar]
  31. Beddek AJ, Li MS, Kroll JS, Jordan TW, Martin DR. Evidence for capsule switching between carried and disease-causing Neisseria meningitidis strains. Infect Immun 2009; 77:2989–2994 [View Article] [PubMed]
    [Google Scholar]
  32. Lucidarme J, Hill DMC, 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]
  33. Wang Q, Shao Z, Wang X, Gao Y, Li M et al. Genetic study of capsular switching between Neisseria meningitidis sequence type 7 serogroup A and C strains. Infect Immun 2010; 78:3883–3888 [View Article] [PubMed]
    [Google Scholar]
  34. Stefanelli P, Fazio C, Neri A, Sofia T, Mastrantonio P. First report of capsule replacement among electrophoretic type 37 Neisseria meningitidis strains in Italy. J Clin Microbiol 2003; 41:5783–5786 [View Article] [PubMed]
    [Google Scholar]
  35. Lancellotti M, Guiyoule A, Ruckly C, Hong E, Alonso J-M et al. Conserved virulence of C to B capsule switched Neisseria meningitidis clinical isolates belonging to ET-37/ST-11 clonal complex. Microbes Infect 2006; 8:191–196 [View Article] [PubMed]
    [Google Scholar]
  36. Simões MJ, Cunha M, Almeida F, Furtado C, Brum L. Molecular surveillance of Neisseria meningitidis capsular switching in Portugal, 2002-2006. Epidemiol Infect 2009; 137:161–165 [View Article] [PubMed]
    [Google Scholar]
  37. Harrison LH, Shutt KA, Schmink SE, Marsh JW, Harcourt BH et al. Population structure and capsular switching of invasive Neisseria meningitidis isolates in the pre-meningococcal conjugate vaccine era--United States, 2000-2005. J Infect Dis 2010; 201:1208–1224 [View Article] [PubMed]
    [Google Scholar]
  38. Trotter CL, Ramsay ME, Gray S, Fox A, Kaczmarski E. No evidence for capsule replacement following mass immunisation with meningococcal serogroup C conjugate vaccines in England and Wales. Lancet Infect Dis 2006; 6:616–617 [View Article] [PubMed]
    [Google Scholar]
  39. Castiñeiras TMPP, Barroso DE, Marsh JW, Tulenko MM, Krauland MG et al. Capsular switching in invasive Neisseria meningitidis, Brazil(1). Emerg Infect Dis 2012; 18:1336–1338 [View Article] [PubMed]
    [Google Scholar]
  40. Wang X, Shutt KA, Vuong JT, Cohn A, MacNeil J et al. Changes in the population structure of invasive Neisseria meningitidis in the United States after quadrivalent meningococcal conjugate vaccine licensure. J Infect Dis 2015; 211:1887–1894 [View Article] [PubMed]
    [Google Scholar]
  41. Pan J, Yao P, Zhang H, Sun X, He H et al. The case of a new sequence type 7 serogroup X Neisseria meningitidis infection in China: may capsular switching change serogroup profile?. Int J Infect Dis 2014; 29:62–64 [View Article] [PubMed]
    [Google Scholar]
  42. Bettencourt C, Nunes A, Correia AM, Gomes JP, Simões MJ. Lung abscess due to Neisseria meningitidis serogroup X-unexpected virulence of a commensal resulting from putative serogroup B capsular switching. Eur J Clin Microbiol Infect Dis 2020; 39:2327–2334 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001504
Loading
/content/journal/jmm/10.1099/jmm.0.001504
Loading

Data & Media loading...

Supplements

Supplementary material 1

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