Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 29, Number 11—November 2023
Synopsis

Detection of Novel US Neisseria meningitidis Urethritis Clade Subtypes in Japan

Hideyuki TakahashiComments to Author , Masatomo Morita, Mitsuru Yasuda, Yuki Ohama, Yoshitomo Kobori, Munekado Kojima, Ken Shimuta, Yukihiro Akeda, and Makoto Ohnishi
Author affiliations: National Institute of Infectious Diseases, Tokyo, Japan (H. Takahashi, M. Morita, Y. Ohama, K. Shimuta, Y. Akeda, M. Ohnishi); Sapporo Medical University, Sapporo, Japan (M. Yasuda); Private Care Clinic Tokyo, Tokyo (Y. Kobori); Nagoya Urology Hospital, Aichi, Japan (M. Kojima)

Main Article

Figure 2

Organization of genes within the cps locus of Neisseria meningitidis isolates in study of detection of novel US N. meningitidis urethritis clade subtypes in Japan. N. meningitidis isolates from Japan (NIID835, NIID836, NIID838) and United States (US_NmUC) were compared with N. meningitidis strain FAM18 (GenBank accession no. AM421808). Open red arrows indicate the cssA, cssB, cssC, csc, and cssE genes in region A responsible for capsule synthesis and open blue arrows the ctrD, ctrC, ctrB, and ctrA genes (in that order) in region C responsible for capsule transport. Insertion sequence IS1301 is indicated. Open reading frames identical to NMC0044 (solid red), NMC0049 (gray), NMC0068 (yellow), NMC0071 (green), NMC0073 (pink), and NMC0075 (blue) in FAM18 are shown for each isolate. Partial deletion is indicated for the csc gene (csc′). The cps locus for US_NmUC had 2 configurations created by a ≈20-kb genome inversion between 2 IS1301 sequences (designated as A and B). Gene alignments in the region between the 2 IS1301 sequences have been omitted and are indicated by the dashed line. Although ctrD, ctrC, ctrB, and ctrA genes were shown to be proximal to dnaJ (12), contigs containing the dnaJ-rfbC, rfbA, and rfbB genes and the ctrD, ctrC, ctrB, and ctrA genes (shown on the left side of A and B), as well as 2 IS1301 and pykA genes (shown on the right side of A and B), were not connected by our analysis because of the absence of US_NmUC long-read sequences. Therefore, unidentified connections of the 2 contigs are indicated by a dotted line.

Figure 2. Organization of genes within the cps locus of Neisseria meningitidis isolates in study of detection of novel US N. meningitidis urethritis clade subtypes in Japan. N. meningitidis isolates from Japan (NIID835, NIID836, NIID838) and United States (US_NmUC) were compared with N. meningitidis strain FAM18 (GenBank accession no. AM421808). Open red arrows indicate the cssA, cssB, cssC, csc, and cssE genes in region A responsible for capsule synthesis and open blue arrows the ctrD, ctrC, ctrB, and ctrA genes (in that order) in region C responsible for capsule transport. Insertion sequence IS1301 is indicated. Open reading frames identical to NMC0044 (solid red), NMC0049 (gray), NMC0068 (yellow), NMC0071 (green), NMC0073 (pink), and NMC0075 (blue) in FAM18 are shown for each isolate. Partial deletion is indicated for the csc gene (csc′). The cps locus for US_NmUC had 2 configurations created by a ≈20-kb genome inversion between 2 IS1301 sequences (designated as A and B). Gene alignments in the region between the 2 IS1301 sequences have been omitted and are indicated by the dashed line. Although ctrD, ctrC, ctrB, and ctrA genes were shown to be proximal to dnaJ (12), contigs containing the dnaJ-rfbC, rfbA, and rfbB genes and the ctrD, ctrC, ctrB, and ctrA genes (shown on the left side of A and B), as well as 2 IS1301 and pykA genes (shown on the right side of A and B), were not connected by our analysis because of the absence of US_NmUC long-read sequences. Therefore, unidentified connections of the 2 contigs are indicated by a dotted line.

Main Article

References
  1. Acevedo  R, Bai  X, Borrow  R, Caugant  DA, Carlos  J, Ceyhan  M, et al. The Global Meningococcal Initiative meeting on prevention of meningococcal disease worldwide: Epidemiology, surveillance, hypervirulent strains, antibiotic resistance and high-risk populations. Expert Rev Vaccines. 2019;18:1530. DOIPubMedGoogle Scholar
  2. Taha  MK, Martinon-Torres  F, Köllges  R, Bonanni  P, Safadi  MAP, Booy  R, et al. Equity in vaccination policies to overcome social deprivation as a risk factor for invasive meningococcal disease. Expert Rev Vaccines. 2022;21:65974. DOIPubMedGoogle Scholar
  3. Mustapha  MM, Marsh  JW, Harrison  LH. Global epidemiology of capsular group W meningococcal disease (1970-2015): Multifocal emergence and persistence of hypervirulent sequence type (ST)-11 clonal complex. Vaccine. 2016;34:151523. DOIPubMedGoogle Scholar
  4. Schmink  S, Watson  JT, Coulson  GB, Jones  RC, Diaz  PS, Mayer  LW, et al. Molecular epidemiology of Neisseria meningitidis isolates from an outbreak of meningococcal disease among men who have sex with men, Chicago, Illinois, 2003. J Clin Microbiol. 2007;45:376870. DOIPubMedGoogle Scholar
  5. Marcus  U, Vogel  U, Schubert  A, Claus  H, Baetzing-Feigenbaum  J, Hellenbrand  W, et al. A cluster of invasive meningococcal disease in young men who have sex with men in Berlin, October 2012 to May 2013. Euro Surveill. 2013;18:20523. DOIPubMedGoogle Scholar
  6. Kratz  MM, Weiss  D, Ridpath  A, Zucker  JR, Geevarughese  A, Rakeman  J, et al. Community-based outbreak of Neisseria meningitidis serogroup C infection in men who have sex with men, New York City, New York, USA, 2010–2013. Emerg Infect Dis. 2015;21:137986. DOIPubMedGoogle Scholar
  7. Taha  MK, Claus  H, Lappann  M, Veyrier  FJ, Otto  A, Becher  D, et al. Evolutionary events associated with an outbreak of meningococcal disease in men who have sex with men. PLoS One. 2016;11:e0154047. DOIPubMedGoogle Scholar
  8. Nanduri  S, Foo  C, Ngo  V, Jarashow  C, Civen  R, Schwartz  B, et al. Outbreak of serogroup C meningococcal disease primarily affecting men who have sex with men—Southern California, 2016. MMWR Morb Mortal Wkly Rep. 2016;65:93940. DOIPubMedGoogle Scholar
  9. Folaranmi  TA, Kretz  CB, Kamiya  H, MacNeil  JR, Whaley  MJ, Blain  A, et al. Increased risk for meningococcal disease among men who have sex with men in the United States, 2012–2015. Clin Infect Dis. 2017;65:75663. DOIPubMedGoogle Scholar
  10. Bazan  JA, Peterson  AS, Kirkcaldy  RD, Briere  EC, Maierhofer  C, Turner  AN, et al. Notes from the field: increase in Neisseria meningitidis–associated urethritis among men at two sentinel clinics—Columbus, Ohio, and Oakland County, Michigan, 2015. MMWR Morb Mortal Wkly Rep. 2016;65:5502. DOIPubMedGoogle Scholar
  11. Toh  E, Gangaiah  D, Batteiger  BE, Williams  JA, Arno  JN, Tai  A, et al. Neisseria meningitidis ST11 complex isolates associated with nongonococcal urethritis, Indiana, USA, 2015–2016. Emerg Infect Dis. 2017;23:3369. DOIPubMedGoogle Scholar
  12. Tzeng  YL, Bazan  JA, Turner  AN, Wang  X, Retchless  AC, Read  TD, et al. Emergence of a new Neisseria meningitidis clonal complex 11 lineage 11.2 clade as an effective urogenital pathogen. Proc Natl Acad Sci U S A. 2017;114:423742. DOIPubMedGoogle Scholar
  13. Bazan  JA, Stephens  DS, Turner  AN. Emergence of a novel urogenital-tropic Neisseria meningitidis. Curr Opin Infect Dis. 2021;34:349. DOIPubMedGoogle Scholar
  14. Burns  BL, Rhoads  DD. Meningococcal urethritis: old and new. J Clin Microbiol. 2022;60:e0057522. DOIPubMedGoogle Scholar
  15. Bartley  SN, Tzeng  YL, Heel  K, Lee  CW, Mowlaboccus  S, Seemann  T, et al. Attachment and invasion of Neisseria meningitidis to host cells is related to surface hydrophobicity, bacterial cell size and capsule. PLoS One. 2013;8:e55798. DOIPubMedGoogle Scholar
  16. Yee  WX, Barnes  G, Lavender  H, Tang  CM. Meningococcal factor H-binding protein: implications for disease susceptibility, virulence, and vaccines. Trends Microbiol. 2023;31:80515. DOIPubMedGoogle Scholar
  17. Tzeng  YL, Sannigrahi  S, Berman  Z, Bourne  E, Edwards  JL, Bazan  JA, et al. Acquisition of gonococcal AniA-NorB pathway by the Neisseria meningitidis urethritis clade confers denitrifying and microaerobic respiration advantages for urogenital adaptation. Infect Immun. 2023;91:e0007923. DOIPubMedGoogle Scholar
  18. Brooks  A, Lucidarme  J, Campbell  H, Campbell  L, Fifer  H, Gray  S, et al. Detection of the United States Neisseria meningitidis urethritis clade in the United Kingdom, August and December 2019 - emergence of multiple antibiotic resistance calls for vigilance. Euro Surveill. 2020;25:2000375. DOIPubMedGoogle Scholar
  19. Nguyen  HT, Phan  TV, Tran  HP, Vu  TTP, Pham  NTU, Nguyen  TTT, et al. Outbreak of sexually transmitted nongroupable Neisseria meningitidis–associated urethritis, Vietnam. Emerg Infect Dis. 2023;29:21304. DOIPubMedGoogle Scholar
  20. Taha  MK. Simultaneous approach for nonculture PCR-based identification and serogroup prediction of Neisseria meningitidis. J Clin Microbiol. 2000;38:8557. DOIPubMedGoogle Scholar
  21. Maiden  MC, Bygraves  JA, Feil  E, Morelli  G, Russell  JE, Urwin  R, 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;95:31405. DOIPubMedGoogle Scholar
  22. Saito  R, Nakajima  J, Prah  I, Morita  M, Mahazu  S, Ota  Y, et al. Penicillin- and ciprofloxacin-resistant invasive Neisseria meningitidis isolates from Japan. Microbiol Spectr. 2022;10:e0062722. DOIPubMedGoogle Scholar
  23. Wick  RR, Judd  LM, Holt  KE. Performance of neural network basecalling tools for Oxford Nanopore sequencing. Genome Biol. 2019;20:129. DOIPubMedGoogle Scholar
  24. 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. DOIPubMedGoogle Scholar
  25. Tanizawa  Y, Fujisawa  T, Nakamura  Y. DFAST: a flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics. 2018;34:10379. DOIPubMedGoogle Scholar
  26. Page  AJ, Cummins  CA, Hunt  M, Wong  VK, Reuter  S, Holden  MT, et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics. 2015;31:36913. DOIPubMedGoogle Scholar
  27. Page  AJ, Taylor  B, Delaney  AJ, Soares  J, Seemann  T, Keane  JA, et al. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microb Genom. 2016;2:e000056. DOIPubMedGoogle Scholar
  28. Letunic  I, Bork  P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49(W1):W2936. DOIPubMedGoogle Scholar
  29. Takahashi  H, Morita  M, Kamiya  H, Fukusumi  M, Sunagawa  M, Nakamura-Miwa  H, et al. Genomic characterization of Japanese meningococcal strains isolated over a 17-year period between 2003 and 2020 in Japan. Vaccine. 2023;41:41626. DOIPubMedGoogle Scholar
  30. Ma  KC, Unemo  M, Jeverica  S, Kirkcaldy  RD, Takahashi  H, Ohnishi  M, et al. Genomic characterization of urethritis-associated Neisseria meningitidis shows that a wide range of N. meningitidis strains can cause urethritis. J Clin Microbiol. 2017;55:337483. DOIPubMedGoogle Scholar
  31. Tettelin  H, Saunders  NJ, Heidelberg  J, Jeffries  AC, Nelson  KE, Eisen  JA, et al. Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science. 2000;287:180915. DOIPubMedGoogle Scholar
  32. Retchless  AC, Kretz  CB, Chang  HY, Bazan  JA, Abrams  AJ, Norris Turner  A, et al. Expansion of a urethritis-associated Neisseria meningitidis clade in the United States with concurrent acquisition of N. gonorrhoeae alleles. BMC Genomics. 2018;19:176. DOIPubMedGoogle Scholar
  33. Biagini  M, Spinsanti  M, De Angelis  G, Tomei  S, Ferlenghi  I, Scarselli  M, et al. Expression of factor H binding protein in meningococcal strains can vary at least 15-fold and is genetically determined. Proc Natl Acad Sci U S A. 2016;113:27149. DOIPubMedGoogle Scholar
  34. Sukhum  KV, Jean  S, Wallace  M, Anderson  N, Burnham  CA, Dantas  G. Genomic characterization of emerging bacterial uropathogen Neisseria meningitidis, which was misidentified as Neisseria gonorrhoeae by nucleic acid amplification testing. J Clin Microbiol. 2021;59:e0169920. DOIPubMedGoogle Scholar
  35. Bazan  JA, Tzeng  YL, Bischof  KM, Satola  SW, Stephens  DS, Edwards  JL, et al. Antibiotic susceptibility profile for the US Neisseria meningitidis urethritis clade. Open Forum Infect Dis. 2023;10:ofac661.
  36. Willerton  L, Lucidarme  J, Walker  A, Lekshmi  A, Clark  SA, Walsh  L, et al. Antibiotic resistance among invasive Neisseria meningitidis isolates in England, Wales and Northern Ireland (2010/11 to 2018/19). PLoS One. 2021;16:e0260677. DOIPubMedGoogle Scholar
  37. Kretz  CB, Bergeron  G, Aldrich  M, Bloch  D, Del Rosso  PE, Halse  TA, et al. Neonatal conjunctivitis caused by Neisseria meningitidis US urethritis clade, New York, USA, August 2017. Emerg Infect Dis. 2019;25:9725. DOIPubMedGoogle Scholar
  38. Virji  M, Makepeace  K, Ferguson  DJ, Achtman  M, Sarkari  J, Moxon  ER. Expression of the Opc protein correlates with invasion of epithelial and endothelial cells by Neisseria meningitidis. Mol Microbiol. 1992;6:278595. DOIPubMedGoogle Scholar
  39. Stephens  DS, Spellman  PA, Swartley  JS. Effect of the (alpha 2—>8)-linked polysialic acid capsule on adherence of Neisseria meningitidis to human mucosal cells. J Infect Dis. 1993;167:4759. DOIPubMedGoogle Scholar
  40. McNeil  G, Virji  M, Moxon  ER. Interactions of Neisseria meningitidis with human monocytes. Microb Pathog. 1994;16:15363. DOIPubMedGoogle Scholar
  41. Kolb-Mäurer  A, Unkmeir  A, Kämmerer  U, Hübner  C, Leimbach  T, Stade  A, et al. Interaction of Neisseria meningitidis with human dendritic cells. Infect Immun. 2001;69:691222. DOIPubMedGoogle Scholar
  42. Hill  DJ, Griffiths  NJ, Borodina  E, Virji  M. Cellular and molecular biology of Neisseria meningitidis colonization and invasive disease. Clin Sci (Lond). 2010;118:54764. DOIPubMedGoogle Scholar
  43. Sutherland  TC, Quattroni  P, Exley  RM, Tang  CM. Transcellular passage of Neisseria meningitidis across a polarized respiratory epithelium. Infect Immun. 2010;78:383247. DOIPubMedGoogle Scholar
  44. Takahashi  H, Kim  KS, Watanabe  H. Differential in vitro infectious abilities of two common Japan-specific sequence-type (ST) clones of disease-associated ST-2032 and carrier-associated ST-2046 Neisseria meningitidis strains in human endothelial and epithelial cell lines. FEMS Immunol Med Microbiol. 2008;52:3646. DOIPubMedGoogle Scholar
  45. Stefanelli  P, Colotti  G, Neri  A, Salucci  ML, Miccoli  R, Di Leandro  L, et al. Molecular characterization of nitrite reductase gene (aniA) and gene product in Neisseria meningitidis isolates: is aniA essential for meningococcal survival? IUBMB Life. 2008;60:62936. DOIPubMedGoogle Scholar
  46. Barth  KR, Isabella  VM, Clark  VL. Biochemical and genomic analysis of the denitrification pathway within the genus Neisseria. Microbiology (Reading). 2009;155:4093103. DOIPubMedGoogle Scholar
  47. Takahashi  H, Kuroki  T, Watanabe  Y, Tanaka  H, Inouye  H, Yamai  S, et al. Characterization of Neisseria meningitidis isolates collected from 1974 to 2003 in Japan by multilocus sequence typing. J Med Microbiol. 2004;53:65762. DOIPubMedGoogle Scholar
  48. Fukusumi  M, Kamiya  H, Takahashi  H, Kanai  M, Hachisu  Y, Saitoh  T, et al. National surveillance for meningococcal disease in Japan, 1999-2014. Vaccine. 2016;34:406871. DOIPubMedGoogle Scholar
  49. Jolley  KA, Maiden  MCJ. BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics. 2010;11:595. DOIPubMedGoogle Scholar

Main Article

Page created: September 29, 2023
Page updated: October 23, 2023
Page reviewed: October 23, 2023
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external