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Abstract

The PorB porins are the major pore-forming proteins in the genus . The trimeric PorB porins consist of 16 highly conserved transmembrane domains that form an amphipathic β-sheet connected by short periplasmic turns and eight extracellular hydrophilic loops. These loops are immunogenic and also play an important role in mediating antimicrobial influx. This study sought to (i) characterize the variations in Neisserial loop 3(355–438 bp) associated with intermediate resistance to penicillin/tetracycline and (ii) evaluate if there was evidence of horizontal gene transfer in any of the loops. We collated an integrated database consisting of 19 018 spp. genomes – 17 882 , 114 and 1022 commensal spp. To identify the alleles, a gene-by-gene approach (chewBBACA) was employed. To evaluate the presence of recombination events, the Recombination Detection Programme (RDP4) was used. In total, 3885 alleles were detected. Paralogues were identified in 17 isolates. Putative recombination was identified in loop regions. Intraspecies recombination among isolates and interspecies recombination between and commensal spp., and and were identified. Here, we present a large-scale study of 19 018 isolates to describe recombination and variation in the porB gene. Importantly, we found putative recombination in loop regions between the pathogenic and non-pathogenic spp. These findings suggest the need for pheno- and genotypic surveillance of antimicrobial susceptibility in commensal spp. to prevent the emergence of AMR in the pathogenic . This article contains data hosted by Microreact.

Funding
This study was supported by the:
  • SOFI 2021 grant—“PReventing the Emergence of untreatable STIs via radical Prevention” (PRESTIP).
    • Principle Award Recipient: ChrisKenyon
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2023-06-09
2024-05-03
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References

  1. Manoharan-Basil SS, Gestels Z, Abdellati S, Akomoneh EA, Kenyon C. Evidence of horizontal Gene transfer within porB in 19 018 whole-genome Neisseria spp. isolates: a global phylogenetic analysis. Microbiology Society. Dataset 2023 [View Article]
    [Google Scholar]
  2. Quillin SJ, Seifert HS. Neisseria gonorrhoeae host adaptation and pathogenesis. Nat Rev Microbiol 2018; 16:226–240 [View Article] [PubMed]
    [Google Scholar]
  3. Retchless AC, Kretz CB, Chang H-Y, Bazan JA, Abrams AJ 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 [View Article] [PubMed]
    [Google Scholar]
  4. Tinsley CR, Nassif X. Analysis of the genetic differences between Neisseria meningitidis and Neisseria gonorrhoeae: two closely related bacteria expressing two different pathogenicities. Proc Natl Acad Sci 1996; 93:11109–11114 [View Article] [PubMed]
    [Google Scholar]
  5. Everts RJ, Speers D, George ST, Ansell BJ, Karunajeewa H et al. Neisseria lactamica arthritis and septicemia complicating myeloma. J Clin Microbiol 2010; 48:2318 [View Article] [PubMed]
    [Google Scholar]
  6. Kozlova A, Palazzolo L, Michael A. Neisseria sicca: a rare cause of bacterial conjunctivitis. Am J Case Rep 2020; 21:e923135 [View Article] [PubMed]
    [Google Scholar]
  7. 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]
    [Google Scholar]
  8. McDade K, Singla A, Pash D, Bavaro M, De La Houssaye C. Neisseria cinerea bacteremia secondary to a retropharyngeal abscess. Cureus 2021; 13:e14217 [View Article] [PubMed]
    [Google Scholar]
  9. Murphy TF. 215 - Moraxella catarrhalis, Kingella, and other Gram-negative cocci. In Bennett JE, Dolin R, Blaser D. eds Bennett’s Principles and Practice of Infectious Diseases (Eighth Edition) MJBT-M (Eds). W.B. Saunders Philadelphia: Saunders; 2015 pp 2463–2470e2
    [Google Scholar]
  10. Uwamino Y, Sugita K, Iwasaki E, Fujiwara H, Nishimura T et al. The first case report of acute cholangitis and bacteremia due to Neisseria subflava. Intern Med 2017; 56:221–223 [View Article] [PubMed]
    [Google Scholar]
  11. Derrick JP, Urwin R, Suker J, Feavers IM, Maiden MC. Structural and evolutionary inference from molecular variation in Neisseria porins. Infect Immun 1999; 67:2406–2413 [View Article] [PubMed]
    [Google Scholar]
  12. Gotschlich EC, Seiff ME, Blake MS, Koomey M. Porin protein of Neisseria gonorrhoeae: cloning and gene structure. Proc Natl Acad Sci 1987; 84:8135–8139 [View Article] [PubMed]
    [Google Scholar]
  13. Haines KA, Yeh L, Blake MS, Cristello P, Korchak H et al. Protein I, a translocatable ion channel from Neisseria gonorrhoeae, selectively inhibits exocytosis from human neutrophils without inhibiting O2- generation. J Biol Chem 1988; 263:945–951 [PubMed]
    [Google Scholar]
  14. Rudel T, Schmid A, Benz R, Kolb HA, Lang F et al. Modulation of Neisseria porin (PorB) by cytosolic ATP/GTP of target cells: parallels between pathogen accommodation and mitochondrial endosymbiosis. Cell 1996; 85:391–402 [View Article] [PubMed]
    [Google Scholar]
  15. Brunham RC, Plummer F, Slaney L, Rand F, DeWitt W. Correlation of auxotype and protein I type with expression of disease due to Neisseria gonorrhoeae. J Infect Dis 1985; 152:339–343 [View Article] [PubMed]
    [Google Scholar]
  16. Cannon JG, Buchanan TM, Sparling PF. Confirmation of association of protein I serotype of Neisseria gonorrhoeae with ability to cause disseminated infection. Infect Immun 1983; 40:816–819 [View Article]
    [Google Scholar]
  17. Carbonetti NH, Simnad VI, Seifert HS, So M, Sparling PF. Genetics of protein I of Neisseria gonorrhoeae: construction of hybrid porins. Proc Natl Acad Sci 1988; 85:6841–6845 [View Article]
    [Google Scholar]
  18. Fudyk TC, Maclean IW, Simonsen JN, Njagi EN, Kimani J et al. Genetic diversity and mosaicism at the por locus of Neisseria gonorrhoeae. J Bacteriol 1999; 181:5591–5599 [View Article] [PubMed]
    [Google Scholar]
  19. Massari P, Ram S, Macleod H, Wetzler LM. The role of porins in Neisserial pathogenesis and immunity. Trends Microbiol 2003; 11:87–93 [View Article] [PubMed]
    [Google Scholar]
  20. Olesky M, Zhao S, Rosenberg RL, Nicholas RA. Porin-mediated antibiotic resistance in Neisseria gonorrhoeae: ion, solute, and antibiotic permeation through PIB proteins with penB mutations. J Bacteriol 2006; 188:2300–2308 [View Article] [PubMed]
    [Google Scholar]
  21. Frasch CE, Zollinger WD, Poolman JT. Serotype antigens of Neisseria meningitidis and a proposed scheme for designation of serotypes. Rev Infect Dis 1985; 7:504–510 [View Article] [PubMed]
    [Google Scholar]
  22. Feavers IM, Maiden MC. A gonococcal porA pseudogene: implications for understanding the evolution and pathogenicity of Neisseria gonorrhoeae. Mol Microbiol 1998; 30:647–656 [View Article] [PubMed]
    [Google Scholar]
  23. Carbonetti NH, Sparling PF. Molecular cloning and characterization of the structural gene for protein I, the major outer membrane protein of Neisseria gonorrhoeae. Proc Natl Acad Sci 1987; 84:9084–9088 [View Article] [PubMed]
    [Google Scholar]
  24. Foerster S, Drusano G, Golparian D, Neely M, Piddock LJV et al. In vitro antimicrobial combination testing of and evolution of resistance to the first-in-class spiropyrimidinetrione zoliflodacin combined with six therapeutically relevant antimicrobials for Neisseria gonorrhoeae. J Antimicrob Chemother 2019; 74:3521–3529 [View Article] [PubMed]
    [Google Scholar]
  25. Mee BJ, Thomas H, Cooke SJ, Lambden PR, Heckels JE. Structural comparison and epitope analysis of outer-membrane protein PIA from strains of Neisseria gonorrhoeae with differing serovar specificities. J Gen Microbiol 1993; 139:2613–2620 [View Article] [PubMed]
    [Google Scholar]
  26. Garvin LE, Bash MC, Keys C, Warner DM, Ram S et al. Phenotypic and genotypic analyses of Neisseria gonorrhoeae isolates that express frequently recovered PorB PIA variable region types suggest that certain P1a porin sequences confer a selective advantage for urogenital tract infection. Infect Immun 2008; 76:3700–3709 [View Article] [PubMed]
    [Google Scholar]
  27. Gotschlich EC. Gram-negative cocci, pathogenic. In Schaechter MBT-E of M, 3rd. edn Oxford: Academic Press; 2009 pp 133–144
    [Google Scholar]
  28. Gill MJ, Simjee S, Al-Hattawi K, Robertson BD, Easmon CSF et al. Gonococcal resistance to β-Lactams and tetracycline involves mutation in loop 3 of the porin encoded at the penB locus. Antimicrob Agents Chemother 1998; 42:2799–2803 [View Article]
    [Google Scholar]
  29. Olesky M, Hobbs M, Nicholas RA. Identification and analysis of amino acid mutations in porin IB that mediate intermediate-level resistance to penicillin and tetracycline in Neisseria gonorrhoeae. Antimicrob Agents Chemother 2002; 46:2811–2820 [View Article] [PubMed]
    [Google Scholar]
  30. Baarda BI, Zielke RA, Holm AK, Sikora AE, Burns DL. Comprehensive bioinformatic assessments of the variability of Neisseria gonorrhoeae vaccine candidates. mSphere 2021; 6: [View Article]
    [Google Scholar]
  31. Rice PA, Shafer WM, Ram S, Jerse AE. Neisseria gonorrhoeae: drug resistance,mouse models, and vaccine development. Annu Rev Microbiol 2017; 71:665–686 [View Article] [PubMed]
    [Google Scholar]
  32. Russell MW, Jerse AE, Gray-Owen SD. Progress toward a gonococcal vaccine: the way forward. Front Immunol 2019; 10:2417 [View Article] [PubMed]
    [Google Scholar]
  33. Kim JJ, Mandrell RE, Griffiss JM. Neisseria lactamica and Neisseria meningitidis share lipooligosaccharide epitopes but lack common capsular and class 1, 2, and 3 protein epitopes. Infect Immun 1989; 57:602–608 [View Article]
    [Google Scholar]
  34. Troncoso G, Sánchez S, Criado MT, Ferreirós CM. Analysis of Neisseria lactamica antigens putatively implicated in acquisition of natural immunity to Neisseria meningitidis. FEMS Immunol Med Microbiol 2002; 34:9–15 [View Article]
    [Google Scholar]
  35. Bennett JS, Callaghan MJ, Derrick JP, Maiden MCJ. Variation in the Neisseria lactamica porin, and its relationship to meningococcal PorB. Microbiology 2008; 154:1525–1534 [View Article]
    [Google Scholar]
  36. Bowler LD, Zhang QY, Riou JY, Spratt BG. Interspecies recombination between the penA genes of Neisseria meningitidis and commensal Neisseria species during the emergence of penicillin resistance in N. meningitidis: natural events and laboratory simulation. J Bacteriol 1994; 176:333–337 [View Article] [PubMed]
    [Google Scholar]
  37. Fiore MA, Raisman JC, Wong NH, Hudson AO, Wadsworth CB. Exploration of the Neisseria resistome reveals resistance mechanisms in commensals that may be acquired by N. gonorrhoeae through horizontal gene transfer. Antibiotics 2020; 9:656 [View Article]
    [Google Scholar]
  38. Manoharan-Basil SS, González N, Laumen JGE, Kenyon C. Horizontal gene transfer of fluoroquinolone resistance-conferring genes from commensal Neisseria to Neisseria gonorrhoeae: a global phylogenetic analysis of 20,047 isolates. Front Microbiol 2022; 13:793612 [View Article] [PubMed]
    [Google Scholar]
  39. Manoharan-Basil SS, Laumen JGE, Van Dijck C, De Block T, De Baetselier I et al. Evidence of horizontal gene transfer of 50S ribosomal genes rplB, rplD, and rplY in Neisseria gonorrhoeae. Front Microbiol 2021; 12:1263 [View Article]
    [Google Scholar]
  40. Shafer WM. Mosaic drug efflux gene sequences from commensal Neisseria can lead to low-level azithromycin resistance expressed by Neisseria gonorrhoeae clinical isolates. mBio 2018; 9:e01747-18 [View Article] [PubMed]
    [Google Scholar]
  41. Wadsworth CB, Arnold BJ, Sater MRA, Grad YH. Azithromycin resistance through interspecific acquisition of an epistasis-dependent efflux pump component and transcriptional regulator in Neisseria gonorrhoeae. mBio 2018; 9:e01419-18 [View Article] [PubMed]
    [Google Scholar]
  42. Yahara K, Nakayama S, Shimuta K, Lee K, Morita M et al. Genomic surveillance of Neisseria gonorrhoeae to investigate the distribution and evolution of antimicrobial-resistance determinants and lineages. Microbial Genomics 2018; 4: [View Article]
    [Google Scholar]
  43. Chen X, Cai X, Chen Z, Wu J, Hao G et al. Mosaic evolution of Beta-Barrel-Porin-Encoding genes in Escherichia coli. Appl Environ Microbiol 2022; 88:e0006022 [View Article] [PubMed]
    [Google Scholar]
  44. Stenkova AM, Isaeva MP, Shubin FN, Rasskazov VA, Rakin AV. Trends of the major porin gene (ompF) evolution: insight from the genus Yersinia. PLoS One 2011; 6:e20546 [View Article] [PubMed]
    [Google Scholar]
  45. Harrison OB, Cehovin A, Skett J, Jolley KA, Massari P et al. Neisseria gonorrhoeae population genomics: use of the gonococcal core genome to improve surveillance of antimicrobial resistance. J Infect Dis 2020; 222:1816–1825 [View Article]
    [Google Scholar]
  46. O’Rourke M, Stevens E. Genetic structure of Neisseria gonorrhoeae populations: a non-clonal pathogen. J Gen Microbiol 1993; 139:2603–2611 [View Article] [PubMed]
    [Google Scholar]
  47. Pérez-Losada M, Viscidi RP, Demma JC, Zenilman J, Crandall KA. Population genetics of Neisseria gonorrhoeae in a high-prevalence community using a hypervariable outer membrane porB and 13 slowly evolving housekeeping genes. Mol Biol Evol 2005; 22:1887–1902 [View Article] [PubMed]
    [Google Scholar]
  48. Chen A, Seifert HS. Saturating mutagenesis of an essential gene: a majority of the Neisseria gonorrhoeae major outer membrane porin (PorB) is mutable. J Bacteriol 2014; 196:540–547 [View Article] [PubMed]
    [Google Scholar]
  49. Urwin R, Holmes EC, Fox AJ, Derrick JP, Maiden MCJ. Phylogenetic evidence for frequent positive selection and recombination in the meningococcal surface antigen PorB. Mol Biol Evol 2002; 19:1686–1694 [View Article] [PubMed]
    [Google Scholar]
  50. Feil EJ, Holmes EC, Bessen DE, Chan MS, Day NP et al. Recombination within natural populations of pathogenic bacteria: short-term empirical estimates and long-term phylogenetic consequences. Proc Natl Acad Sci 2001; 98:182–187 [View Article] [PubMed]
    [Google Scholar]
  51. Keymer DP, Boehm AB. Recombination shapes the structure of an environmental Vibrio cholerae population. Appl Environ Microbiol 2011; 77:537–544 [View Article] [PubMed]
    [Google Scholar]
  52. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 2015; 1:vev003 [View Article] [PubMed]
    [Google Scholar]
  53. Shimodaira H, Hasegawa M. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 2001; 17:1246–1247 [View Article] [PubMed]
    [Google Scholar]
  54. Smith JM, Smith NH, O’Rourke M, Spratt BG. How clonal are bacteria?. Proc Natl Acad Sci 1993; 90:4384–4388 [View Article] [PubMed]
    [Google Scholar]
  55. Posada D, Crandall KA, Holmes EC. Recombination in evolutionary genomics. Annu Rev Genet 2002; 36:75–97 [View Article] [PubMed]
    [Google Scholar]
  56. Galtier N, Daubin V. Dealing with incongruence in phylogenomic analyses. Phil Trans R Soc B 2008; 363:4023–4029 [View Article]
    [Google Scholar]
  57. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res 2018; 3:124 [View Article] [PubMed]
    [Google Scholar]
  58. Bratcher HB, Corton C, Jolley KA, Parkhill J, Maiden MCJ. 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]
  59. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  60. Silva M, Machado MP, Silva DN, Rossi M, Moran-Gilad J et al. chewBBACA: a complete suite for gene-by-gene schema creation and strain identification. Microb Genom 2018; 4:e000166 [View Article] [PubMed]
    [Google Scholar]
  61. Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11:119 [View Article] [PubMed]
    [Google Scholar]
  62. Harrison OB, Clemence M, Dillard JP, Tang CM, Trees D et al. Genomic analyses of Neisseria gonorrhoeae reveal an association of the gonococcal genetic island with antimicrobial resistance. J Infect 2016; 73:578–587 [View Article] [PubMed]
    [Google Scholar]
  63. Unemo M, Golparian D, Sánchez-Busó L, Grad Y, Jacobsson S et al. The novel 2016 WHO Neisseria gonorrhoeae reference strains for global quality assurance of laboratory investigations: phenotypic, genetic and reference genome characterization. J Antimicrob Chemother 2016; 71:3096–3108 [View Article] [PubMed]
    [Google Scholar]
  64. Zhou Z, Alikhan N-F, Sergeant MJ, Luhmann N, Vaz C et al. GrapeTree: visualization of core genomic relationships among 100,000 bacterial pathogens. Genome Res 2018; 28:1395–1404 [View Article] [PubMed]
    [Google Scholar]
  65. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
    [Google Scholar]
  66. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
    [Google Scholar]
  67. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
    [Google Scholar]
  68. Sandström EG, Knapp JS, Reller LB, Thompson SE, Hook EW et al. Serogrouping of Neisseria gonorrhoeae: correlation of serogroup with disseminated gonococcal infection. Sex Transm Dis 1984; 11:77–80 [View Article] [PubMed]
    [Google Scholar]
  69. Demczuk W, Sidhu S, Unemo M, Whiley DM, Allen VG et al. Neisseria gonorrhoeae sequence typing for antimicrobial resistance, a novel antimicrobial resistance multilocus typing scheme for tracking global dissemination of N. gonorrhoeae strains. J Clin Microbiol 2017; 55:1454–1468 [View Article] [PubMed]
    [Google Scholar]
  70. Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M et al. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 2020; 48:D517–D525 [View Article] [PubMed]
    [Google Scholar]
  71. Boni MF, Posada D, Feldman MW. An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 2007; 176:1035–1047 [View Article] [PubMed]
    [Google Scholar]
  72. Gibbs MJ, Armstrong JS, Gibbs AJ. Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 2000; 16:573–582 [View Article] [PubMed]
    [Google Scholar]
  73. Graham J, McNeney B, Seillier-Moiseiwitsch F. Stepwise detection of recombination breakpoints in sequence alignments. Bioinformatics 2005; 21:589–595 [View Article] [PubMed]
    [Google Scholar]
  74. Martin D, Rybicki E. RDP: detection of recombination amongst aligned sequences. Bioinformatics 2000; 16:562–563 [View Article] [PubMed]
    [Google Scholar]
  75. Sawyer S. Statistical tests for detecting gene conversion. Mol Biol Evol 1989; 6:526–538 [View Article] [PubMed]
    [Google Scholar]
  76. Salminen MO, Carr JK, Burke DS, McCutchan FE. Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res Hum Retroviruses 1995; 11:1423–1425 [View Article]
    [Google Scholar]
  77. Nokchan N, Wongsurawat T, Jenjaroenpun P, Nitayanon P, Tribuddharat C. Whole-genome sequence analysis of high-level penicillin-resistant strains and antimicrobial susceptibility of Neisseria gonorrhoeae clinical isolates from Thailand. PLoS One 2022; 17:e0271657 [View Article] [PubMed]
    [Google Scholar]
  78. Morse SA, Johnson SR, Biddle JW, Roberts MC. High-level tetracycline resistance in Neisseria gonorrhoeae is result of acquisition of streptococcal tetM determinant. Antimicrob Agents Chemother 1986; 30:664–670 [View Article]
    [Google Scholar]
  79. Ng L-K, Martin I, Lau A. National Gonococcal Surveillance Program Members Trends of chromosomally mediated antimicrobial resistance in Neisseria gonorrhoeae in Canada: 1994-1999. Sex Transm Dis 2003; 30:896–900 [View Article] [PubMed]
    [Google Scholar]
  80. Cooke SJ, de la Paz H, La Poh C, Ison CA, Heckels JE. Variation within serovars of Neisseria gonorrhoeae detected by structural analysis of outer-membrane protein PIB and by pulsed-field gel electrophoresis. Microbiology 1997; 143 (Pt 4):1415–1422 [View Article] [PubMed]
    [Google Scholar]
  81. Hu M, Nandi S, Davies C, Nicholas RA. High-level chromosomally mediated tetracycline resistance in Neisseria gonorrhoeae results from a point mutation in the rpsJ gene encoding ribosomal protein S10 in combination with the mtrR and penB resistance determinants. Antimicrob Agents Chemother 2005; 49:4327–4334 [View Article] [PubMed]
    [Google Scholar]
  82. Ison CA, Tekki N, Gill MJ. Detection of the tetM determinant in Neisseria gonorrhoeae. Sex Transm Dis 1993; 20:329–333 [PubMed]
    [Google Scholar]
  83. Sun A, Fan X, Gu Y, Du P, Tang R et al. Predominant porB1A and porB1B genotypes and correlation of gene mutations with drug resistance in Neisseria gonorrhoeae isolates in Eastern China. BMC Infect Dis 2010; 10:323 [View Article] [PubMed]
    [Google Scholar]
  84. Al Suwayyid BA, Coombs GW, Speers DJ, Pearson J, Wise MJ et al. Genomic epidemiology and population structure of Neisseria gonorrhoeae from remote highly endemic Western Australian populations. BMC Genomics 2018; 19:165 [View Article] [PubMed]
    [Google Scholar]
  85. Ezewudo MN, Joseph SJ, Castillo-Ramirez S, Dean D, Del Rio C et al. Population structure of Neisseria gonorrhoeae based on whole genome data and its relationship with antibiotic resistance. PeerJ 2015; 3:e806 [View Article] [PubMed]
    [Google Scholar]
  86. Lee RS, Seemann T, Heffernan H, Kwong JC, Gonçalves da Silva A et al. Genomic epidemiology and antimicrobial resistance of Neisseria gonorrhoeae in New Zealand. J Antimicrob Chemother 2018; 73:353–364 [View Article] [PubMed]
    [Google Scholar]
  87. Sánchez-Busó L, Golparian D, Corander J, Grad YH, Ohnishi M et al. The impact of antimicrobials on gonococcal evolution. Nat Microbiol 2019; 4:1941–1950 [View Article] [PubMed]
    [Google Scholar]
  88. Kenyon C, Laumen J, Manoharan-Basil S. Choosing new therapies for gonorrhoea: we need to consider the impact on the pan-Neisseria genome. A viewpoint. Antibiotics 2021; 10:515 [View Article]
    [Google Scholar]
  89. Edwards JL, Jennings MP, Apicella MA, Seib KL. Is gonococcal disease preventable? The importance of understanding immunity and pathogenesis in vaccine development. Crit Rev Microbiol 2016; 42:928–941 [View Article] [PubMed]
    [Google Scholar]
  90. Gottlieb SL, Johnston C. Future prospects for new vaccines against sexually transmitted infections. Curr Opin Infect Dis 2017; 30:77–86 [View Article] [PubMed]
    [Google Scholar]
  91. Jerse AE, Deal CD. Vaccine research for gonococcal infections: where are we?. Sex Transm Infect 2013; 89 Suppl 4:iv63–8 [View Article] [PubMed]
    [Google Scholar]
  92. Tramont EC. Gonococcal vaccines. Clin Microbiol Rev 1989; 2 Suppl:S74–7 [View Article] [PubMed]
    [Google Scholar]
  93. Zhu W, Chen C-J, Thomas CE, Anderson JE, Jerse AE et al. Vaccines for gonorrhea: can we rise to the challenge?. Front Microbiol 2011; 2:124 [View Article] [PubMed]
    [Google Scholar]
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