1932

Abstract

and are closely related organisms that cause the sexually transmitted infection gonorrhea and serious bacterial meningitis and septicemia, respectively. Both species possess multiple mechanisms to alter the expression of surface-exposed proteins through the processes of phase and antigenic variation. This potential for wide variability in surface-exposed structures allows the organisms to always have subpopulations of divergent antigenic types to avoid immune surveillance and to contribute to functional variation. Additionally, the are naturally competent for DNA transformation, which is their main means of genetic exchange. Although bacteriophages and plasmids are present in this genus, they are not as effective as DNA transformation for horizontal genetic exchange. There are barriers to genetic transfer, such as restriction-modification systems and CRISPR loci, that limit particular types of exchange. These host-restricted pathogens illustrate the rich complexity of genetics that can help define the similarities and differences of closely related organisms.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-120213-092007
2014-11-23
2024-06-24
Loading full text...

Full text loading...

/deliver/fulltext/genet/48/1/annurev-genet-120213-092007.html?itemId=/content/journals/10.1146/annurev-genet-120213-092007&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Deleted in proof.
  2. Aho EL, Botten JW, Hall RJ, Larson MK, Ness JK. 2.  1997. Characterization of a class II pilin expression locus from Neisseria meningitidis: evidence for increased diversity among pilin genes in pathogenic Neisseria species. Infect. Immunity 65:2613–20 [Google Scholar]
  3. Aho EL, Dempsey JA, Hobbs MM, Klapper DG, Cannon JG. 3.  1991. Characterization of the opa (class 5) gene family of Neisseria meningitidis. Mol. Microbiol. 5:1429–37 [Google Scholar]
  4. Aho EL, Keating AM, McGillivray SM. 4.  2000. A comparative analysis of pilin genes from pathogenic and nonpathogenic Neisseria species. Microb. Pathog. 28:81–88 [Google Scholar]
  5. Allen VG, Mitterni L, Seah C, Rebbapragada A, Martin IE. 5.  et al. 2013. Neisseria gonorrhoeae treatment failure and susceptibility to cefixime in Toronto, Canada. J. Am. Med. Assoc. 309:163–70 [Google Scholar]
  6. Ambur OH, Frye SA, Nilsen M, Hovland E, Tonjum T. 5a.  2012. Restriction and sequence alterations affect DNA uptake sequence-dependent transformation in Neisseria meningitidis. PLOS ONE 7:e39742 [Google Scholar]
  7. Ambur OH, Frye SA, Tonjum T. 6.  2007. New functional identity for the DNA uptake sequence in transformation and its presence in transcriptional terminators. J. Bacteriol. 189:2077–85 [Google Scholar]
  8. Baehr W, Gotschlich EC, Hitchcock PJ. 7.  1989. The virulence-associated gonococcal H.8 gene encodes 14 tandemly repeated pentapeptides. Mol. Microbiol. 3:49–55 [Google Scholar]
  9. Ball LM, Criss AK. 8.  2013. Constitutively Opa-expressing and Opa-deficient Neisseria gonorrhoeae strains differentially stimulate and survive exposure to human neutrophils. J. Bacteriol. 195:2982–90 [Google Scholar]
  10. Banerjee A, Wang R, Supernavage SL, Ghosh SK, Parker J. 9.  et al. 2002. Implications of phase variation of a gene (pgtA) encoding a pilin galactosyl transferase in gonococcal pathogenesis. J. Exp. Med. 196:147–62 [Google Scholar]
  11. Bayliss CD, Hoe JC, Makepeace K, Martin P, Hood DW, Moxon ER. 10.  2008. Neisseria meningitidis escape from the bactericidal activity of a monoclonal antibody is mediated by phase variation of lgtG and enhanced by a mutator phenotype. Infect. Immunity 76:5038–48 [Google Scholar]
  12. Belland RJ, Morrison SG, Carlson JH, Hogan DM. 11.  1997. Promoter strength influences phase variation of neisserial opa genes. Mol. Microbiol. 23:123–35 [Google Scholar]
  13. Bentley SD, Vernikos GS, Snyder LA, Churcher C, Arrowsmith C. 12.  et al. 2007. Meningococcal genetic variation mechanisms viewed through comparative analysis of serogroup C strain FAM18. PLOS Genet. 3:e23 [Google Scholar]
  14. Berry JL, Cehovin A, McDowell MA, Lea SM, Pelicic V. 13.  2013. Functional analysis of the interdependence between DNA uptake sequence and its cognate ComP receptor during natural transformation in Neisseria species. PLOS Genet. 9:e1004014 [Google Scholar]
  15. Bhat KS, Gibbs CP, Barrera O, Morrison SG, Jahnig F. 14.  et al. 1991. The opacity proteins of Neisseria gonorrhoeae strain MS11 are encoded by a family of 11 complete genes. Mol. Microbiol. 5:1889–901 [Google Scholar]
  16. Bille E, Ure R, Gray SJ, Kaczmarski EB, McCarthy ND. 15.  et al. 2008. Association of a bacteriophage with meningococcal disease in young adults. PLOS ONE 3:e3885 [Google Scholar]
  17. Bille E, Zahar JR, Perrin A, Morelle S, Kriz P. 16.  et al. 2005. A chromosomally integrated bacteriophage in invasive meningococci. J. Exp. Med. 201:1905–13 [Google Scholar]
  18. Biswas GD, Sox T, Blackman E, Sparling PF. 17.  1977. Factors affecting genetic transformation of Neisseria gonorrhoeae. J. Bacteriol. 129:983–92 [Google Scholar]
  19. Biswas GD, Sparling PF. 18.  1981. Entry of double-stranded deoxyribonucleic acid during transformation of Neisseria gonorrhoeae. J. Bacteriol. 145:638–40 [Google Scholar]
  20. Boyle-Vavra S, Seifert HS. 19.  1996. Uptake-sequence-independent DNA transformation exists in Neisseria gonorrhoeae. Microbiology 142:Pt. 102839–45 [Google Scholar]
  21. Budroni S, Siena E, Dunning Hotopp JC, Seib KL, Serruto D. 20.  et al. 2011. Neisseria meningitidis is structured in clades associated with restriction modification systems that modulate homologous recombination. Proc. Natl. Acad. Sci. USA 108:4494–99 [Google Scholar]
  22. Buisine N, Tang CM, Chalmers R. 21.  2002. Transposon-like Correia elements: structure, distribution and genetic exchange between pathogenic Neisseria sp. FEBS Lett. 522:52–58 [Google Scholar]
  23. Cahoon LA, Seifert HS. 22.  2009. An alternative DNA structure is necessary for pilin antigenic variation in Neisseria gonorrhoeae. Science 325:764–67 [Google Scholar]
  24. Cahoon LA, Seifert HS. 23.  2013. Transcription of a cis-acting, noncoding, small RNA is required for pilin antigenic variation in Neisseria gonorrhoeae. PLOS Pathogens 9:e1003074 [Google Scholar]
  25. Campbell LA, Short HB, Young FE, Clark VL. 24.  1985. Autoplaquing in Neisseria gonorrhoeae. J. Bacteriol. 164:461–65 [Google Scholar]
  26. Carson SD, Stone B, Beucher M, Fu J, Sparling PF. 25.  2000. Phase variation of the gonococcal siderophore receptor FetA. Mol. Microbiol. 36:585–93 [Google Scholar]
  27. Cary SG, Hunter DH. 26.  1967. Isolation of bacteriophages active against Neisseria meningitidis. J. Virol. 1:538–42 [Google Scholar]
  28. 27. CDC 2013. Sexually Transmitted Disease Surveillance 2012. Atlanta, GA: CDC [Google Scholar]
  29. Cehovin A, Simpson PJ, McDowell MA, Brown DR, Noschese R. 28.  et al. 2013. Specific DNA recognition mediated by a type IV pilin. Proc. Natl. Acad. Sci. USA 110:3065–70 [Google Scholar]
  30. Chaussee MS, Hill SA. 29.  1998. Formation of single-stranded DNA during DNA transformation of Neisseria gonorrhoeae. J. Bacteriol. 180:5117–22 [Google Scholar]
  31. Cheng Y, Johnson MD, Burillo-Kirch C, Mocny JC, Anderson JE. 30.  et al. 2013. Mutation of the conserved calcium-binding motif in Neisseria gonorrhoeae PilC1 impacts adhesion but not piliation. Infect. Immunity 81:4280–89 [Google Scholar]
  32. Claus H, Maiden MC, Wilson DJ, McCarthy ND, Jolley KA. 31.  et al. 2005. Genetic analysis of meningococci carried by children and young adults. J. Infect. Dis. 191:1263–71 [Google Scholar]
  33. Cole JG, Fulcher NB, Jerse AE. 32.  2010. Opacity proteins increase Neisseria gonorrhoeae fitness in the female genital tract due to a factor under ovarian control. Infect. Immunity 78:1629–41 [Google Scholar]
  34. Correia FF, Inouye S, Inouye M. 33.  1986. A 26-base-pair repetitive sequence specific for Neisseria gonorrhoeae and Neisseria meningitidis genomic DNA. J. Bacteriol. 167:1009–15 [Google Scholar]
  35. Correia FF, Inouye S, Inouye M. 34.  1988. A family of small repeated elements with some transposon-like properties in the genome of Neisseria gonorrhoeae. J. Biol. Chem. 263:12194–98 [Google Scholar]
  36. Criss AK, Kline KA, Seifert HS. 35.  2005. The frequency and rate of pilin antigenic variation in Neisseria gonorrhoeae. Mol. Microbiol. 58:510–19 [Google Scholar]
  37. Criss AK, Seifert HS. 36.  2012. A bacterial siren song: intimate interactions between Neisseria and neutrophils. Nat. Rev. Microbiol. 10:178–90 [Google Scholar]
  38. Daly MJ, Minton KW. 37.  1995. Interchromosomal recombination in the extremely radioresistant bacterium Deinococcus radiodurans. J. Bacteriol. 177:5495–505 [Google Scholar]
  39. Daou N, Yu C, McClure R, Gudino C, Reed GW, Genco CA. 38.  2013. Neisseria prophage repressor implicated in gonococcal pathogenesis. Infect. Immunity 81:3652–61 [Google Scholar]
  40. Davidsen T, Rodland EA, Lagesen K, Seeberg E, Rognes T, Tonjum T. 39.  2004. Biased distribution of DNA uptake sequences towards genome maintenance genes. Nucleic Acids Res. 32:1050–58 [Google Scholar]
  41. Davies JK, Harrison PF, Lin YH, Bartley S, Khoo CA. 40.  et al. 2014. The use of high-throughput DNA sequencing in the investigation of antigenic variation: application to Neisseria species. PLOS ONE 9:e86704 [Google Scholar]
  42. De Bolle X, Bayliss CD, Field D, van de Ven T, Saunders NJ. 41.  et al. 2000. The length of a tetranucleotide repeat tract in Haemophilus influenzae determines the phase variation rate of a gene with homology to type III DNA methyltransferases. Mol. Microbiol. 35:211–22 [Google Scholar]
  43. De Gregorio E, Abrescia C, Carlomagno MS, Di Nocera PP. 42.  2003. Asymmetrical distribution of Neisseria miniature insertion sequence DNA repeats among pathogenic and nonpathogenic Neisseria strains. Infect. Immunity 71:4217–21 [Google Scholar]
  44. Dempsey JA, Litaker W, Madhure A, Snodgrass TL, Cannon JG. 43.  1991. Physical map of the chromosome of Neisseria gonorrhoeae FA1090 with locations of genetic markers, including opa and pil genes. J. Bacteriol. 173:5476–86 [Google Scholar]
  45. Dillard JP. 44.  2011. Genetic manipulation of Neisseria gonorrhoeae. Curr. Protoc. Microbiol. doi: 10.1002/9780471729259.mc04a02s00 [Google Scholar]
  46. Dillard JP, Seifert HS. 45.  2001. A variable genetic island specific for Neisseria gonorrhoeae is involved in providing DNA for natural transformation and is found more often in disseminated infection isolates. Mol. Microbiol. 41:263–77 [Google Scholar]
  47. Dominguez NM, Hackett KT, Dillard JP. 46.  2011. XerCD-mediated site-specific recombination leads to loss of the 57-kilobase gonococcal genetic island. J. Bacteriol. 193:377–88 [Google Scholar]
  48. Duffin PM, Seifert HS. 47.  2010. DNA uptake sequence-mediated enhancement of transformation in Neisseria gonorrhoeae is strain dependent. J. Bacteriol. 192:4436–44 [Google Scholar]
  49. Dunning Hotopp JC, Grifantini R, Kumar N, Tzeng YL, Fouts D. 48.  et al. 2006. Comparative genomics of Neisseria meningitidis: core genome, islands of horizontal transfer and pathogen-specific genes. Microbiology 52:3733–-49 [Google Scholar]
  50. Eisenstein BI, Sox T, Biswas G, Blackman E, Sparling PF. 49.  1977. Conjugal transfer of the gonococcal penicillinase plasmid. Science 195:998–1000 [Google Scholar]
  51. Evans CM, Pratt CB, Matheson M, Vaughan TE, Findlow J. 50.  et al. 2011. Nasopharyngeal colonization by Neisseria lactamica and induction of protective immunity against Neisseria meningitidis. Clin. Infect. Dis. 52:70–77 [Google Scholar]
  52. Facinelli B, Varaldo PE. 51.  1987. Plasmid-mediated sulfonamide resistance in Neisseria meningitidis. Antimicrob. Agents Chemother. 31:1642–43 [Google Scholar]
  53. Forest KT, Bernstein SL, Getzoff ED, So M, Tribbick G. 52.  et al. 1996. Assembly and antigenicity of the Neisseria gonorrhoeae pilus mapped with antibodies. Infect. Immun. 64:644–52 [Google Scholar]
  54. Francis F, Ramirez-Arcos S, Salimnia H, Victor C, Dillon JR. 53.  2000. Organization and transcription of the division cell wall (dcw) cluster in Neisseria gonorrhoeae. Gene 251:141–51 [Google Scholar]
  55. Frye SA, Nilsen M, Tonjum T, Ambur OH. 54.  2013. Dialects of the DNA uptake sequence in Neisseriaceae. PLOS Genet. 9:e1003458 [Google Scholar]
  56. Gangel H, Hepp C, Muller S, Oldewurtel ER, Aas FE. 54a.  et al. 2014. Concerted spatio-temporal dynamics of imported DNA and ComE DNA uptake protein during gonococcal transformation. PLoS Pathog. 10:e1004043 [Google Scholar]
  57. Gold R, Goldschneider I, Lepow ML, Draper TF, Randolph M. 55.  1978. Carriage of Neisseria meningitidis and Neisseria lactamica in infants and children. J. Infect. Dis. 137:112–21 [Google Scholar]
  58. Goodman SD, Scocca JJ. 56.  1988. Identification and arrangement of the DNA sequence recognized in specific transformation of Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. USA 85:6982–86 [Google Scholar]
  59. Graves JF, Biswas GD, Sparling PF. 57.  1982. Sequence-specific DNA uptake in transformation of Neisseria gonorrhoeae. J. Bacteriol. 152:1071–77 [Google Scholar]
  60. Grissa I, Vergnaud G, Pourcel C. 58.  2007. The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinform. 8:172 [Google Scholar]
  61. Haas R, Meyer TF. 59.  1986. The repertoire of silent pilus genes in Neisseria gonorrhoeae: evidence for gene conversion. Cell 44:107–15 [Google Scholar]
  62. Haber JE. 60.  1998. Mating-type gene switching in Saccharomyces cerevisiae. Annu. Rev. Genet. 32:561–99 [Google Scholar]
  63. Hall LM, Henderson-Begg SK. 61.  2006. Hypermutable bacteria isolated from humans: a critical analysis. Microbiology 152:2505–14 [Google Scholar]
  64. Hamilton HL, Dillard JP. 62.  2006. Natural transformation of Neisseria gonorrhoeae: from DNA donation to homologous recombination. Mol. Microbiol. 59:376–85 [Google Scholar]
  65. Hamilton HL, Dominguez NM, Schwartz KJ, Hackett KT, Dillard JP. 63.  2005. Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol. Microbiol. 55:1704–21 [Google Scholar]
  66. Hamilton HL, Schwartz KJ, Dillard JP. 64.  2001. Insertion-duplication mutagenesis of Neisseria: use in characterization of DNA transfer genes in the gonococcal genetic island. J. Bacteriol. 183:4718–26 [Google Scholar]
  67. Hammerschmidt S, Muller A, Sillmann H, Muhlenhoff M, Borrow R. 65.  et al. 1996. Capsule phase variation in Neisseria meningitidis serogroup B by slipped-strand mispairing in the polysialyltransferase gene (siaD): correlation with bacterial invasion and the outbreak of meningococcal disease. Mol. Microbiol. 20:1211–20 [Google Scholar]
  68. Hamrick TS, Dempsey JA, Cohen MS, Cannon JG. 66.  2001. Antigenic variation of gonococcal pilin expression in vivo: analysis of the strain FA1090 pilin repertoire and identification of the pilS gene copies recombining with pilE during experimental human infection. Microbiology 147:839–49 [Google Scholar]
  69. Harrison LH, Trotter CL, Ramsay ME. 67.  2009. Global epidemiology of meningococcal disease. Vaccine 27:Suppl. 2B51–63 [Google Scholar]
  70. Haubold B, Travisano M, Rainey PB, Hudson RR. 68.  1998. Detecting linkage disequilibrium in bacterial populations. Genetics 150:1341–48 [Google Scholar]
  71. Helm RA, Seifert HS. 69.  2010. Frequency and rate of pilin antigenic variation of Neisseria meningitidis. J. Bacteriol. 192:3822–23 [Google Scholar]
  72. Hill SA, Davies JK. 70.  2009. Pilin gene variation in Neisseria gonorrhoeae: reassessing the old paradigms. FEMS Microbiol. Rev. 33:521–30 [Google Scholar]
  73. Hill SA, Grant CC. 71.  2002. Recombinational error and deletion formation in Neisseria gonorrhoeae: a role for RecJ in the production of pilE (L) deletions. Mol. Genet. Genomics 266:962–72 [Google Scholar]
  74. Horrocks P, Pinches R, Christodoulou Z, Kyes SA, Newbold CI. 72.  2004. Variable var transition rates underlie antigenic variation in malaria. Proc. Natl. Acad. Sci. USA 101:11129–34 [Google Scholar]
  75. Hou Z, Zhang Y, Propson NE, Howden SE, Chu LF. 73.  et al. 2013. Efficient genome engineering in human pluripotent stem cells using Cas9 from Neisseria meningitidis. Proc. Natl. Acad. Sci. USA 110:15644–49 [Google Scholar]
  76. Howell-Adams B, Seifert HS. 74.  2000. Molecular models accounting for the gene conversion reactions mediating gonococcal pilin antigenic variation. Mol. Microbiol. 37:1146–58 [Google Scholar]
  77. Howell-Adams B, Wainwright LA, Seifert HS. 75.  1996. The size and position of heterologous insertions in a silent locus differentially affect pilin recombination in Neisseria gonorrhoeae. Mol. Microbiol. 22:509–22 [Google Scholar]
  78. Ison CA, Bellinger CM, Walker J. 76.  1986. Homology of cryptic plasmid of Neisseria gonorrhoeae with plasmids from Neisseria meningitidis and Neisseria lactamica. J. Clin. Pathol. 39:1119–23 [Google Scholar]
  79. Jain S, Zweig M, Peeters E, Siewering K, Hackett KT. 77.  et al. 2012. Characterization of the single stranded DNA binding protein SsbB encoded in the gonoccocal genetic island. PLOS ONE 7:e35285 [Google Scholar]
  80. Jansen R, Embden JD, Gaastra W, Schouls LM. 78.  2002. Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43:1565–75 [Google Scholar]
  81. Jennings MP, Srikhanta YN, Moxon ER, Kramer M, Poolman JT. 79.  et al. 1999. The genetic basis of the phase variation repertoire of lipopolysaccharide immunotypes in Neisseria meningitidis. Microbiology 145:Pt. 113013–21 [Google Scholar]
  82. Jennings MP, Virji M, Evans D, Foster V, Srikhanta YN. 80.  et al. 1998. Identification of a novel gene involved in pilin glycosylation in Neisseria meningitidis. Mol. Microbiol. 29:975–84 [Google Scholar]
  83. Jolley KA, Sun L, Moxon ER, Maiden MC. 81.  2004. Dam inactivation in Neisseria meningitidis: prevalence among diverse hyperinvasive lineages. BMC Microbiol. 4:34 [Google Scholar]
  84. Jonsson AB, Nyberg G, Normark S. 82.  1991. Phase variation of gonococcal pili by frameshift mutation in pilC, a novel gene for pilus assembly. EMBO J. 10:477–88 [Google Scholar]
  85. Jordan P, Snyder LA, Saunders NJ. 83.  2003. Diversity in coding tandem repeats in related Neisseria spp. BMC Microbiol. 3:23 [Google Scholar]
  86. Jordan PW, Snyder LA, Saunders NJ. 84.  2005. Strain-specific differences in Neisseria gonorrhoeae associated with the phase variable gene repertoire. BMC Microbiol. 5:21 [Google Scholar]
  87. Kawai M, Uchiyama I, Kobayashi I. 85.  2006. Genome comparison in silico in Neisseria suggests integration of filamentous bacteriophages by their own transposase. DNA Res. 12:389–401 [Google Scholar]
  88. Kellogg DS Jr, Peacock WL Jr, Deacon WE, Brown L, Pirkle DI. 86.  1963. Neisseria gonorrhoeae. I. Virulence genetically linked to clonal variation. J. Bacteriol. 85:1274–79 [Google Scholar]
  89. Kline KA, Criss AK, Wallace A, Seifert HS. 87.  2007. Transposon mutagenesis identifies sites upstream of the Neisseria gonorrhoeae pilE gene that modulate pilin antigenic variation. J. Bacteriol. 189:3462–70 [Google Scholar]
  90. Kline KA, Sechman EV, Skaar EP, Seifert HS. 88.  2003. Recombination, repair and replication in the pathogenic Neisseriae: the 3 R's of molecular genetics of two human-specific bacterial pathogens. Mol. Microbiol. 50:3–13 [Google Scholar]
  91. Kobayashi I. 89.  2001. Behavior of restriction-modification systems as selfish mobile elements and their impact on genome evolution. Nucleic Acids Res. 29:3742–56 [Google Scholar]
  92. Koomey M, Gotschlich EC, Robbins K, Bergstrom S, Swanson J. 90.  1987. Effects of recA mutations on pilus antigenic variation and phase transitions in Neisseria gonorrhoeae. Genetics 117:391–98 [Google Scholar]
  93. Korch C, Hagblom P, Ohman H, Goransson M, Normark S. 91.  1985. Cryptic plasmid of Neisseria gonorrhoeae: complete nucleotide sequence and genetic organization. J. Bacteriol. 163:430–38 [Google Scholar]
  94. Kuzminov A. 91a.  1999. Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol. Mol. Biol. Rev. 63:751–813 [Google Scholar]
  95. Kupsch EM, Aubel D, Gibbs CP, Kahrs AF, Rudel T, Meyer TF. 92.  1996. Construction of Hermes shuttle vectors: a versatile system useful for genetic complementation of transformable and non-transformable Neisseria mutants. Mol. Gen. Genet. 250:558–69 [Google Scholar]
  96. Kupsch EM, Knepper B, Kuroki T, Heuer I, Meyer TF. 93.  1993. Variable opacity (Opa) outer membrane proteins account for the cell tropisms displayed by Neisseria gonorrhoeae for human leukocytes and epithelial cells. EMBO J. 12:641–50 [Google Scholar]
  97. 94. Lahra MM, WHO West. Pac. South East Asian Gonococcal Antimicrob. Surveill. Programme 2012. Surveillance of antibiotic resistance in Neisseria gonorrhoeae in the WHO Western Pacific and South East Asian Regions, 2010. Commun. Dis. Intell. Q. Rep. 36:95–100 [Google Scholar]
  98. LeVan A, Zimmerman LI, Mahle AC, Swanson KV, DeShong P. 95.  et al. 2012. Construction and characterization of a derivative of Neisseria gonorrhoeae strain MS11 devoid of all opa genes. J. Bacteriol. 194:6468–78 [Google Scholar]
  99. Levinson G, Gutman GA. 96.  1987. High frequencies of short frameshifts in poly-CA/TG tandem repeats borne by bacteriophage M13 in Escherichia coli K-12. Nucleic Acids Res. 15:5323–38 [Google Scholar]
  100. Levinson G, Gutman GA. 97.  1987. Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol. Biol. Evol. 4:203–21 [Google Scholar]
  101. Lin YH, Ryan CS, Davies JK. 98.  2011. Neisserial Correia repeat-enclosed elements do not influence the transcription of pil genes in Neisseria gonorrhoeae and Neisseria meningitidis. J. Bacteriol. 193:5728–36 [Google Scholar]
  102. Liu SV, Saunders NJ, Jeffries A, Rest RF. 99.  2002. Genome analysis and strain comparison of Correia repeats and Correia repeat-enclosed elements in pathogenic Neisseria. J. Bacteriol. 184:6163–73 [Google Scholar]
  103. Loenen WA, Dryden DT, Raleigh EA, Wilson GG, Murray NE. 100.  2014. Highlights of the DNA cutters: a short history of the restriction enzymes. Nucleic Acids Res. 42:3–19 [Google Scholar]
  104. Marri PR, Paniscus M, Weyand NJ, Rendon MA, Calton CM. 101.  et al. 2010. Genome sequencing reveals widespread virulence gene exchange among human Neisseria species. PLOS ONE 5:e11835 [Google Scholar]
  105. Martin P, Makepeace K, Hill SA, Hood DW, Moxon ER. 102.  2005. Microsatellite instability regulates transcription factor binding and gene expression. Proc. Natl. Acad. Sci. USA 102:3800–4 [Google Scholar]
  106. Martin P, Sun L, Hood DW, Moxon ER. 103.  2004. Involvement of genes of genome maintenance in the regulation of phase variation frequencies in Neisseria meningitidis. Microbiology 150:3001–12 [Google Scholar]
  107. Masignani V, Giuliani MM, Tettelin H, Comanducci M, Rappuoli R, Scarlato V. 104.  2001. Mu-like prophage in serogroup B Neisseria meningitidis coding for surface-exposed antigens. Infect. Immun. 69:2580–88 [Google Scholar]
  108. Mayer LW. 105.  1982. Rates in vitro changes of gonococcal colony opacity phenotypes. Infect. Immun. 37:481–85 [Google Scholar]
  109. Mazzone M, De Gregorio E, Lavitola A, Pagliarulo C, Alifano P, Di Nocera PP. 106.  2001. Whole-genome organization and functional properties of miniature DNA insertion sequences conserved in pathogenic Neisseriae. Gene 278:211–22 [Google Scholar]
  110. Mehr IJ, Seifert HS. 107.  1998. Differential roles of homologous recombination pathways in Neisseria gonorrhoeae pilin antigenic variation, DNA transformation and DNA repair. Mol. Microbiol. 30:697–710 [Google Scholar]
  111. Metruccio MM, Pigozzi E, Roncarati D, Berlanda Scorza F, Norais N. 108.  et al. 2009. A novel phase variation mechanism in the meningococcus driven by a ligand-responsive repressor and differential spacing of distal promoter elements. PLOS Pathogens 5:e1000710 [Google Scholar]
  112. Miller F, Phan G, Brissac T, Bouchiat C, Lioux G. 109.  et al. 2014. The hypervariable region of meningococcal major pilin PilE controls the host cell response via antigenic variation. mBio 5:e01024–13 [Google Scholar]
  113. Mirkin SM. 110.  2007. Expandable DNA repeats and human disease. Nature 447:932–40 [Google Scholar]
  114. Morand PC, Tattevin P, Eugene E, Beretti JL, Nassif X. 111.  2001. The adhesive property of the type IV pilus-associated component PilC1 of pathogenic Neisseria is supported by the conformational structure of the N-terminal part of the molecule. Mol. Microbiol. 40:846–56 [Google Scholar]
  115. Morse SA, Johnson SR, Biddle JW, Roberts MC. 112.  1986. High-level tetracycline resistance in Neisseria gonorrhoeae is result of acquisition of streptococcal tetM determinant. Antimicrob. Agents Chemother. 30:664–70 [Google Scholar]
  116. Moxon R, Bayliss C, Hood D. 113.  2006. Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu. Rev. Genet. 40:307–33 [Google Scholar]
  117. Murphy GL, Connell TD, Barritt DS, Koomey M, Cannon JG. 114.  1989. Phase variation of gonococcal protein II: regulation of gene expression by slipped-strand mispairing of a repetitive DNA sequence. Cell 56:539–47 [Google Scholar]
  118. O'Ryan M, Stoddard J, Toneatto D, Wassil J, Dull PM. 115.  2014. A multi-component meningococcal serogroup B vaccine (4CMenB): the clinical development program. Drugs 74:15–30 [Google Scholar]
  119. Pachulec E, van der Does C. 116.  2010. Conjugative plasmids of Neisseria gonorrhoeae. PLOS ONE 5:e9962 [Google Scholar]
  120. Pagotto FJ, Salimnia H, Totten PA, Dillon JR. 117.  2000. Stable shuttle vectors for Neisseria gonorrhoeae, Haemophilus spp. and other bacteria based on a single origin of replication. Gene 244:13–19 [Google Scholar]
  121. Parker BO, Marinus MG. 118.  1992. Repair of DNA heteroduplexes containing small heterologous sequences in Escherichia coli. Proc. Natl. Acad. Sci. USA 89:1730–34 [Google Scholar]
  122. Parkhill J, Achtman M, James KD, Bentley SD, Churcher C. 119.  et al. 2000. Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491. Nature 404:502–6 [Google Scholar]
  123. Phelps LN. 120.  1967. Isolation and characterization of bacteriophages for Neisseria. J. Gen. Virol. 1:529–36 [Google Scholar]
  124. Piekarowicz A, Klyz A, Majchrzak M, Adamczyk-Poplawska M, Maugel TK, Stein DC. 121.  2007. Characterization of the dsDNA prophage sequences in the genome of Neisseria gonorrhoeae and visualization of productive bacteriophage. BMC Microbiol. 7:66 [Google Scholar]
  125. Piekarowicz A, Klyz A, Majchrzak M, Szczesna E, Piechucki M. 122.  et al. 2014. Neisseria gonorrhoeae filamentous phage Ngoϕ6 is capable of infecting a variety of gram-negative bacteria. J. Virol. 88:1002–10 [Google Scholar]
  126. Piekarowicz A, Majchrzak M, Klyz A, Adamczyk-Poplawska M. 123.  2006. Analysis of the filamentous bacteriophage genomes integrated into Neisseria gonorrhoeae FA1090 chromosome. Pol. J. Microbiol. 55:251–60 [Google Scholar]
  127. Power PM, Roddam LF, Rutter K, Fitzpatrick SZ, Srikhanta YN, Jennings MP. 124.  2003. Genetic characterization of pilin glycosylation and phase variation in Neisseria meningitidis. Mol. Microbiol. 49:833–47 [Google Scholar]
  128. Reynaud CA, Anquez V, Grimal H, Weill JC. 125.  1987. A hyperconversion mechanism generates the chicken light chain preimmune repertoire. Cell 48:379–88 [Google Scholar]
  129. Richardson AR, Stojiljkovic I. 126.  2001. Mismatch repair and the regulation of phase variation in Neisseria meningitidis. Mol. Microbiol. 40:645–55 [Google Scholar]
  130. Richardson AR, Yu Z, Popovic T, Stojiljkovic I. 127.  2002. Mutator clones of Neisseria meningitidis in epidemic serogroup A disease. Proc. Natl. Acad. Sci. USA 99:6103–7 [Google Scholar]
  131. Roberts M, Piot P, Falkow S. 128.  1979. The ecology of gonococcal plasmids. J. Gen. Microbiol. 114:491–94 [Google Scholar]
  132. Roberts MC. 129.  1989. Plasmids of Neisseria gonorrhoeae and other Neisseria species. Clin. Microbiol. Rev. 2:S18–23 [Google Scholar]
  133. Roberts MC, Knapp JS. 130.  1988. Host range of the conjugative 25.2-megadalton tetracycline resistance plasmid from Neisseria gonorrhoeae and related species. Antimicrob. Agents Chemother. 32:488–91 [Google Scholar]
  134. Roberts RJ, Vincze T, Posfai J, Macelis D. 131.  2010. REBASE—a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acids Res. 38:D234–36 [Google Scholar]
  135. Rohrer MS, Lazio MP, Seifert HS. 132.  2005. A real-time semi-quantitative RT-PCR assay demonstrates that the pilE sequence dictates the frequency and characteristics of pilin antigenic variation in Neisseria gonorrhoeae. Nucleic Acids Res. 33:3363–71 [Google Scholar]
  136. Rosenstein NE, Perkins BA, Stephens DS, Popovic T, Hughes JM. 133.  2001. Meningococcal disease. N. Engl. J. Med. 344:1378–88 [Google Scholar]
  137. Sadarangani M, Hoe JC, Callaghan MJ, Jones C, Chan H. 134.  et al. 2012. Construction of Opa-positive and Opa-negative strains of Neisseria meningitidis to evaluate a novel meningococcal vaccine. PLOS ONE 7:e51045 [Google Scholar]
  138. Sadarangani M, Pollard AJ, Gray-Owen SD. 135.  2011. Opa proteins and CEACAMs: pathways of immune engagement for pathogenic Neisseria. FEMS Microbiol. Rev. 35:498–514 [Google Scholar]
  139. Sarkari J, Pandit N, Moxon ER, Achtman M. 136.  1994. Variable expression of the Opc outer membrane protein in Neisseria meningitidis is caused by size variation of a promoter containing poly-cytidine. Mol. Microbiol. 13:207–17 [Google Scholar]
  140. Saunders NJ, Jeffries AC, Peden JF, Hood DW, Tettelin H. 137.  et al. 2000. Repeat-associated phase variable genes in the complete genome sequence of Neisseria meningitidis strain MC58. Mol. Microbiol. 37:207–15 [Google Scholar]
  141. Saunders NJ, Snyder LA. 138.  2002. The minimal mobile element. Microbiology 148:3756–60 [Google Scholar]
  142. Schoen C, Blom J, Claus H, Schramm-Gluck A, Brandt P. 139.  et al. 2008. Whole-genome comparison of disease and carriage strains provides insights into virulence evolution in Neisseria meningitidis. Proc. Natl. Acad. Sci. USA 105:3473–78 [Google Scholar]
  143. Schoen C, Joseph B, Claus H, Vogel U, Frosch M. 140.  2007. Living in a changing environment: insights into host adaptation in Neisseria meningitidis from comparative genomics. Int. J. Med. Microbiol. 297:601–13 [Google Scholar]
  144. Schofield MJ, Hsieh P. 141.  2003. DNA mismatch repair: molecular mechanisms and biological function. Annu. Rev. Microbiol. 57:579–608 [Google Scholar]
  145. Scholten RJ, Kuipers B, Valkenburg HA, Dankert J, Zollinger WD, Poolman JT. 142.  1994. Lipo-oligosaccharide immunotyping of Neisseria meningitidis by a whole-cell ELISA with monoclonal antibodies. J. Med. Microbiol. 41:236–43 [Google Scholar]
  146. Schork S, Schluter A, Blom J, Schneiker-Bekel S, Puhler A. 143.  et al. 2012. Genome sequence of a Neisseria meningitidis capsule null locus strain from the clonal complex of sequence type 198. J. Bacteriol. 194:5144–45 [Google Scholar]
  147. Sechman EV, Kline KA, Seifert HS. 144.  2006. Loss of both Holliday junction processing pathways is synthetically lethal in the presence of gonococcal pilin antigenic variation. Mol. Microbiol. 61:185–93 [Google Scholar]
  148. Sechman EV, Rohrer MS, Seifert HS. 145.  2005. A genetic screen identifies genes and sites involved in pilin antigenic variation in Neisseria gonorrhoeae. Mol. Microbiol. 57:468–83 [Google Scholar]
  149. Seifert HS, Wright CJ, Jerse AE, Cohen MS, Cannon JG. 146.  1994. Multiple gonococcal pilin antigenic variants are produced during experimental human infections. J. Clin. Investig. 93:2744–49 [Google Scholar]
  150. Serkin CD, Seifert HS. 147.  1998. Frequency of pilin antigenic variation in Neisseria gonorrhoeae. J. Bacteriol. 180:1955–58 [Google Scholar]
  151. Serkin CD, Seifert HS. 148.  2000. Iron availability regulates DNA recombination in Neisseria gonorrhoeae. Mol. Microbiol. 37:1075–86 [Google Scholar]
  152. Shafer WM, Rest RF. 149.  1989. Interactions of gonococci with phagocytic cells. Annu. Rev. Microbiol. 43:121–45 [Google Scholar]
  153. Siddique A, Buisine N, Chalmers R. 150.  2011. The transposon-like Correia elements encode numerous strong promoters and provide a potential new mechanism for phase variation in the meningococcus. PLOS Genet. 7:e1001277 [Google Scholar]
  154. Skaar EP, Lazio MP, Seifert HS. 151.  2002. Roles of the recJ and recN genes in homologous recombination and DNA repair pathways of Neisseria gonorrhoeae. J. Bacteriol. 184:919–27 [Google Scholar]
  155. Skaar EP, Lecuyer B, Lenich AG, Lazio MP, Perkins-Balding D. 152.  et al. 2005. Analysis of the Piv recombinase-related gene family of Neisseria gonorrhoeae. J. Bacteriol. 187:1276–86 [Google Scholar]
  156. Smith HO, Gwinn ML, Salzberg SL. 153.  1999. DNA uptake signal sequences in naturally transformable bacteria. Res. Microbiol. 150:603–16 [Google Scholar]
  157. Smith JM, Smith NH, O'Rourke M, Spratt BG. 154.  1993. How clonal are bacteria?. Proc. Natl. Acad. Sci. USA 90:4384–88 [Google Scholar]
  158. Snyder LA, Butcher SA, Saunders NJ. 155.  2001. Comparative whole-genome analyses reveal over 100 putative phase-variable genes in the pathogenic Neisseria spp. Microbiology 147:2321–32 [Google Scholar]
  159. Snyder LA, Cole JA, Pallen MJ. 156.  2009. Comparative analysis of two Neisseria gonorrhoeae genome sequences reveals evidence of mobilization of Correia repeat enclosed elements and their role in regulation. BMC Genomics 10:70 [Google Scholar]
  160. Snyder LA, Jarvis SA, Saunders NJ. 157.  2005. Complete and variant forms of the “gonococcal genetic island” in Neisseria meningitidis. Microbiology 151:4005–13 [Google Scholar]
  161. Snyder LA, McGowan S, Rogers M, Duro E, O'Farrell E, Saunders NJ. 158.  2007. The repertoire of minimal mobile elements in the Neisseria species and evidence that these are involved in horizontal gene transfer in other bacteria. Mol. Biol. Evol. 24:2802–15 [Google Scholar]
  162. Snyder LA, Saunders NJ. 159.  2006. The majority of genes in the pathogenic Neisseria species are present in non-pathogenic Neisseria lactamica, including those designated as “virulence genes.”. BMC Genomics 7:128 [Google Scholar]
  163. Snyder LA, Shafer WM, Saunders NJ. 160.  2003. Divergence and transcriptional analysis of the division cell wall (dcw) gene cluster in Neisseria spp. Mol. Microbiol. 47:431–42 [Google Scholar]
  164. Solomon JM, Grossman AD. 161.  1996. Who's competent and when: regulation of natural genetic competence in bacteria. Trends Genet. 12:150–55 [Google Scholar]
  165. Sparling PF. 162.  1966. Genetic transformation of Neisseria gonorrhoeae to streptomycin resistance. J. Bacteriol. 92:1364–71 [Google Scholar]
  166. Spencer-Smith R, Varkey EM, Fielder MD, Snyder LA. 163.  2012. Sequence features contributing to chromosomal rearrangements in Neisseria gonorrhoeae. PLOS ONE 7:e46023 [Google Scholar]
  167. Srikhanta YN, Dowideit SJ, Edwards JL, Falsetta ML, Wu HJ. 164.  et al. 2009. Phasevarions mediate random switching of gene expression in pathogenic Neisseria. PLOS Pathog. 5:e1000400 [Google Scholar]
  168. Stein DC. 165.  1991. Transformation of Neisseria gonorrhoeae: physical requirements of the transforming DNA. Can. J. Microbiol. 37:345–49 [Google Scholar]
  169. Stein DC, Gregoire S, Piekarowicz A. 166.  1988. Restriction of plasmid DNA during transformation but not conjugation in Neisseria gonorrhoeae. Infect. Immun. 56:112–16 [Google Scholar]
  170. Stein DC, Gunn JS, Radlinska M, Piekarowicz A. 167.  1995. Restriction and modification systems of Neisseria gonorrhoeae. Gene 157:19–22 [Google Scholar]
  171. Stein DC, Silver LE, Clark VL, Young FE. 168.  1983. Construction and characterization of a new shuttle vector, pLES2, capable of functioning in Escherichia coli and Neisseria gonorrhoeae. Gene 25:241–47 [Google Scholar]
  172. Steinberg VI, Hart EJ, Handley J, Goldberg ID. 169.  1976. Isolation and characterization of a bacteriophage specific for Neisseria perflava. J. Clin. Microbiol. 4:87–91 [Google Scholar]
  173. Stephens DS, Greenwood B, Brandtzaeg P. 170.  2007. Epidemic meningitis, meningococcaemia, and Neisseria meningitidis. Lancet 369:2196–210 [Google Scholar]
  174. Stern A, Brown M, Nickel P, Meyer TF. 171.  1986. Opacity genes in Neisseria gonorrhoeae: control of phase and antigenic variation. Cell 47:61–71 [Google Scholar]
  175. Stern A, Keren L, Wurtzel O, Amitai G, Sorek R. 172.  2010. Self-targeting by CRISPR: gene regulation or autoimmunity?. Trends Genet. 26:335–40 [Google Scholar]
  176. Stern A, Meyer TF. 173.  1987. Common mechanism controlling phase and antigenic variation in pathogenic Neisseriae. Mol. Microbiol. 1:5–12 [Google Scholar]
  177. Stohl EA, Seifert HS. 174.  2001. The recX gene potentiates homologous recombination in Neisseria gonorrhoeae. Mol. Microbiol. 40:1301–10 [Google Scholar]
  178. Stone RL, Culbertson CG, Powell HM. 175.  1956. Studies of a bacteriophage active against a chromogenic Neisseria. J. Bacteriol. 71:516–20 [Google Scholar]
  179. Swanson J. 176.  1973. Studies on gonococcus infection. IV. Pili: their role in attachment of gonococci to tissue culture cells. J. Exp. Med. 137:571–89 [Google Scholar]
  180. Swanson J. 177.  1978. Studies on gonococcus infection. XIV. Cell wall protein differences among color/opacity colony variants of Neisseria gonorrhoeae. Infect. Immun. 21:292–302 [Google Scholar]
  181. Swanson J, Bergstrom S, Barrera O, Robbins K, Corwin D. 178.  1985. Pilus− gonococcal variants. Evidence for multiple forms of piliation control. J. Exp. Med. 162:729–44 [Google Scholar]
  182. Swanson J, Bergstrom S, Robbins K, Barrera O, Corwin D, Koomey JM. 179.  1986. Gene conversion involving the pilin structural gene correlates with pilus+ in equilibrium with pilus− changes in Neisseria gonorrhoeae. Cell 47:267–76 [Google Scholar]
  183. Swanson J, Kraus SJ, Gotschlich EC. 180.  1971. Studies on gonococcus infection. I. Pili and zones of adhesion: their relation to gonococcal growth patterns. J. Exp. Med. 134:886–906 [Google Scholar]
  184. Tabrizi SN, Unemo M, Limnios AE, Hogan TR, Hjelmevoll SO. 181.  et al. 2011. Evaluation of six commercial nucleic acid amplification tests for detection of Neisseria gonorrhoeae and other Neisseria species. J. Clin. Microbiol. 49:3610–15 [Google Scholar]
  185. Tauseef I, Ali YM, Bayliss CD. 182.  2013. Phase variation of PorA, a major outer membrane protein, mediates escape of bactericidal antibodies by Neisseria meningitidis. Infect. Immun. 81:1374–80 [Google Scholar]
  186. Tettelin H, Saunders NJ, Heidelberg J, Jeffries AC, Nelson KE. 183.  et al. 2000. Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science 287:1809–15 [Google Scholar]
  187. Thompson SA, Wang LL, West A, Sparling PF. 184.  1993. Neisseria meningitidis produces iron-regulated proteins related to the RTX family of exoproteins. J. Bacteriol. 175:811–18 [Google Scholar]
  188. Tobiason DM, Seifert HS. 185.  2006. The obligate human pathogen, Neisseria gonorrhoeae, is polyploid. PLOS Biol. 4:e185 [Google Scholar]
  189. Tobiason DM, Seifert HS. 186.  2010. Genomic content of Neisseria species. J. Bacteriol. 192:2160–68 [Google Scholar]
  190. Tonjum T, Caugant DA, Dunham SA, Koomey M. 187.  1998. Structure and function of repetitive sequence elements associated with a highly polymorphic domain of the Neisseria meningitidis PilQ protein. Mol. Microbiol. 29:111–24 [Google Scholar]
  191. Trembizki E, Lahra M, Stevens K, Freeman K, Hogan T. 188.  et al. 2014. A national quality assurance survey of Neisseria gonorrhoeae testing. J. Med. Microbiol. 63:45–49 [Google Scholar]
  192. Turner CM, Barry JD. 189.  1989. High frequency of antigenic variation in Trypanosoma brucei rhodesiense infections. Parasitology 99:Pt. 167–75 [Google Scholar]
  193. van der Ende A, Hopman CT, Dankert J. 190.  2000. Multiple mechanisms of phase variation of PorA in Neisseria meningitidis. Infect. Immun. 68:6685–90 [Google Scholar]
  194. van der Ende A, Hopman CT, Zaat S, Essink BB, Berkhout B, Dankert J. 191.  1995. Variable expression of class 1 outer membrane protein in Neisseria meningitidis is caused by variation in the spacing between the −10 and −35 regions of the promoter. J. Bacteriol. 177:2475–80 [Google Scholar]
  195. van Passel MW, Bart A, Luyf AC, van Kampen AH, van der Ende A. 192.  2006. Identification of acquired DNA in Neisseria lactamica. FEMS Microbiol. Lett. 262:77–84 [Google Scholar]
  196. van Passel MW, van der Ende A, Bart A. 193.  2006. Plasmid diversity in neisseriae. Infect. Immun. 74:4892–99 [Google Scholar]
  197. Vink C, Rudenko G, Seifert HS. 194.  2012. Microbial antigenic variation mediated by homologous DNA recombination. FEMS Microbiol. Rev. 36917–48 [Google Scholar]
  198. Wainwright LA, Frangipane JV, Seifert HS. 195.  1997. Analysis of protein binding to the Sma/Cla DNA repeat in pathogenic Neisseriae. Nucleic Acids Res. 25:1362–68 [Google Scholar]
  199. Wainwright LA, Pritchard KH, Seifert HS. 196.  1994. A conserved DNA sequence is required for efficient gonococcal pilin antigenic variation. Mol. Microbiol. 13:75–87 [Google Scholar]
  200. 197. WHO 1998. Control of Epidemic Meningococcal Disease. WHO Practical Guidelines Geneva, Switz: World Health Organ. [Google Scholar]
  201. 198. WHO 2012. Global Incidence and Prevalence of Selected Curable Sexually Transmitted Infections - 2008 Geneva, Switz: World Health Organ. [Google Scholar]
  202. Wolfgang M, Lauer P, Park HS, Brossay L, Hebert J, Koomey M. 199.  1998. PilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated Neisseria gonorrhoeae. Mol. Microbiol. 29:321–30 [Google Scholar]
  203. Woodhams KL, Benet ZL, Blonsky SE, Hackett KT, Dillard JP. 200.  2012. Prevalence and detailed mapping of the gonococcal genetic island in Neisseria meningitidis. J. Bacteriol. 194:2275–85 [Google Scholar]
  204. Woods JP, Spinola SM, Strobel SM, Cannon JG. 201.  1989. Conserved lipoprotein H.8 of pathogenic Neisseria consists entirely of pentapeptide repeats. Mol. Microbiol. 3:43–48 [Google Scholar]
  205. Workowski KA, Berman S. 202.  2010. Sexually transmitted diseases treatment guidelines, 2010. Morb. Mortal. Wkly. Rep. 59:1–110 [Google Scholar]
  206. Workowski KA, Berman SM, Douglas JM Jr. 203.  2008. Emerging antimicrobial resistance in Neisseria gonorrhoeae: urgent need to strengthen prevention strategies. Ann. Intern. Med. 148:606–13 [Google Scholar]
  207. Yang QL, Gotschlich EC. 204.  1996. Variation of gonococcal lipooligosaccharide structure is due to alterations in poly-G tracts in lgt genes encoding glycosyl transferases. J. Exp. Med. 183:323–27 [Google Scholar]
  208. Zhang JR, Norris SJ. 205.  1998. Genetic variation of the Borrelia burgdorferi gene vlsE involves cassette-specific, segmental gene conversion. Infect. Immun. 66:3698–704 [Google Scholar]
  209. Zhang Y, Heidrich N, Ampattu BJ, Gunderson CW, Seifert HS. 206.  et al. 2013. Processing-independent CRISPR RNAs limit natural transformation in Neisseria meningitidis. Mol. Cell 50:488–503 [Google Scholar]
  210. Zola TA, Strange HR, Dominguez NM, Dillard JP, Cornelissen CN. 207.  2010. Type IV secretion machinery promotes Ton-independent intracellular survival of Neisseria gonorrhoeae within cervical epithelial cells. Infect. Immun. 78:2429–37 [Google Scholar]
/content/journals/10.1146/annurev-genet-120213-092007
Loading
/content/journals/10.1146/annurev-genet-120213-092007
Loading

Data & Media loading...

  • Article Type: Review Article
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