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. 1995 Nov;177(22):6390–6400. doi: 10.1128/jb.177.22.6390-6400.1995

The physical map of the chromosome of a serogroup A strain of Neisseria meningitidis shows complex rearrangements relative to the chromosomes of the two mapped strains of the closely related species N. gonorrhoeae.

J A Dempsey 1, A B Wallace 1, J G Cannon 1
PMCID: PMC177488  PMID: 7592413

Abstract

A physical map of the chromosome of N. meningitidis Z2491 (serogroup A, subgroup IV-1) has been constructed. Z2491 DNA was digested with NheI, SpeI, SgfI, PacI, BglII, or PmeI, resulting in a limited number of fragments that were resolved by contour-clamped homogeneous electric field (CHEF) electrophoresis. The estimated genome size for this strain was 2,226 kb. To construct the map, probes corresponding to single-copy genes or sequences were used on Southern blots of chromosomal DNA digested with the different mapping enzymes and subjected to CHEF electrophoresis. By determining which fragments from different digests hybridized to each specific probe, it was possible to walk back and forth between digests to form a circular macrorestriction map. The intervals between mapped restriction sites range from 10 to 143 kb in size. A total of 117 markers have been placed on the map; 75 represent identified genes, with the remaining markers defined by anonymous cloned fragments of neisserial DNA. Comparison of the arrangement of genetic loci in Z2491 with that in gonococcal strain FA1090, for which a physical map was previously constructed, revealed complex genomic rearrangements between the two strains. Although gene order is generally conserved over much of the chromosome, a region of approximately 500 kb shows translocation and/or inversion of multiple blocks of markers between the two strains. Even within the relatively conserved portions of the maps, several genetic markers are in different positions in Z2491 and FA1090.

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Selected References

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  1. Achtman M. Clonal spread of serogroup A meningococci: a paradigm for the analysis of microevolution in bacteria. Mol Microbiol. 1994 Jan;11(1):15–22. doi: 10.1111/j.1365-2958.1994.tb00285.x. [DOI] [PubMed] [Google Scholar]
  2. Achtman M., Wall R. A., Bopp M., Kusecek B., Morelli G., Saken E., Hassan-King M. Variation in class 5 protein expression by serogroup A meningococci during a meningitis epidemic. J Infect Dis. 1991 Aug;164(2):375–382. doi: 10.1093/infdis/164.2.375. [DOI] [PubMed] [Google Scholar]
  3. Aho E. L., Cannon J. G. Characterization of a silent pilin gene locus from Neisseria meningitidis strain FAM18. Microb Pathog. 1988 Nov;5(5):391–398. doi: 10.1016/0882-4010(88)90039-3. [DOI] [PubMed] [Google Scholar]
  4. Aho E. L., Dempsey J. A., Hobbs M. M., Klapper D. G., Cannon J. G. Characterization of the opa (class 5) gene family of Neisseria meningitidis. Mol Microbiol. 1991 Jun;5(6):1429–1437. doi: 10.1111/j.1365-2958.1991.tb00789.x. [DOI] [PubMed] [Google Scholar]
  5. Anderson J. E., Sparling P. F., Cornelissen C. N. Gonococcal transferrin-binding protein 2 facilitates but is not essential for transferrin utilization. J Bacteriol. 1994 Jun;176(11):3162–3170. doi: 10.1128/jb.176.11.3162-3170.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Barlow A. K., Heckels J. E., Clarke I. N. The class 1 outer membrane protein of Neisseria meningitidis: gene sequence and structural and immunological similarities to gonococcal porins. Mol Microbiol. 1989 Feb;3(2):131–139. doi: 10.1111/j.1365-2958.1989.tb01802.x. [DOI] [PubMed] [Google Scholar]
  7. Bautsch W. A NheI macrorestriction map of the Neisseria meningitidis B1940 genome. FEMS Microbiol Lett. 1993 Mar 1;107(2-3):191–197. doi: 10.1111/j.1574-6968.1993.tb06029.x. [DOI] [PubMed] [Google Scholar]
  8. Belland R. J., Morrison S. G., Ison C., Huang W. M. Neisseria gonorrhoeae acquires mutations in analogous regions of gyrA and parC in fluoroquinolone-resistant isolates. Mol Microbiol. 1994 Oct;14(2):371–380. doi: 10.1111/j.1365-2958.1994.tb01297.x. [DOI] [PubMed] [Google Scholar]
  9. Beucher M., Sparling P. F. Cloning, sequencing, and characterization of the gene encoding FrpB, a major iron-regulated, outer membrane protein of Neisseria gonorrhoeae. J Bacteriol. 1995 Apr;177(8):2041–2049. doi: 10.1128/jb.177.8.2041-2049.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bhat K. S., Gibbs C. P., Barrera O., Morrison S. G., Jähnig F., Stern A., Kupsch E. M., Meyer T. F., Swanson J. The opacity proteins of Neisseria gonorrhoeae strain MS11 are encoded by a family of 11 complete genes. Mol Microbiol. 1991 Aug;5(8):1889–1901. doi: 10.1111/j.1365-2958.1991.tb00813.x. [DOI] [PubMed] [Google Scholar]
  11. Bihimaier A., Römling U., Meyer T. F., Tümmler B., Gibbs C. P. Physical and genetic map of the Neisseria gonorrhoeae strain MS11-N198 chromosome. Mol Microbiol. 1991 Oct;5(10):2529–2539. doi: 10.1111/j.1365-2958.1991.tb02099.x. [DOI] [PubMed] [Google Scholar]
  12. Biswas G. D., Thompson S. A., Sparling P. F. Gene transfer in Neisseria gonorrhoeae. Clin Microbiol Rev. 1989 Apr;2 (Suppl):S24–S28. doi: 10.1128/cmr.2.suppl.s24. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Butcher S., Sarvas M., Runeberg-Nyman K. Class-3 porin protein of Neisseria meningitidis: cloning and structure of the gene. Gene. 1991 Aug 30;105(1):125–128. doi: 10.1016/0378-1119(91)90523-e. [DOI] [PubMed] [Google Scholar]
  14. Bygraves J. A., Maiden M. C. Analysis of the clonal relationships between strains of Neisseria meningitidis by pulsed field gel electrophoresis. J Gen Microbiol. 1992 Mar;138(3):523–531. doi: 10.1099/00221287-138-3-523. [DOI] [PubMed] [Google Scholar]
  15. Cantor C. R., Smith C. L., Mathew M. K. Pulsed-field gel electrophoresis of very large DNA molecules. Annu Rev Biophys Biophys Chem. 1988;17:287–304. doi: 10.1146/annurev.bb.17.060188.001443. [DOI] [PubMed] [Google Scholar]
  16. Carle G. F., Olson M. V. Separation of chromosomal DNA molecules from yeast by orthogonal-field-alternation gel electrophoresis. Nucleic Acids Res. 1984 Jul 25;12(14):5647–5664. doi: 10.1093/nar/12.14.5647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Chu G., Vollrath D., Davis R. W. Separation of large DNA molecules by contour-clamped homogeneous electric fields. Science. 1986 Dec 19;234(4783):1582–1585. doi: 10.1126/science.3538420. [DOI] [PubMed] [Google Scholar]
  18. Cole S. T., Saint Girons I. Bacterial genomics. FEMS Microbiol Rev. 1994 Jun;14(2):139–160. doi: 10.1111/j.1574-6976.1994.tb00084.x. [DOI] [PubMed] [Google Scholar]
  19. Connell T. D., Black W. J., Kawula T. H., Barritt D. S., Dempsey J. A., Kverneland K., Jr, Stephenson A., Schepart B. S., Murphy G. L., Cannon J. G. Recombination among protein II genes of Neisseria gonorrhoeae generates new coding sequences and increases structural variability in the protein II family. Mol Microbiol. 1988 Mar;2(2):227–236. doi: 10.1111/j.1365-2958.1988.tb00024.x. [DOI] [PubMed] [Google Scholar]
  20. Cornelissen C. N., Biswas G. D., Tsai J., Paruchuri D. K., Thompson S. A., Sparling P. F. Gonococcal transferrin-binding protein 1 is required for transferrin utilization and is homologous to TonB-dependent outer membrane receptors. J Bacteriol. 1992 Sep;174(18):5788–5797. doi: 10.1128/jb.174.18.5788-5797.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Crowe B. A., Wall R. A., Kusecek B., Neumann B., Olyhoek T., Abdillahi H., Hassan-King M., Greenwood B. M., Poolman J. T., Achtman M. Clonal and variable properties of Neisseria meningitidis isolated from cases and carriers during and after an epidemic in The Gambia, West Africa. J Infect Dis. 1989 Apr;159(4):686–700. doi: 10.1093/infdis/159.4.686. [DOI] [PubMed] [Google Scholar]
  22. Davies J. K. DNA restriction and modification systems in Neisseria gonorrhoeae. Clin Microbiol Rev. 1989 Apr;2 (Suppl):S78–S82. doi: 10.1128/cmr.2.suppl.s78. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Dempsey J. A., Cannon J. G. Locations of genetic markers on the physical map of the chromosome of Neisseria gonorrhoeae FA1090. J Bacteriol. 1994 Apr;176(7):2055–2060. doi: 10.1128/jb.176.7.2055-2060.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Dempsey J. A., Litaker W., Madhure A., Snodgrass T. L., Cannon J. G. Physical map of the chromosome of Neisseria gonorrhoeae FA1090 with locations of genetic markers, including opa and pil genes. J Bacteriol. 1991 Sep;173(17):5476–5486. doi: 10.1128/jb.173.17.5476-5486.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Dempsey J. A., Sharp G., Litaker W. An inexpensive power supply for agarose gel electrophoresis. Biotechniques. 1994 Apr;16(4):602–604. [PubMed] [Google Scholar]
  26. Enright M. C., Carter P. E., MacLean I. A., McKenzie H. Phylogenetic relationships between some members of the genera Neisseria, Acinetobacter, Moraxella, and Kingella based on partial 16S ribosomal DNA sequence analysis. Int J Syst Bacteriol. 1994 Jul;44(3):387–391. doi: 10.1099/00207713-44-3-387. [DOI] [PubMed] [Google Scholar]
  27. Feavers I. M., Heath A. B., Bygraves J. A., Maiden M. C. Role of horizontal genetic exchange in the antigenic variation of the class 1 outer membrane protein of Neisseria meningitidis. Mol Microbiol. 1992 Feb;6(4):489–495. doi: 10.1111/j.1365-2958.1992.tb01493.x. [DOI] [PubMed] [Google Scholar]
  28. Frosch M., Edwards U., Bousset K., Krausse B., Weisgerber C. Evidence for a common molecular origin of the capsule gene loci in gram-negative bacteria expressing group II capsular polysaccharides. Mol Microbiol. 1991 May;5(5):1251–1263. doi: 10.1111/j.1365-2958.1991.tb01899.x. [DOI] [PubMed] [Google Scholar]
  29. Gotschlich E. C., Seiff M., Blake M. S. The DNA sequence of the structural gene of gonococcal protein III and the flanking region containing a repetitive sequence. Homology of protein III with enterobacterial OmpA proteins. J Exp Med. 1987 Feb 1;165(2):471–482. doi: 10.1084/jem.165.2.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Guibourdenche M., Popoff M. Y., Riou J. Y. Deoxyribonucleic acid relatedness among Neisseria gonorrhoeae, N. meningitidis, N. lactamica, N. cinerea and "Neisseria polysaccharea". Ann Inst Pasteur Microbiol. 1986 Sep-Oct;137B(2):177–185. doi: 10.1016/s0769-2609(86)80106-5. [DOI] [PubMed] [Google Scholar]
  31. Gunn J. S., Piekarowicz A., Chien R., Stein D. C. Cloning and linkage analysis of Neisseria gonorrhoeae DNA methyltransferases. J Bacteriol. 1992 Sep;174(17):5654–5660. doi: 10.1128/jb.174.17.5654-5660.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Halter R., Pohlner J., Meyer T. F. Mosaic-like organization of IgA protease genes in Neisseria gonorrhoeae generated by horizontal genetic exchange in vivo. EMBO J. 1989 Sep;8(9):2737–2744. doi: 10.1002/j.1460-2075.1989.tb08415.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hatten L. A., Schweizer H. P., Averill N., Wang L., Schryvers A. B. Cloning and characterization of the Neisseria meningitidis asd gene. Gene. 1993 Jul 15;129(1):123–128. doi: 10.1016/0378-1119(93)90707-a. [DOI] [PubMed] [Google Scholar]
  34. Heckels J. E. Structure and function of pili of pathogenic Neisseria species. Clin Microbiol Rev. 1989 Apr;2 (Suppl):S66–S73. doi: 10.1128/cmr.2.suppl.s66. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Hobbs M. M., Seiler A., Achtman M., Cannon J. G. Microevolution within a clonal population of pathogenic bacteria: recombination, gene duplication and horizontal genetic exchange in the opa gene family of Neisseria meningitidis. Mol Microbiol. 1994 Apr;12(2):171–180. doi: 10.1111/j.1365-2958.1994.tb01006.x. [DOI] [PubMed] [Google Scholar]
  36. Hoehn G. T., Clark V. L. Isolation and nucleotide sequence of the gene (aniA) encoding the major anaerobically induced outer membrane protein of Neisseria gonorrhoeae. Infect Immun. 1992 Nov;60(11):4695–4703. doi: 10.1128/iai.60.11.4695-4703.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Jonsson A. B., Nyberg G., Normark S. Phase variation of gonococcal pili by frameshift mutation in pilC, a novel gene for pilus assembly. EMBO J. 1991 Feb;10(2):477–488. doi: 10.1002/j.1460-2075.1991.tb07970.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. KELLOGG D. S., Jr, PEACOCK W. L., Jr, DEACON W. E., BROWN L., PIRKLE D. I. NEISSERIA GONORRHOEAE. I. VIRULENCE GENETICALLY LINKED TO CLONAL VARIATION. J Bacteriol. 1963 Jun;85:1274–1279. doi: 10.1128/jb.85.6.1274-1279.1963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Koomey J. M., Falkow S. Cloning of the recA gene of Neisseria gonorrhoeae and construction of gonococcal recA mutants. J Bacteriol. 1987 Feb;169(2):790–795. doi: 10.1128/jb.169.2.790-795.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Koomey J. M., Gill R. E., Falkow S. Genetic and biochemical analysis of gonococcal IgA1 protease: cloning in Escherichia coli and construction of mutants of gonococci that fail to produce the activity. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7881–7885. doi: 10.1073/pnas.79.24.7881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Kristiansen B. E., Rådström P., Jenkins A., Ask E., Facinelli B., Sköld O. Cloning and characterization of a DNA fragment that confers sulfonamide resistance in a serogroup B, serotype 15 strain of Neisseria meningitidis. Antimicrob Agents Chemother. 1990 Nov;34(11):2277–2279. doi: 10.1128/aac.34.11.2277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Lauer P., Albertson N. H., Koomey M. Conservation of genes encoding components of a type IV pilus assembly/two-step protein export pathway in Neisseria gonorrhoeae. Mol Microbiol. 1993 Apr;8(2):357–368. doi: 10.1111/j.1365-2958.1993.tb01579.x. [DOI] [PubMed] [Google Scholar]
  43. Liu S. L., Hessel A., Sanderson K. E. The XbaI-BlnI-CeuI genomic cleavage map of Salmonella typhimurium LT2 determined by double digestion, end labelling, and pulsed-field gel electrophoresis. J Bacteriol. 1993 Jul;175(13):4104–4120. doi: 10.1128/jb.175.13.4104-4120.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Liu S. L., Sanderson K. E. Rearrangements in the genome of the bacterium Salmonella typhi. Proc Natl Acad Sci U S A. 1995 Feb 14;92(4):1018–1022. doi: 10.1073/pnas.92.4.1018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Maiden M. C. Population genetics of a transformable bacterium: the influence of horizontal genetic exchange on the biology of Neisseria meningitidis. FEMS Microbiol Lett. 1993 Sep 15;112(3):243–250. doi: 10.1111/j.1574-6968.1993.tb06457.x. [DOI] [PubMed] [Google Scholar]
  46. Martin P. R., Cooperider J. W., Mulks M. H. Sequence of the argF gene encoding ornithine transcarbamoylase from Neisseria gonorrhoeae. Gene. 1990 Sep 28;94(1):139–140. doi: 10.1016/0378-1119(90)90482-7. [DOI] [PubMed] [Google Scholar]
  47. Martin P. R., Mulks M. H. Sequence analysis and complementation studies of the argJ gene encoding ornithine acetyltransferase from Neisseria gonorrhoeae. J Bacteriol. 1992 Apr;174(8):2694–2701. doi: 10.1128/jb.174.8.2694-2701.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. McShan W. M., Williams R. P., Hull R. A. A recombinant molecule from a disseminating strain of Neisseria gonorrhoeae that confers serum bactericidal resistance. Infect Immun. 1987 Dec;55(12):3017–3022. doi: 10.1128/iai.55.12.3017-3022.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Meyer T. F., Gibbs C. P., Haas R. Variation and control of protein expression in Neisseria. Annu Rev Microbiol. 1990;44:451–477. doi: 10.1146/annurev.mi.44.100190.002315. [DOI] [PubMed] [Google Scholar]
  50. Miloso M., Limauro D., Alifano P., Rivellini F., Lavitola A., Gulletta E., Bruni C. B. Characterization of the rho genes of Neisseria gonorrhoeae and Salmonella typhimurium. J Bacteriol. 1993 Dec;175(24):8030–8037. doi: 10.1128/jb.175.24.8030-8037.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Morelli G., del Valle J., Lammel C. J., Pohlner J., Müller K., Blake M., Brooks G. F., Meyer T. F., Koumaré B., Brieske N. Immunogenicity and evolutionary variability of epitopes within IgA1 protease from serogroup A Neisseria meningitidis. Mol Microbiol. 1994 Jan;11(1):175–187. doi: 10.1111/j.1365-2958.1994.tb00299.x. [DOI] [PubMed] [Google Scholar]
  52. O'Rourke M., Spratt B. G. Further evidence for the non-clonal population structure of Neisseria gonorrhoeae: extensive genetic diversity within isolates of the same electrophoretic type. Microbiology. 1994 Jun;140(Pt 6):1285–1290. doi: 10.1099/00221287-140-6-1285. [DOI] [PubMed] [Google Scholar]
  53. Olyhoek A. J., Sarkari J., Bopp M., Morelli G., Achtman M. Cloning and expression in Escherichia coli of opc, the gene for an unusual class 5 outer membrane protein from Neisseria meningitidis (meningococci/surface antigen). Microb Pathog. 1991 Oct;11(4):249–257. doi: 10.1016/0882-4010(91)90029-a. [DOI] [PubMed] [Google Scholar]
  54. Palermo D. A., Evans T. M., Clark V. L. Expression of a cloned lipopolysaccharide antigen from Neisseria gonorrhoeae on the surface of Escherichia coli K-12. Infect Immun. 1987 Nov;55(11):2844–2849. doi: 10.1128/iai.55.11.2844-2849.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Pan W., Spratt B. G. Regulation of the permeability of the gonococcal cell envelope by the mtr system. Mol Microbiol. 1994 Feb;11(4):769–775. doi: 10.1111/j.1365-2958.1994.tb00354.x. [DOI] [PubMed] [Google Scholar]
  56. Pannekoek Y., Dankert J., van Putten J. P. Construction of recombinant neisserial Hsp60 proteins and mapping of antigenic domains. Mol Microbiol. 1995 Jan;15(2):277–285. doi: 10.1111/j.1365-2958.1995.tb02242.x. [DOI] [PubMed] [Google Scholar]
  57. Perry A. C., Nicolson I. J., Saunders J. R. Neisseria meningitidis C114 contains silent, truncated pilin genes that are homologous to Neisseria gonorrhoeae pil sequences. J Bacteriol. 1988 Apr;170(4):1691–1697. doi: 10.1128/jb.170.4.1691-1697.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Picard F. J., Dillon J. R. Cloning and organization of seven arginine biosynthesis genes from Neisseria gonorrhoeae. J Bacteriol. 1989 Mar;171(3):1644–1651. doi: 10.1128/jb.171.3.1644-1651.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Potts W. J., Saunders J. R. Nucleotide sequence of the structural gene for class I pilin from Neisseria meningitidis: homologies with the pilE locus of Neisseria gonorrhoeae. Mol Microbiol. 1988 Sep;2(5):647–653. doi: 10.1111/j.1365-2958.1988.tb00073.x. [DOI] [PubMed] [Google Scholar]
  60. Roberts M. C. Plasmids of Neisseria gonorrhoeae and other Neisseria species. Clin Microbiol Rev. 1989 Apr;2 (Suppl):S18–S23. doi: 10.1128/cmr.2.suppl.s18. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Robertson B. D., Meyer T. F. Genetic variation in pathogenic bacteria. Trends Genet. 1992 Dec;8(12):422–427. doi: 10.1016/0168-9525(92)90325-x. [DOI] [PubMed] [Google Scholar]
  62. Sarkari J., Pandit N., Moxon E. R., Achtman M. Variable expression of the Opc outer membrane protein in Neisseria meningitidis is caused by size variation of a promoter containing poly-cytidine. Mol Microbiol. 1994 Jul;13(2):207–217. doi: 10.1111/j.1365-2958.1994.tb00416.x. [DOI] [PubMed] [Google Scholar]
  63. Smith C. L., Condemine G. New approaches for physical mapping of small genomes. J Bacteriol. 1990 Mar;172(3):1167–1172. doi: 10.1128/jb.172.3.1167-1172.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Spratt B. G., Bowler L. D., Zhang Q. Y., Zhou J., Smith J. M. Role of interspecies transfer of chromosomal genes in the evolution of penicillin resistance in pathogenic and commensal Neisseria species. J Mol Evol. 1992 Feb;34(2):115–125. doi: 10.1007/BF00182388. [DOI] [PubMed] [Google Scholar]
  65. Spratt B. G. Hybrid penicillin-binding proteins in penicillin-resistant strains of Neisseria gonorrhoeae. Nature. 1988 Mar 10;332(6160):173–176. doi: 10.1038/332173a0. [DOI] [PubMed] [Google Scholar]
  66. Stein D. C., Danaher R. J., Cook T. M. Characterization of a gyrB mutation responsible for low-level nalidixic acid resistance in Neisseria gonorrhoeae. Antimicrob Agents Chemother. 1991 Apr;35(4):622–626. doi: 10.1128/aac.35.4.622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Stein D. C., Silver L. E., Clark V. L., Young F. E. Cloning genes for proline biosynthesis from Neisseria gonorrhoeae: identification by interspecific complementation of Escherichia coli mutants. J Bacteriol. 1984 May;158(2):696–700. doi: 10.1128/jb.158.2.696-700.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Stern A., Brown M., Nickel P., Meyer T. F. Opacity genes in Neisseria gonorrhoeae: control of phase and antigenic variation. Cell. 1986 Oct 10;47(1):61–71. doi: 10.1016/0092-8674(86)90366-1. [DOI] [PubMed] [Google Scholar]
  69. Stern A., Meyer T. F. Common mechanism controlling phase and antigenic variation in pathogenic neisseriae. Mol Microbiol. 1987 Jul;1(1):5–12. doi: 10.1111/j.1365-2958.1987.tb00520.x. [DOI] [PubMed] [Google Scholar]
  70. Sullivan K. M., Saunders J. R. Nucleotide sequence and genetic organization of the NgoPII restriction-modification system of Neisseria gonorrhoeae. Mol Gen Genet. 1989 Apr;216(2-3):380–387. doi: 10.1007/BF00334379. [DOI] [PubMed] [Google Scholar]
  71. Sullivan K. M., Saunders J. R. Sequence analysis of the NgoPII methyltransferase gene from Neisseria gonorrhoeae P9: homologies with other enzymes recognizing the sequence 5'-GGCC-3'. Nucleic Acids Res. 1988 May 25;16(10):4369–4387. doi: 10.1093/nar/16.10.4369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Thomas C. E., Sparling P. F. Identification and cloning of a fur homologue from Neisseria meningitidis. Mol Microbiol. 1994 Feb;11(4):725–737. doi: 10.1111/j.1365-2958.1994.tb00350.x. [DOI] [PubMed] [Google Scholar]
  73. Thompson S. A., Wang L. L., Sparling P. F. Cloning and nucleotide sequence of frpC, a second gene from Neisseria meningitidis encoding a protein similar to RTX cytotoxins. Mol Microbiol. 1993 Jul;9(1):85–96. doi: 10.1111/j.1365-2958.1993.tb01671.x. [DOI] [PubMed] [Google Scholar]
  74. Thompson S. A., Wang L. L., West A., Sparling P. F. Neisseria meningitidis produces iron-regulated proteins related to the RTX family of exoproteins. J Bacteriol. 1993 Feb;175(3):811–818. doi: 10.1128/jb.175.3.811-818.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Tinsley C. R., Manjula B. N., Gotschlich E. C. Purification and characterization of polyphosphate kinase from Neisseria meningitidis. Infect Immun. 1993 Sep;61(9):3703–3710. doi: 10.1128/iai.61.9.3703-3710.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Tsai W. M., Larsen S. H., Wilde C. E., 3rd Cloning and DNA sequence of the omc gene encoding the outer membrane protein-macromolecular complex from Neisseria gonorrhoeae. Infect Immun. 1989 Sep;57(9):2653–2659. doi: 10.1128/iai.57.9.2653-2659.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Virji M., Heckels J. E., Potts W. J., Hart C. A., Saunders J. R. Identification of epitopes recognized by monoclonal antibodies SM1 and SM2 which react with all pili of Neisseria gonorrhoeae but which differentiate between two structural classes of pili expressed by Neisseria meningitidis and the distribution of their encoding sequences in the genomes of Neisseria spp. J Gen Microbiol. 1989 Dec;135(12):3239–3251. doi: 10.1099/00221287-135-12-3239. [DOI] [PubMed] [Google Scholar]
  78. Virji M., Makepeace K., Ferguson D. J., Achtman M., Moxon E. R. Meningococcal Opa and Opc proteins: their role in colonization and invasion of human epithelial and endothelial cells. Mol Microbiol. 1993 Nov;10(3):499–510. doi: 10.1111/j.1365-2958.1993.tb00922.x. [DOI] [PubMed] [Google Scholar]
  79. Virji M., Makepeace K., Ferguson D. J., Achtman M., Sarkari J., Moxon E. R. Expression of the Opc protein correlates with invasion of epithelial and endothelial cells by Neisseria meningitidis. Mol Microbiol. 1992 Oct;6(19):2785–2795. doi: 10.1111/j.1365-2958.1992.tb01458.x. [DOI] [PubMed] [Google Scholar]
  80. Virji M., Makepeace K., Moxon E. R. Distinct mechanisms of interactions of Opc-expressing meningococci at apical and basolateral surfaces of human endothelial cells; the role of integrins in apical interactions. Mol Microbiol. 1994 Oct;14(1):173–184. doi: 10.1111/j.1365-2958.1994.tb01277.x. [DOI] [PubMed] [Google Scholar]
  81. Vollrath D., Davis R. W. Resolution of DNA molecules greater than 5 megabases by contour-clamped homogeneous electric fields. Nucleic Acids Res. 1987 Oct 12;15(19):7865–7876. doi: 10.1093/nar/15.19.7865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Vázquez J. A., Berrón S., O'Rourke M., Carpenter G., Feil E., Smith N. H., Spratt B. G. Interspecies recombination in nature: a meningococcus that has acquired a gonococcal PIB porin. Mol Microbiol. 1995 Mar;15(6):1001–1007. doi: 10.1111/j.1365-2958.1995.tb02275.x. [DOI] [PubMed] [Google Scholar]
  83. Weil M. D., McClelland M. Enzymatic cleavage of a bacterial genome at a 10-base-pair recognition site. Proc Natl Acad Sci U S A. 1989 Jan;86(1):51–55. doi: 10.1073/pnas.86.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Woods J. P., Dempsey J. F., Kawula T. H., Barritt D. S., Cannon J. G. Characterization of the neisserial lipid-modified azurin bearing the H.8 epitope. Mol Microbiol. 1989 May;3(5):583–591. doi: 10.1111/j.1365-2958.1989.tb00205.x. [DOI] [PubMed] [Google Scholar]
  85. Woods J. P., Spinola S. M., Strobel S. M., Cannon J. G. Conserved lipoprotein H.8 of pathogenic Neisseria consists entirely of pentapeptide repeats. Mol Microbiol. 1989 Jan;3(1):43–48. doi: 10.1111/j.1365-2958.1989.tb00102.x. [DOI] [PubMed] [Google Scholar]
  86. Wright C. J., Jerse A. E., Cohen M. S., Cannon J. G., Seifert H. S. Nonrepresentative PCR amplification of variable gene sequences in clinical specimens containing dilute, complex mixtures of microorganisms. J Clin Microbiol. 1994 Feb;32(2):464–468. doi: 10.1128/jcm.32.2.464-468.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Young R. A., Davis R. W. Efficient isolation of genes by using antibody probes. Proc Natl Acad Sci U S A. 1983 Mar;80(5):1194–1198. doi: 10.1073/pnas.80.5.1194. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Zhou D., Lee N. G., Apicella M. A. Lipooligosaccharide biosynthesis in Neisseria gonorrhoeae: cloning, identification and characterization of the alpha 1,5 heptosyltransferase I gene (rfaC) Mol Microbiol. 1994 Nov;14(4):609–618. doi: 10.1111/j.1365-2958.1994.tb01300.x. [DOI] [PubMed] [Google Scholar]
  89. Zhou D., Stephens D. S., Gibson B. W., Engstrom J. J., McAllister C. F., Lee F. K., Apicella M. A. Lipooligosaccharide biosynthesis in pathogenic Neisseria. Cloning, identification, and characterization of the phosphoglucomutase gene. J Biol Chem. 1994 Apr 15;269(15):11162–11169. [PubMed] [Google Scholar]
  90. Zhou J., Spratt B. G. Sequence diversity within the argF, fbp and recA genes of natural isolates of Neisseria meningitidis: interspecies recombination within the argF gene. Mol Microbiol. 1992 Aug;6(15):2135–2146. doi: 10.1111/j.1365-2958.1992.tb01387.x. [DOI] [PubMed] [Google Scholar]

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