Description of an unusual Neisseria meningitidis isolate containing and expressing neisseria gonorrhoeae-specific 16S rRNA gene sequences

Journal of Clinical Microbiology

Volumn 51, Issue 10, 2013, Pages 3199-3206

  Walcher, Marion ^a   Skvoretz, Rhonda ^a   Montgomery Fullerton, Megan ^a   Jonas, Vivian ^a   Brentano, Steve ^a  

^a Gen Probe Incorporated   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

ARTICLE; BACTERIAL GENE; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; CROSS REACTION; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; GENE SEQUENCE; GENETIC RECOMBINATION; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RNA 16S GENE; SEQUENCE ANALYSIS; STRAIN DIFFERENCE;

BACTERIAL TYPING TECHNIQUES; CLUSTER ANALYSIS; DNA, BACTERIAL; DNA, RIBOSOMAL; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MOLECULAR SEQUENCE DATA; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

EID: 84884807566     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.00309-13     Document Type: Article

References (74)

1. Gibbs CP, Meyer TF. 1996. Genome plasticity in Neisseria gonorrhoeae. FEMS Microbiol. Lett. 145:173-179. (Pubitemid 26395412)
2. Hamilton HL, Dillard JP. 2006. Natural transformation of Neisseria gonorrhoeae: from DNA donation to homologous recombination. Mol. Microbiol. 59:376-385.
3. Linz B, Schenker M, Zhu P, Achtman M. 2000. Frequent interspecific genetic exchange between commensal neisseriae and Neisseria meningitidis. Mol. Microbiol. 36:1049-1058. (Pubitemid 30330677)
4. Dunning Hotopp JC, Grifantini R, Kumar N, Tzeng YL, Fouts D, Frigimelica E, Draghi M, Giuliani MM, Rappuoli R, Stephens DS, Grandi G, Tettelin H. 2006. Comparative genomics of Neisseria meningitidis: core genome, islands of horizontal transfer and pathogen-specific genes. Microbiology 152:3733-3749. (Pubitemid 46040693)
5. Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, Zhang Q, Zhou J, Zurth K, Caugant DA, Feavers IM, Achtman M, Spratt BG. 1998. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. U. S. A. 95:3140-3145. (Pubitemid 28135868)
6. Marri PR, Paniscus M, Weyand NJ, Rendon MA, Calton CM, Hernandez DR, Higashi DL, Sodergren E, Weinstock GM, Rounsley SD, So M. 2010. Genome sequencing reveals widespread virulence gene exchange among human Neisseria species. PLoS One 5:e11835. doi:10.1371/journal. pone.0011835.
7. Feil EJ, Enright MC, Spratt BG. 2000. Estimating the relative contributions of mutation and recombination to clonal diversification: a comparison between Neisseria meningitidis and Streptococcus pneumoniae. Res. Microbiol. 151:465-469. (Pubitemid 30619799)
8. Feil EJ, Maiden MC, Achtman M, Spratt BG. 1999. The relative contributions of recombination and mutation to the divergence of clones of Neisseria meningitidis. Mol. Biol. Evol. 16:1496-1502. (Pubitemid 29510892)
9. Bennett JS, Jolley KA, Sparling PF, Saunders NJ, Hart CA, Feavers IM, Maiden MC. 2007. Species status of Neisseria gonorrhoeae: evolutionary and epidemiological inferences from multilocus sequence typing. BMC Biol. 5:35. doi:10.1186/1741-7007-5-35. (Pubitemid 47617292)
10. Yakubu DE, Abadi FJ, Pennington TH. 1999. Molecular typing methods for Neisseria meningitidis. J. Med. Microbiol. 48:1055-1064.
11. Didelot X, Urwin R, Maiden MC, Falush D. 2009. Genealogical typing of Neisseria meningitidis. Microbiology 155:3176-3186.
12. Urwin R, Maiden MC. 2003. Multi-locus sequence typing: a tool for global epidemiology. Trends Microbiol. 11:479-487. (Pubitemid 37214875)
13. Jolley KA, Brehony C, Maiden MC. 2007. Molecular typing of meningococci: recommendations for target choice and nomenclature. FEMS Microbiol. Rev. 31:89-96. (Pubitemid 46058824)
14. Jolley KA, Maiden MC. 2006. Agdb Net: antigen sequence database software for bacterial typing. BMC Bioinformatics 7:314. doi:10.1186/1471-2105-7-314.
15. Caugant DA. 2001. Global trends in meningococcal disease. Methods Mol. Med. 67:273-292.
16. Guibourdenche M, Popoff MY, Riou JY. 1986. Deoxyribonucleic acid relatedness among Neisseria gonorrhoeae, N. meningitidis, N. lactamica, N. cinerea and "Neisseria polysaccharea." Ann. Inst. Pasteur Microbiol. 137B: 177-185. (Pubitemid 17186317)
17. Kingsbury DT. 1967. Deoxyribonucleic acid homologies among species of the genus Neisseria. J. Bacteriol. 94:870-874.
18. Vazquez JA, de la Fuente L, Berron S, O'Rourke M, Smith NH, Zhou J, Spratt BG. 1993. Ecological separation and genetic isolation of Neisseria gonorrhoeae and Neisseria meningitidis. Curr. Biol. 3:567-572.
19. Faur YC, Wilson ME, May PS. 1981. Isolation of N. meningitidis from patients in a gonorrhea screen program: a four-year survey in New York City. Am. J. Public Health 71:53-58. (Pubitemid 11207807)
20. Wilson AP, Wolff J, Atia W. 1989. Acute urethritis due to Neisseria meningitidis group Aacquired by orogenital contact: case report. Genitourin. Med. 65:122-123. (Pubitemid 19130411)
21. Beck A, Fluker JL, Platt DJ. 1974. Neisseria meningitidis in urogenital infection. Br. J. Vener. Dis. 50:367-369.
22. Kanemitsu N, Hayashi I, Satoh N, Hayakawa T, Mitsuya H, Hayase Y, Hiramoto K, Kojima M. 2003. Acute urethritis caused by Neisseria meningitidis. Int. J. Urol. 10:346-347. (Pubitemid 36776079)
23. Katz AR, Chasnoff R, Komeya A, Lee MV. 2011. Neisseria meningitidis urethritis: a case report highlighting clinical similarities to and epidemiological differences from gonococcal urethritis. Sex. Transm. Dis. 38:439-441.
24. Urra E, Alkorta M, Sota M, Alcala B, Martinez I, Barron J, Cisterna R. 2005. Orogenital transmission of Neisseria meningitidis serogroup C confirmed by genotyping techniques. Eur. J. Clin. Microbiol. Infect. Dis. 24: 51-53. (Pubitemid 40179133)
25. Unemo M, Golparian D, Potocnik M, Jeverica S. 2012. Treatment failure of pharyngeal gonorrhoea with internationally recommended first-line ceftriaxone verified in Slovenia, September 2011. Euro Surveill. 17(25): pii-20200. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20200.
26. Young H, Bain SS. 1983. Neisserial colonisation of the pharynx. Br. J. Vener. Dis. 59:228-231. (Pubitemid 13026242)
27. Bissessor M, Tabrizi SN, Fairley CK, Danielewski J, Whitton B, Bird S, Garland S, Chen MY. 2011. Differing Neisseria gonorrhoeae bacterial loads in the pharynx and rectum in men who have sex with men: implications for gonococcal detection, transmission, and control. J. Clin. Microbiol. 49:4304-4306.
28. Judson FN, Ehret JM, Eickhoff TC. 1978. Anogenital infection with Neisseria meningitidis in homosexual men. J. Infect. Dis. 137:458-463. (Pubitemid 8327259)
29. Quarto M, Barbuti S, Germinario C, Vena GA, Foti C. 1991. Urethritis caused by Neisseria meningitidis: a case report. Eur. J. Epidemiol. 7:699-701.
30. Hagman M, Danielsson D. 1989. Increased adherence to vaginal epithelial cells and phagocytic killing of gonococci and urogenital meningococci associated with heat modifiable proteins. APMIS 97:839-844. (Pubitemid 19242091)
31. Hagman M, Forslin L, Moi H, Danielsson D. 1991. Neisseria meningitidis in specimens from urogenital sites: is increased awareness necessary? Sex. Transm. Dis. 18:228-232.
32. Hodge DS, Ashton FE, Terro R, Ali AS. 1987. Organism resembling Neisseria gonorrhoeae and Neisseria meningitidis. J. Clin. Microbiol. 25: 1546-1547. (Pubitemid 17098738)
33. Vazquez JA, Berron S, O'Rourke M, Carpenter G, Feil E, Smith NH, Spratt BG. 1995. Interspecies recombination in nature: a meningococcus that has acquired a gonococcal PIB porin. Mol. Microbiol. 15:1001-1007.
34. Hanage WP, Fraser C, Spratt BG. 2005. Fuzzy species among recombinogenic bacteria. BMC Biol. 3:6. doi:10.1186/1741-7007-3-6. (Pubitemid 41534978)
35. Palmer HM, Mallinson H, Wood RL, Herring AJ. 2003. Evaluation of the specificities of five DNA amplification methods for the detection of Neisseria gonorrhoeae. J. Clin. Microbiol. 41:835-837. (Pubitemid 36184209)
36. Popovic T, Sacchi CT, Reeves MW, Whitney AM, Mayer LW, Noble CA, Ajello GW, Mostashari F, Bendana N, Lingappa J, Hajjeh R, Rosenstein NE. 2000. Neisseria meningitidis serogroup W135 isolates associated with the ET-37 complex. Emerg. Infect. Dis. 6:428-429. (Pubitemid 30643673)
37. Mayer LW, Reeves MW, Al-Hamdan N, Sacchi CT, Taha MK, Ajello GW, Schmink SE, Noble CA, Tondella ML, Whitney AM, Al-Mazrou Y, Al-Jefri M, Mishkhis A, Sabban S, Caugant DA, Lingappa J, Rosenstein NE, Popovic T. 2002. Outbreak of W135 meningococcal disease in 2000: not emergence of a new W135 strain but clonal expansion within the electrophoretic type-37 complex. J. Infect. Dis. 185:1596-1605. (Pubitemid 34587521)
38. Klappenbach JA, Dunbar JM, Schmidt TM. 2000. rRNA operon copy number reflects ecological strategies of bacteria. Appl. Environ. Microbiol. 66:1328-1333. (Pubitemid 30185597)
39. Klappenbach JA, Saxman PR, Cole JR, Schmidt TM. 2001. rrndb: the Ribosomal RNA Operon Copy Number Database. Nucleic Acids Res. 29: 181-184. (Pubitemid 32054441)
40. Turova TP. 2003. Copy number of ribosomal operons in prokaryotes and its effect on phylogenic analyses. Mikrobiologiia 72:437-452. (In Russian.)
41. Sacchi CT, Whitney AM, Reeves MW, Mayer LW, Popovic T. 2002. Sequence diversity of Neisseria meningitidis 16S rRNA genes and use of 16S rRNA gene sequencing as a molecular subtyping tool. J. Clin. Microbiol. 40:4520-4527. (Pubitemid 35434940)
42. Smith NH, Holmes EC, Donovan GM, Carpenter GA, Spratt BG. 1999. Networks and groups within the genus Neisseria: analysis of argF, recA, rho, and 16S rRNA sequences from human Neisseria species. Mol. Biol. Evol. 16:773-783. (Pubitemid 29260831)
43. Lowe P, O'Loughlin P, Evans K, White M, Bartley PB, Vohra R. 2006. Comparison of the Gen-Probe APTIMA Combo 2 assay to the AMPLICOR CT/NG assay for detection of Chlamydia trachomatis and Neisseria gonorrhoeae in urine samples from Australian men and women. J. Clin. Microbiol. 44:2619-2621. (Pubitemid 44092444)
44. Tabrizi SN, Unemo M, Limnios AE, Hogan TR, Hjelmevoll SO, Garland SM, Tapsall J. 2011. Evaluation of six commercial nucleic acid amplification tests for detection of Neisseria gonorrhoeae and other Neisseria species. J. Clin. Microbiol. 49:3610-3615.
45. Golparian D, Tabrizi SN, Unemo M. 2013. Analytical specificity and sensitivity of the APTIMA Combo 2 and APTIMA GC assays for detection of commensal Neisseria species and Neisseria gonorrhoeae on the Gen-Probe Panther instrument. Sex. Transm. Dis. 40:175-178.
46. Amann R, Snaidr J, Wagner M, Ludwig W, Schleifer KH. 1996. In situ visualization of high genetic diversity in a natural microbial community. J. Bacteriol. 178:3496-3500. (Pubitemid 26179053)
47. Amann RI, Krumholz L, Stahl DA. 1990. Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J. Bacteriol. 172:762-770. (Pubitemid 20070387)
48. Poppert S, Essig A, Stoehr B, Steingruber A, Wirths B, Juretschko S, Reischl U, Wellinghausen N. 2005. Rapid diagnosis of bacterial meningitis by real-time PCR and fluorescence in situ hybridization. J. Clin. Microbiol. 43:3390-3397. (Pubitemid 40981352)
49. Kanagawa T. 2003. Bias and artifacts in multitemplate polymerase chain reactions (PCR). J. Biosci. Bioeng. 96:317-323. (Pubitemid 37500201)
50. Keohavong P, Thilly WG. 1989. Fidelity of DNA polymerases in DNA amplification. Proc. Natl. Acad. Sci. U. S. A. 86:9253-9257. (Pubitemid 20010403)
51. Kurata S, Kanagawa T, Magariyama Y, Takatsu K, Yamada K, Yokomaku T, Kamagata Y. 2004. Reevaluation and reduction of a PCR bias caused by reannealing of templates. Appl. Environ. Microbiol. 70:7545-7549. (Pubitemid 39643822)
52. Qiu X, Wu L, Huang H, McDonel PE, Palumbo AV, Tiedje JM, Zhou J. 2001. Evaluation of PCR-generated chimeras, mutations, and heteroduplexes with 16S rRNA gene-based cloning. Appl. Environ. Microbiol. 67:880-887. (Pubitemid 32121383)
53. Speksnijder AG, Kowalchuk GA, De Jong S, Kline E, Stephen JR, Laanbroek HJ. 2001. Microvariation artifacts introduced by PCR and cloning of closely related 16S rRNA gene sequences. Appl. Environ. Microbiol. 67:469-472. (Pubitemid 32044454)
54. Hunt DE, Klepac-Ceraj V, Acinas SG, Gautier C, Bertilsson S, Polz MF. 2006. Evaluation of 23S rRNA PCR primers for use in phylogenetic studies of bacterial diversity. Appl. Environ. Microbiol. 72:2221-2225.
55. Ueda K, Seki T, Kudo T, Yoshida T, Kataoka M. 1999. Two distinct mechanisms cause heterogeneity of 16S rRNA. J. Bacteriol. 181:78-82. (Pubitemid 29013656)
56. Kulick S, Moccia C, Didelot X, Falush D, Kraft C, Suerbaum S. 2008. Mosaic DNA imports with interspersions of recipient sequence after natural transformation of Helicobacter pylori. PLoS One 3:e3797. doi:10.1371/journal. pone.0003797. (Pubitemid 352761156)
57. Cilia V, Lafay B, Christen R. 1996. Sequence heterogeneities among 16S ribosomal RNA sequences, and their effect on phylogenetic analyses at the species level. Mol. Biol. Evol. 13:451-461. (Pubitemid 26066097)
58. Harrington CS, On SL. 1999. Extensive 16S rRNA gene sequence diversity in Campylobacter hyointestinalis strains: taxonomic and applied implications. Int. J. Syst. Bacteriol. 49:1171-1175. (Pubitemid 29320769)
59. Ninet B, Monod M, Emler S, Pawlowski J, Metral C, Rohner P, Auckenthaler R, Hirschel B. 1996. Two different 16S rRNA genes in a mycobacterial strain. J. Clin. Microbiol. 34:2531-2536. (Pubitemid 26307807)
60. Reischl U, Feldmann K, Naumann L, Gaugler BJ, Ninet B, Hirschel B, Emler S. 1998. 16S rRNA sequence diversity in Mycobacterium celatum strains caused by presence of two different copies of 16S rRNA gene. J. Clin. Microbiol. 36:1761-1764. (Pubitemid 28226068)
61. Korch C, Drabkin H. 1999. Improved DNA sequencing accuracy and detection of heterozygous alleles using manganese citrate and different fluorescent dye terminators. Genome Res. 9:588-595. (Pubitemid 29361276)
62. Davidson CJ, Zeringer E, Champion KJ, Gauthier MP, Wang F, Boonyaratanakornkit J, Jones JR, Schreiber E. 2012. Improving the limit of detection for Sanger sequencing: a comparison of methodologies for KRAS variant detection. Biotechniques 53:182-188.
63. Joseph B, Schwarz RF, Linke B, Blom J, Becker A, Claus H, Goesmann A, Frosch M, Muller T, Vogel U, Schoen C. 2011. Virulence evolution of the human pathogen Neisseria meningitidis by recombination in the core and accessory genome. PLoS One 6:e18441. doi:10.1371/journal.pone. 0018441.
64. Schoen C, Weber-Lehmann J, Blom J, Joseph B, Goesmann A, Strittmatter A, Frosch M. 2011. Whole-genome sequence of the transformable Neisseria meningitidis serogroup A strain WUE2594. J. Bacteriol. 193: 2064-2065.
65. Ito M, Deguchi T, Mizutani KS, Yasuda M, Yokoi S, Ito S, Takahashi Y, Ishihara S, Kawamura Y, Ezaki T. 2005. Emergence and spread of Neisseria gonorrhoeae clinical isolates harboring mosaic-like structure of penicillin-binding protein 2 in central Japan. Antimicrob. Agents Chemother. 49:137-143. (Pubitemid 40065784)
66. Tapsall JW, Ray S, Limnios A. 2010. Characteristics and population dynamics of mosaic penA allele-containing Neisseria gonorrhoeae isolates collected in Sydney, Australia, in 2007-2008. Antimicrob. Agents Chemother. 54:554-556.
67. Maiden MC. 1993. Population genetics of a transformable bacterium: the influence of horizontal genetic exchange on the biology of Neisseria meningitidis. FEMS Microbiol. Lett. 112:243-250. (Pubitemid 23280690)
68. Rokbi B, Maitre-Wilmotte G, Mazarin V, Fourrichon L, Lissolo L, Quentin-Millet MJ. 1995. Variable sequences in a mosaic-like domain of meningococcal tbp2 encode immunoreactive epitopes. FEMS Microbiol. Lett. 132:277-283.
69. Taha MK. 2002. Molecular detection and characterization of Neisseria meningitidis. Expert Rev. Mol. Diagn. 2:143-150.
70. Hugenholtz P, Goebel BM, Pace NR. 1998. Impact of cultureindependent studies on the emerging phylogenetic view of bacterial diversity. J. Bacteriol. 180:4765-4774. (Pubitemid 28429361)
71. Rappe MS, Giovannoni SJ. 2003. The uncultured microbial majority. Annu. Rev. Microbiol. 57:369-394. (Pubitemid 37392948)
72. Viezens J, Arvand M. 2008. Simultaneous presence of two different copies of the 16S rRNA gene in Bartonella henselae. Microbiology 154:2881-2886.
73. Gonzalez-Escalona N, Romero J, Espejo RT. 2005. Polymorphism and gene conversion of the 16S rRNA genes in the multiple rRNA operons of Vibrio parahaemolyticus. FEMS Microbiol. Lett. 246:213-219. (Pubitemid 40724432)
74. Michon AL, Aujoulat F, Roudiere L, Soulier O, Zorgniotti I, Jumas-Bilak E, Marchandin H. 2010. Intragenomic and intraspecific heterogeneity in rrs may surpass interspecific variability in a natural population of Veillonella. Microbiology 156:2080-2091.