Whole-genome sequencing of bacterial sexually transmitted infections: Implications for clinicians

Current Opinion in Infectious Diseases

Volumn 26, Issue 1, 2013, Pages 90-98

  Seth Smith, Helena M B ^a   Thomson, Nicholas R ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

chlamydia; diagnosis; epidemiology; genomics; gonorrhoea; syphilis; typing

Indexed keywords

CEPHALOSPORIN DERIVATIVE; MACROLIDE; PENICILLIN DERIVATIVE; QUINOLINE DERIVED ANTIINFECTIVE AGENT; SULFONAMIDE; TETRACYCLINE;

ACTINOBACTERIA; ANTIBIOTIC RESISTANCE; BACTERIAL GENOME; BACTERIAL INFECTION; BACTERIAL STRAIN; CELL DAMAGE; CHLAMYDIA TRACHOMATIS; CHLAMYDIASIS; CYTOLOGY; DIAGNOSTIC PROCEDURE; EPITHELIAL SCARRING; FIRMICUTES; GENE SEQUENCE; GENITAL ULCER; GENOMICS; GONORRHEA; INCIDENCE; INFERTILITY; LYMPHOGRANULOMA VENEREUM; MALE HOMOSEXUAL; MOLECULAR EPIDEMIOLOGY; MOLLICUTES; MULTILOCUS SEQUENCE TYPING; NEISSERIA GONORRHOEAE; NONHUMAN; NUCLEIC ACID AMPLIFICATION; PATHOGENESIS; PELVIC INFLAMMATORY DISEASE; PHYLOGENY; PROCTITIS; PROTEOBACTERIA; REVIEW; SENSITIVITY AND SPECIFICITY; SEXUALLY TRANSMITTED DISEASE; SPIROCHETE; SYMPTOM; SYPHILIS; TREATMENT FAILURE; TREPONEMA PALLIDUM;

DRUG RESISTANCE, BACTERIAL; GENETIC VARIATION; GENOME, BACTERIAL; GENOME-WIDE ASSOCIATION STUDY; HUMANS; SEXUALLY TRANSMITTED DISEASES, BACTERIAL;

EID: 84871796566     PISSN: 09517375     EISSN: 14736527     Source Type: Journal    
DOI: 10.1097/QCO.0b013e32835c2159     Document Type: Review

References (84)

1. WHO. Global incidence and prevalence of selected curable sexually transmitted infections-2008. Geneva: World Health Organisation; 2012.
2. Health Protection Agency UK. Sexually transmitted infections in England, 2011. Vol. 6. UK: Health Protection Agency; 2012.
3. Prevention CfDCa. Sexually transmitted disease surveillance 2010. Atlanta, USA: U.S. Department of Health and Human Services; 2011.
4. Stephens RS, Kalman S, Lammel C, et al. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 1998; 282:754-759. (Pubitemid 28489390)
5. Thomson NR, Holden MT, Carder C, et al. Chlamydia trachomatis: genome sequence analysis of lymphogranuloma venereum isolates. Genome Res 2008; 18:161-171.
6. Unemo M, Seth-Smith HMB, Cutcliffe LT, et al. The Swedish new variant of Chlamydia trachomatis: genome sequence, morphology, cell tropism and phenotypic characterization. Microbiology 2010; 156:1394-1404.
7. Chung GT, Yoo JS, Oh HB, et al. Complete genome sequence of Neisseria gonorrhoeae NCCP11945. J Bacteriol 2008; 190:6035-6036.
8. Snyder LAS, Davies JK, Ryan CS, Saunders NJ. Comparative overview of the genomic and genetic differences between the pathogenic Neisseria strains and species. Plasmid 2005; 54:191-218. (Pubitemid 41501619)
9. Fraser CM, Norris SJ, Weinstock GM, et al. Complete genome sequence of Treponema pallidum, the syphilis spirochaete. Science 1998; 281:375-388. (Pubitemid 28340777)
10. WHO. GlobalWHOalliance for the elimination of blinding trachoma by 2020. In: Weekly Epidemiological Report. Vol. 17 (87). World Health Organisation; 2012. pp. 161-168.
11. Fournier PE, Raoult D. Prospects for the future using genomics and proteomics in clinical microbiology. Annu Rev Microbiol 2011; 65:169-188.
12. Catlin WB. Nutritional profiles of Neisseria gonorrhoeae, Neisseria meningitidis, and Neisseria lactamica in chemically defined media and the use of growth requirements for gonococcal typing. J Infect Dis 1973; 128:178-194.
13. Ho EL, Lukehart SA. Syphilis: using modern approaches to understand an old disease. J Clin Invest 2011; 121:4584-4592.
14. Carlson JH, Porcella SF, McClarty G, Caldwell HD. Comparative genomic analysis of Chlamydia trachomatis oculotropic and genitotropic strains. Infect Immun 2005; 73:6407-6418. (Pubitemid 41368802)
15. Read TD, Myers GS, Brunham RC, et al. Genome sequence of Chlamydophila caviae (Chlamydia psittaci GPIC): examining the role of niche-specific genes in the evolution of the Chlamydiaceae. Nucleic Acids Res 2003; 31:2134-2147. (Pubitemid 37442081)
16. Belland RJ, Scidmore MA, Crane DD, et al. Chlamydia trachomatis cytotoxicity associated with complete and partial cytotoxin genes. Proc Natl Acad Sci 2001; 98:13984-13989. (Pubitemid 33116010)
17. Carlson JH, Hughes S, Hogan D, et al. Polymorphisms in the Chlamydia trachomatis cytotoxin locus associated with ocular and genital isolates. Infect Immun 2004; 72:7063-7072. (Pubitemid 39552376)
18. Caldwell HD, Wood H, Crane D, et al. Polymorphisms in Chlamydia trachomatis tryptophan synthase genes differentiate between genital and ocular isolates. J Clin Invest 2003; 111:1757-1769. (Pubitemid 38057756)
19. McClarty G, Caldwell HD, Nelson DE. Chlamydial interferon gamma immune evasion influences infection tropism. Curr Opin Microbiol 2007; 10:47-51. (Pubitemid 46216874)
20. Harris SR, Clarke IN, Seth-Smith HMB, et al. Whole-genome analysis of diverse Chlamydia trachomatis strains identifies phylogenetic relationships masked by current clinical typing. Nat Genet 2012; 44:364-366.
21. Jeffrey BM, Suchland RJ, Quinn KL, et al. Genome sequencing of recent clinical Chlamydia trachomatis strains identifies loci associated with tissue tropism and regions of apparent recombination. Infect Immun 2010; 78:2544-2553.
22. Seth-Smith HMB, Harris SR, Persson K, et al. Co-evolution of genomes and plasmids within Chlamydia trachomatis and the emergence in Sweden of a new variant strain. BMC Genomics 2009; 10:239.
23. Joseph SJ, Didelot X, Rithschild J, et al. Population genomics of Chlamydia trachomatis: insights on drift, selection, recombination, and population structure. Mol Biol Evol 2012; 29:3933-3946.
24. Somboonna N, Wan R, Ojcius DM, et al. Hypervirulent Chlamydia trachomatis clinical strain is a recombinant between lymphogranuloma venereum (L(2)) and D lineages. Mol Biol Evol 2011; 2:e00045-e00011.
25. Chen C-C, Hsia K-C, Huang C-T, et al. Draft genome sequence of a dominant, multidrug-resistant Neisseria gonorrhoeae strain, TCDC-NG08107, from a sexual group at high risk of acquiring human immunodeficiency virus infection and syphilis. J Bacteriol 2011; 193:1788-1789.
26. Hess D, Wu A, Golparian D, et al. Genome sequencing of a Neisseria gonorrhoeae isolate of a successful international clone 2 with decreased susceptibility/resistance to extended-spectrum cephalosporins. Antimicrob Agents Chemother 2012; 56:5633-5641.
27. Sparling PF. Genetic transformation of Neisseria gonorrhoeae to streptomycin resistance. J Bacteriol 1966; 92:1364-1371.
28. Graves JF, Biswas GD, Sparling PF. Sequence-specific DNA uptake in transformation of Neisseria gonorrhoeae. J Bacteriol 1982; 152:1071-1077. (Pubitemid 13190410)
29. Biswas GD, Sox T, Blackman E, Sparling PF. Factors affecting genetic transformation of Neisseria gonorrhoeae. J Bacteriol 1977; 129:983-992. (Pubitemid 8043919)
30. Marri PR, Paniscus M, Weyand NJ, et al. Genome sequencing reveals widespread virulence gene exchange among human Neisseria species. PLoS One 2010; 5:e11835.
31. Smajs D, Norris SJ, Weinstock GM. Genetic diversity in Treponema pallidum: implications for pathogenesis, evolution and molecular diagnostics of syphilis and yaws. Infect Genet Evol 2011; 12:191-202.
32. Cejková D, Zobanikova M, Chen L, et al. Whole genome sequences of three Treponema pallidum ssp. pertenue strains: yaws and syphilis treponemes differ in less than 0.2% of the genome sequence. PLoS Negl Trop Dis 2012; 6:e1471.
33. Giacani L, Chattopadhyay S, Centurion-Lara A, et al. Footprint of positive selection in Treponema pallidum subsp. pallidum genome sequences suggest adaptive microevolution of the syphilis pathogen. PLoS Negl Trop Dis 2012; 6:e1698.
34. Giacani L, Jeffrey BM, Molini BJ, et al. Complete genome sequence and annotation of the Treponema pallidum subsp. pallidum Chicago strain. J Bacteriol 2010; 192:2545-2546.
35. Matejkova P, Strouhal M, Smajs D, et al. Complete genome sequenced of Treponema pallidum ssp. pallidum strain SS14 determined with oligonucleotide arrays. BMC Microbiol 2008; 8:76.
36. Mikalova L, Strouhal M, Cejkova D, et al. Genome analysis of Treponema pallidum subsp. pallidum and subsp. pertenue strains: most of the genetic differences are localised in six regions. PLoS One 2010; 5:e15713.
37. Centurion-Lara A, LaFond RE, Hevner K, et al. Gene conversion: a mechanism for generation of heterogeneity in the tprK gene of Treponema pallidum during infection. Mol Microbiol 2004; 52:1579-1596. (Pubitemid 38822670)
38. Pedersen LN, Herrman B, Moller JK. Typing Chlamydia trachomatis: from egg yolk to nanotechnology. FEMS Immunol Med Microbiol 2009; 55:120-130.
39. Thomson NR, Clarke IN. Chlamydia trachomatis: small genome, big challenges. Future Microbiol 2010; 5:555-561.
40. Unemo M, Dillon J-AR. Review and International Recommendation of methods for typing Neisseria gonorrhoeae isolates and their implications for improved knowledge of gonococcal epidemiology,treatment, and biology. Clin Microbiol Rev 2011; 24:447-458.
41. Dean D, Bruno WJ, Wan R, et al. Predicting phenotype and emerging strains among Chlamydia trachomatis infections. Emerg Infect Dis 2009; 15:1385-1394.
42. Maiden MCJ, Bygraves JA, Feil E, et al. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci 1998; 95:3140-3145. (Pubitemid 28135868)
43. Pannekoek Y, Morelli G, Kusecek B, et al. Multi locus sequence typing of Chlamydiales: clonal groupings within the obligate intracellular bacteria Chlamydia trachomatis. BMC Microbiol 2008; 8:42.
44. Viscidi RP, Demma JC. Genetic diversity of Neisseria gonorrhoeae housekeeping genes. J Clin Microbiol 2003; 41:197-204. (Pubitemid 36098576)
45. Ikryannikova LN, Shkarupeta MM, Shitikov EA, et al. Comparative evaluation of new typing schemes for urogenital Chlamydia trachomatis isolates. FEMS Immunol Med Microbiol 2010; 59:188-196.
46. Klint M, Fuxelius HH, Goldkuhl RR, et al. High-resolution genotyping of Chlamydia trachomatis strains by multilocus sequence analysis. J Clin Microbiol 2007; 45:1410-1414. (Pubitemid 46762391)
47. Martin IMC, Ison CA, Aanensen DM, et al. Rapid sequence-based identification of gonococcal transmission clusters in a large metropolitan area. J Infect Dis 2004; 189:1497-1505. (Pubitemid 38552358)
48. Peng R-R, Wang AL, Li J, et al. Molecular typing of Treponema pallidum: a systematic review and meta-analysis. PLoS Negl Trop Dis 2011; 5:e1273.
49. Pillay A, Liu H, Chen CY, et al. Molecular subtying of Treponema pallidum subspecies pallidum. Sex Transm Dis 1998; 25:408-414. (Pubitemid 28446748)
50. Millman K, Black CM, Johnson RE, Dean D. Population-based genetic and evolutionary analysis of Chlamydia trachomatis urogenital strain variation in the United States. J Bacteriol 2004; 186:2457-2465. (Pubitemid 38451850)
51. Gao X, Chen X-S, Yin Y-P, et al. Distribution study of Chlamydia trachomatis serovars among high-risk women in China performed using PCR-restriction fragment length polymorphism genotyping. J Clin Microbiol 2007; 45:1185-1189. (Pubitemid 46626483)
52. Van de Laar MJ, van Duynhoven YT, Fennema JS, et al. Differences in clinical manifestations of genital chlamydial infections related to serovars. Genitourin Med 1996; 72:261-265. (Pubitemid 26290725)
53. Machado ACS, Bandea CI, Alves MFC, et al. Distribution of Chlamydia trachomatis genovars among youths and adults in Brazil. J Med Microbiol 2010; 60:472-476.
54. Lysen M, Osterlund A, Rubin C-J, et al. Characterization of ompA genotypes by sequence analysis of DNA from all detected cases of Chlamydia trachomatis infections during 1 year of contact tracing in a Swedish County. J Clin Microbiol 2004; 42:1641-1647. (Pubitemid 38500810)
55. Van Duynhoven YT, Ossewaarde JM, Derksen-Nawrocki RP, et al. Chlamydia trachomatis genotypes: correlation with clinical manifestations of infection and patients' characteristics. Clin Infect Dis 1998; 26:314-322. (Pubitemid 28083940)
56. Croucher NJ, Harris SR, Fraser CM, et al. Rapid pneumococcal evolution in response to clinical interventions. Science 2011; 331:430-434.
57. Gardy JL, Johnston JC, Ho Sui SJ, et al. Whole-genome sequencing and social-network analysis of a tuberculosis outbreak. N Engl J Med 2011; 364:730-739.
58. Harris SR, Feil EJ, Holden MTG, et al. Evolution of MRSA during hospital transmission and intercontinental spread. Science 2010; 327:469-474.
59. Lewis T, Loman NJ, Bingle L, et al. High-throughput whole-genome sequencing to dissect the epidemiology of Acinetobacter baumannii isolates from a hospital outbreak. J Hosp Infect 2010; 75:37-41.
60. Mutreja A, Kim DW, Thomson NR, et al. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 2011; 477:462-465.
61. Ripa T, Nilsson P. A variant of Chlamydia trachomatis with deletion in cryptic plasmid: implications for use of PCR diagnostic tests. Euro Surveill 2006; 9:E061109.061102.
62. Eastick K, Winter A, Jamdar S. Identification of Neisseria gonorrhoeae isolates with a recombinant porA gene in Scotland, United Kingdom 2010 to 2011. Euro Surveill 2012; 17:20101.
63. Golparian D, Johansson E, Unemo M. Clinical Neisseria gonorrhoeae isolate with a N. meningitidis porA gene and no prolyliminopeptidase activity, Sweden, 2011-danger of false-negative genetic and culture diagnostic results. Euro Surveill 2012; 17:20102.
64. Whiley DM, Limnios A, Moon NJ, et al. False-negative results using Neisseria gonorrhoeae porA pseudogene PCR-a clinical gonococcal isolate with an N. meningitidis porA sequence, Australia. 2011; 16:2.
65. Unemo M, Shafer WM. Antibiotic resistance in Neisseria gonorrhoeae: origin, evolution and lessons learned for the future. Ann N Y Acad Sci 2011; 1230:E19-E28.
66. Lewis DA, Lukehart SA. Antimicrobial resistance in Neisseria gonorrhoeae and Treponema pallidum: evolution, therapeutic challenges and the need to strengthen global surveillance. Sex Transm Infect 2011; 87: ii39-ii43.
67. Fayemiwo SA, Muller EE, Gumede L, Lewis DA. Plasmid-mediated penicillin and tetracycline resistance among Neisseria gonorrhoeae isolates in South Africa: prevalence, detection and typing using a novel molecular assay. Sex Transm Dis 2011; 38:329-333.
68. Goire N, Sloots TP, Nissen MD, Whiley DM. Protocol for the molecular detection of antibiotic resistance mechanisms in Neisseria gonorrhoeae. Methods Mol Biol 2012; 903:319-328.
69. Kugelman G, Tapsall JW, Goire N, et al. Simple, rapid, and inexpensive detection of Neisseria gonorrhoeae resistance mechanisms using heatdenatured isolates and SYBR Green-based Real-Time PCR. Antimicrob Agents Chemother 2009; 53:4211-4216.
70. Matejkova P, Flasarova M, Zakoucka H, et al. Macrolide treatment failure in a case of secondary syphilis: a novel A2059G mutation in the 23S rRNA gene of Treponema pallidum subsp. pallidum. J Med Microbiol 2009; 58:832-836.
71. Stamm LV, Bergen HL. A point mutation associated with bacterial macrolide resistance is present in both 23S rRNA genes of an erythromycin-resistant Treponema pallidum clinical isolate. Antimicrob Agents Chemother 2000; 44:806-807. (Pubitemid 30117989)
72. Muller EE, Paz-Bailey G, Lewis DA. Macrolide resistance testing and molecular subtyping of Treponema pallidum strains from Southern Africa. Sex Transm Infect 2012; 88:470-474.
73. Wang Y, Kahane S, Cutcliffe LT, et al. Development of a transformation system for Chlamydia trachomatis: restoration of glycogen biosynthesis by acquisition of a plasmid shuttle vector. PLoS Pathog 2011; 7:e1002258.
74. DeMars R, Weinfurter J, Guex E, et al. Lateral gene transfer in vitro in the intracellular pathogen Chlamydia trachomatis. J Bacteriol 2007; 189:991-1003. (Pubitemid 46183874)
75. Suchland RJ, Sandoz KM, Jeffrey BM, et al. Horizontal transfer of tetracycline resistance among Chlamydia spp. in vitro. Antimicrob Agents Chemother 2009; 53:4604-4611.
76. Norris SJ, Cox DL, Weinstock GM. Biology of Treponema pallidum: correlation of functional activities with genome sequence data. J Mol Microbiol Biotechnol 2001; 3:37-62. (Pubitemid 32097934)
77. Didelot X, Bowden R, Wilson DJ, et al. Transforming clinical microbiology with bacterial genome sequencing. Nat Rev Genet 2012; 13:601-612.
78. Eyre DW, Golubchik T, Gordon NC, et al. A pilot study of rapid benchtop sequencing of Staphylococcus aureus and Clostridium difficile for outbreak detection and surveillance. BMJ Open 2012; 2:e001124.
79. Kö ser CU, Ellington MJ, Cartwright EJP, et al. Routine use of microbial whole genome sequencing in diagnostic and public health microbiology. PLoS Pathog 2012; 8:e1002824.
80. Kö ser CU, Holden MT, Ellington MJ, et al. Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med 2012; 366:2267-2275.
81. Pallen M, Loman N. Are diagnostic and public health bacteriology ready to become branches of genomic medicine? Genome Med 2011; 3:53.
82. Parkhill J, Wren BW. Bacterial epidemiology and biology-lessons from genome sequencing. Genome Biol 2011; 12:230.
83. Snitkin ES, Zelazny AM, Thomas PJ, et al. Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci Transl Med 2012; 4:148ra116.
84. Kari L, Goheen MM, Randall LB, et al. Generation of targetted Chlamydia trachomatis null mutants. Proc Natl Acad Sci 2011; 108: 7189-7193.