1887

Abstract

This study examined the sequences of the two rRNA () operons of pathogenic non-cultivable treponemes, comprising 11 strains of ssp. (TPA), five strains of ssp. (TPE), two strains of ssp. (TEN), a simian Fribourg-Blanc strain and a rabbit (TPc) strain. PCR was used to determine the type of 16S–23S ribosomal intergenic spacers in the operons from 30 clinical samples belonging to five different genotypes. When compared with the TPA strains, TPc Cuniculi A strain had a 17 bp deletion, and the TPE, TEN and Fribourg-Blanc isolates had a deletion of 33 bp. Other than these deletions, only 17 heterogeneous sites were found within the entire region (excluding the 16S–23S intergenic spacer region encoding tRNA-Ile or tRNA-Ala). The pattern of nucleotide changes in the operons corresponded to the classification of treponemal strains, whilst two different spacer patterns (Ile/Ala and Ala/Ile) appeared to be distributed randomly across species/subspecies classification, time and geographical source of the treponemal strains. It is suggested that the random distribution of tRNA genes is caused by reciprocal translocation between repetitive sequences mediated by a -like system.

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2013-02-01
2019-12-15
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References

  1. Acinas S. G. , Marcelino L. A. , Klepac-Ceraj V. , Polz M. F. . ( 2004; ). Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. . J Bacteriol 186:, 2629–2635. [CrossRef] [PubMed]
    [Google Scholar]
  2. Antón A. I. , Martínez-Murcia A. J. , Rodríguez-Valera F. . ( 1998; ). Sequence diversity in the 16S–23S intergenic spacer region (ISR) of the rRNA operons in representatives of the Escherichia coli ECOR collection. . J Mol Evol 47:, 62–72. [CrossRef] [PubMed]
    [Google Scholar]
  3. Baseman J. B. , Nichols J. C. , Rumpp J. W. , Hayes N. S. . ( 1974; ). Purification of Treponema pallidum from infected rabbit tissue: resolution into two treponemal populations. . Infect Immun 10:, 1062–1067.[PubMed]
    [Google Scholar]
  4. Bunikis J. , Garpmo U. , Tsao J. , Berglund J. , Fish D. , Barbour A. G. . ( 2004; ). Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe. . Microbiology 150:, 1741–1755. [CrossRef] [PubMed]
    [Google Scholar]
  5. Čejková D. , Zobaníková M. , Chen L. , Pospíšilová P. , Strouhal M. , Qin X. , Mikalová L. , Norris S. J. , Muzny D. M. . & other authors ( 2012; ). 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 6:, e1471. [CrossRef] [PubMed]
    [Google Scholar]
  6. Centurion-Lara A. , Castro C. , van Voorhis W. C. , Lukehart S. A. . ( 1996; ). Two 16S–23S ribosomal DNA intergenic regions in different Treponema pallidum subspecies contain tRNA genes. . FEMS Microbiol Lett 143:, 235–240. [CrossRef] [PubMed]
    [Google Scholar]
  7. Comstedt P. , Asokliene L. , Eliasson I. , Olsen B. , Wallensten A. , Bunikis J. , Bergström S. . ( 2009; ). Complex population structure of Lyme borreliosis group spirochete Borrelia garinii in subarctic Eurasia. . PLoS ONE 4:, e5841. [CrossRef] [PubMed]
    [Google Scholar]
  8. Condon C. , Philips J. , Fu Z. Y. , Squires C. , Squires C. L. . ( 1992; ). Comparison of the expression of the seven ribosomal RNA operons in Escherichia coli . . EMBO J 11:, 4175–4185.[PubMed]
    [Google Scholar]
  9. Darling A. E. , Miklós I. , Ragan M. A. . ( 2008; ). Dynamics of genome rearrangement in bacterial populations. . PLoS Genet 4:, e1000128. [CrossRef] [PubMed]
    [Google Scholar]
  10. de Vries M. C. , Siezen R. J. , Wijman J. G. , Zhao Y. , Kleerebezem M. , de Vos W. M. , Vaughan E. E. . ( 2006; ). Comparative and functional analysis of the rRNA-operons and their tRNA gene complement in different lactic acid bacteria. . Syst Appl Microbiol 29:, 358–367. [CrossRef] [PubMed]
    [Google Scholar]
  11. Flasarová M. , Šmajs D. , Matějková P. , Woznicová V. , Heroldová-Dvoráková M. , Votava M. . ( 2006; ). [Molecular detection and subtyping of Treponema pallidum subsp. pallidum in clinical specimens]. . Epidemiol Mikrobiol Imunol 55:, 105–111 (in Czech).[PubMed]
    [Google Scholar]
  12. Flasarová M. , Pospíšilová P. , Mikalová L. , Vališová Z. , Dastychová E. , Strnadel R. , Kuklová I. , Woznicová V. , Zákoucká H. , Šmajs D. . ( 2012; ). Sequencing-based molecular typing of Treponema pallidum strains in the Czech Republic: all identified genotypes are related to the sequence of the SS14 strain. . Acta Derm Venereol 92:, 669–674.[PubMed] [CrossRef]
    [Google Scholar]
  13. Fraser C. M. , Casjens S. , Huang W. M. , Sutton G. G. , Clayton R. , Lathigra R. , White O. , Ketchum K. A. , Dodson R. . & other authors ( 1997; ). Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi . . Nature 390:, 580–586. [CrossRef] [PubMed]
    [Google Scholar]
  14. Fraser C. M. , Norris S. J. , Weinstock G. M. , White O. , Sutton G. G. , Dodson R. , Gwinn M. , Hickey E. K. , Clayton R. . & other authors ( 1998; ). Complete genome sequence of Treponema pallidum, the syphilis spirochete. . Science 281:, 375–388. [CrossRef] [PubMed]
    [Google Scholar]
  15. Fribourg-Blanc A. , Mollaret H. H. . ( 1969; ). Natural treponematosis of the African primate. . Primates Med 3:, 113–121.[PubMed]
    [Google Scholar]
  16. Fukunaga M. , Okuzako N. , Mifuchi I. , Arimitsu Y. , Seki M. . ( 1992; ). Organization of the ribosomal RNA genes in Treponema phagedenis and Treponema pallidum . . Microbiol Immunol 36:, 161–167.[PubMed] [CrossRef]
    [Google Scholar]
  17. Gastinel P. , Vaisman A. , Hamelin A. , Dunoyer F. . ( 1963; ). [Study of a recently isolated strain of Treponema pertenue]. . Prophyl Sanit Morale 35:, 182–188 (in French).[PubMed]
    [Google Scholar]
  18. Giacani L. , Jeffrey B. M. , Molini B. J. , Le H. T. , Lukehart S. A. , Centurion-Lara A. , Rockey D. D. . ( 2010; ). Complete genome sequence and annotation of the Treponema pallidum subsp. pallidum Chicago strain. . J Bacteriol 192:, 2645–2646. [CrossRef] [PubMed]
    [Google Scholar]
  19. Giacani L. , Chattopadhyay S. , Centurion-Lara A. , Jeffrey B. M. , Le H. T. , Molini B. J. , Lukehart S. A. , Sokurenko E. V. , Rockey D. D. . ( 2012; ). Footprint of positive selection in Treponema pallidum subsp. pallidum genome sequences suggests adaptive microevolution of the syphilis pathogen. . PLoS Negl Trop Dis 6:, e1698. [CrossRef] [PubMed]
    [Google Scholar]
  20. Gürtler V. . ( 1999; ). The role of recombination and mutation in 16S–23S rDNA spacer rearrangements. . Gene 238:, 241–252. [CrossRef] [PubMed]
    [Google Scholar]
  21. Gürtler V. , Stanisich V. A. . ( 1996; ). New approaches to typing and identification of bacteria using the 16S–23S rDNA spacer region. . Microbiology 142:, 3–16. [CrossRef] [PubMed]
    [Google Scholar]
  22. Hanincová K. , Liveris D. , Sandigursky S. , Wormser G. P. , Schwartz I. . ( 2008; ). Borrelia burgdorferi sensu stricto is clonal in patients with early Lyme borreliosis. . Appl Environ Microbiol 74:, 5008–5014. [CrossRef] [PubMed]
    [Google Scholar]
  23. Hardy J. B. , Hardy P. H. , Oppenheimer E. H. , Ryan S. J. Jr , Sheff R. N. . ( 1970; ). Failure of penicillin in a newborn with congenital syphilis. . JAMA 212:, 1345–1349. [CrossRef] [PubMed]
    [Google Scholar]
  24. Harvey S. , Hill C. W. . ( 1990; ). Exchange of spacer regions between rRNA operons in Escherichia coli . . Genetics 125:, 683–690.[PubMed]
    [Google Scholar]
  25. Hashimoto J. G. , Stevenson B. S. , Schmidt T. M. . ( 2003; ). Rates and consequences of recombination between rRNA operons. . J Bacteriol 185:, 966–972. [CrossRef] [PubMed]
    [Google Scholar]
  26. Indra A. , Blaschitz M. , Kernbichler S. , Reischl U. , Wewalka G. , Allerberger F. . ( 2010; ). Mechanisms behind variation in the Clostridium difficile 16S–23S rRNA intergenic spacer region. . J Med Microbiol 59:, 1317–1323. [CrossRef] [PubMed]
    [Google Scholar]
  27. Kobayashi I. . ( 1992; ). Mechanisms for gene conversion and homologous recombination: the double-strand break repair model and the successive half crossing-over model. . Adv Biophys 28:, 81–133. [CrossRef] [PubMed]
    [Google Scholar]
  28. Lan R. T. , Reeves P. R. . ( 1998; ). Recombination between rRNA operons created most of the ribotype variation observed in the seventh pandemic clone of Vibrio cholerae . . Microbiology 144:, 1213–1221. [CrossRef] [PubMed]
    [Google Scholar]
  29. Lebuhn M. , Bathe S. , Achouak W. , Hartmann A. , Heulin T. , Schloter M. . ( 2006; ). Comparative sequence analysis of the internal transcribed spacer 1 of Ochrobactrum species. . Syst Appl Microbiol 29:, 265–275. [CrossRef] [PubMed]
    [Google Scholar]
  30. Liao D. . ( 2000; ). Gene conversion drives within genic sequences: concerted evolution of ribosomal RNA genes in bacteria and archaea. . J Mol Evol 51:, 305–317.[PubMed]
    [Google Scholar]
  31. Liska S. L. , Perine P. L. , Hunter E. F. , Crawford J. A. , Feeley J. C. . ( 1982; ). Isolation and transportation of Treponema pertenue in golden hamsters. . Curr Microbiol 7:, 41–43. [CrossRef]
    [Google Scholar]
  32. Liu H. , Rodes B. , Chen C.-Y. , Steiner B. . ( 2001; ). New tests for syphilis: rational design of a PCR method for detection of Treponema pallidum in clinical specimens using unique regions of the DNA polymerase I gene. . J Clin Microbiol 39:, 1941–1946. [CrossRef] [PubMed]
    [Google Scholar]
  33. Liveris D. , Wormser G. P. , Nowakowski J. , Nadelman R. , Bittker S. , Cooper D. , Varde S. , Moy F. H. , Forseter G. . & other authors ( 1996; ). Molecular typing of Borrelia burgdorferi from Lyme disease patients by PCR-restriction fragment length polymorphism analysis. . J Clin Microbiol 34:, 1306–1309.[PubMed]
    [Google Scholar]
  34. Martin D. P. , Lemey P. , Lott M. , Moulton V. , Posada D. , Lefeuvre P. . ( 2010; ). rdp3: a flexible and fast computer program for analyzing recombination. . Bioinformatics 26:, 2462–2463. [CrossRef] [PubMed]
    [Google Scholar]
  35. Matějková P. , Strouhal M. , Šmajs D. , Norris S. J. , Palzkill T. , Petrosino J. F. , Sodergren E. , Norton J. E. , Singh J. . & other authors ( 2008; ). Complete genome sequence of Treponema pallidum ssp. pallidum strain SS14 determined with oligonucleotide arrays. . BMC Microbiol 8:, 76. [CrossRef] [PubMed]
    [Google Scholar]
  36. Matějková P. , Flasarová M. , Zákoucká H. , Boˇrek M. , Kremenová S. , Arenberger P. , Woznicová V. , Weinstock G. M. , Šmajs D. . ( 2009; ). 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 58:, 832–836. [CrossRef] [PubMed]
    [Google Scholar]
  37. Nei M. , Rooney A. P. . ( 2005; ). Concerted and birth-and-death evolution of multigene families. . Annu Rev Genet 39:, 121–152. [CrossRef] [PubMed]
    [Google Scholar]
  38. Nichols H. J. , Hough W. H. . ( 1913; ). Demonstration of Spirochaeta pallida in the cerebrospinal fluid: from a patient with nervous relapse following the use of salvarsan. . JAMA 60:, 108–110. [CrossRef]
    [Google Scholar]
  39. Pei A. , Nossa C. W. , Chokshi P. , Blaser M. J. , Yang L. , Rosmarin D. M. , Pei Z. . ( 2009; ). Diversity of 23S rRNA genes within individual prokaryotic genomes. . PLoS ONE 4:, e5437. [CrossRef] [PubMed]
    [Google Scholar]
  40. Pei A. Y. , Oberdorf W. E. , Nossa C. W. , Agarwal A. , Chokshi P. , Gerz E. A. , Jin Z. , Lee P. , Yang L. . & other authors ( 2010; ). Diversity of 16S rRNA genes within individual prokaryotic genomes. . Appl Environ Microbiol 76:, 3886–3897. [CrossRef] [PubMed]
    [Google Scholar]
  41. Petes T. D. , Hill C. W. . ( 1988; ). Recombination between repeated genes in microorganisms. . Annu Rev Genet 22:, 147–168. [CrossRef] [PubMed]
    [Google Scholar]
  42. Petit M.-A. . ( 2005; ). Mechanisms of homologous recombination in bacteria. . In The Dynamic Bacterial Genome, pp. 3–32. Edited by Mullany P. . . New York:: Cambridge University Press;. [CrossRef]
    [Google Scholar]
  43. Pillay A. , Liu H. , Chen C.-Y. , Holloway B. , Sturm A. W. , Steiner B. , Morse S. A. . ( 1998; ). Molecular subtyping of Treponema pallidum subspecies pallidum . . Sex Transm Dis 25:, 408–414. [CrossRef] [PubMed]
    [Google Scholar]
  44. Posada D. , Crandall K. A. . ( 2001; ). Evaluation of methods for detecting recombination from DNA sequences: computer simulations. . Proc Natl Acad Sci U S A 98:, 13757–13762. [CrossRef] [PubMed]
    [Google Scholar]
  45. Rozen S. , Skaletsky H. . ( 2000; ). Primer3 on the WWW for general users and for biologist programmers. . Methods Mol Biol 132:, 365–386.[PubMed]
    [Google Scholar]
  46. Sadeghifard N. , Gürtler V. , Beer M. , Seviour R. J. . ( 2006; ). The mosaic nature of intergenic 16S–23S rRNA spacer regions suggests rRNA operon copy number variation in Clostridium difficile strains. . Appl Environ Microbiol 72:, 7311–7323. [CrossRef] [PubMed]
    [Google Scholar]
  47. Saitou N. , Nei M. . ( 1987; ). The neighbor-joining method: a new method for reconstructing phylogenetic trees. . Mol Biol Evol 4:, 406–425.[PubMed]
    [Google Scholar]
  48. Santoyo G. , Romero D. . ( 2005; ). Gene conversion and concerted evolution in bacterial genomes. . FEMS Microbiol Rev 29:, 169–183.[PubMed]
    [Google Scholar]
  49. Sawyer S. . ( 1989; ). Statistical tests for detecting gene conversion. . Mol Biol Evol 6:, 526–538.[PubMed]
    [Google Scholar]
  50. Schwartz J. J. , Gazumyan A. , Schwartz I. . ( 1992; ). rRNA gene organization in the Lyme disease spirochete, Borrelia burgdorferi . . J Bacteriol 174:, 3757–3765.[PubMed]
    [Google Scholar]
  51. Seshadri R. , Myers G. S. , Tettelin H. , Eisen J. A. , Heidelberg J. F. , Dodson R. J. , Davidsen T. M. , DeBoy R. T. , Fouts D. E. . & other authors ( 2004; ). Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. . Proc Natl Acad Sci U S A 101:, 5646–5651. [CrossRef] [PubMed]
    [Google Scholar]
  52. Šmajs D. , Mikalová L. , Čejková D. , Strouhal M. , Zobaníková M. , Pospisilova P. , Norris S. J. , Weinstock G. M. . ( 2011a; ). Whole genome analyses of treponemes: new targets for strain- and subspecies-specific molecular diagnostics. . In Syphilis – Recognition, Description and Diagnosis, pp. 19–34. Edited by Sato N. S. . . Rijeka, Croatia:: InTech;. [CrossRef]
    [Google Scholar]
  53. Šmajs D. , Zobaníková M. , Strouhal M. , Čejková D. , Dugan-Rocha S. , Pospís˜ilová P. , Norris S. J. , Albert T. , Qin X. . & other authors ( 2011b; ). Complete genome sequence of Treponema paraluiscuniculi, strain Cuniculi A: the loss of infectivity to humans is associated with genome decay. . PLoS ONE 6:, e20415. [CrossRef] [PubMed]
    [Google Scholar]
  54. Smith J. M. . ( 1992; ). Analyzing the mosaic structure of genes. . J Mol Evol 34:, 126–129. [CrossRef] [PubMed]
    [Google Scholar]
  55. Stamm L. V. , Bergen H. L. . ( 2000; ). 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 44:, 806–807. [CrossRef] [PubMed]
    [Google Scholar]
  56. Stamm L. V. , Kerner T. C. Jr , Bankaitis V. A. , Bassford P. J. Jr . ( 1983; ). Identification and preliminary characterization of Treponema pallidum protein antigens expressed in Escherichia coli . . Infect Immun 41:, 709–721.[PubMed]
    [Google Scholar]
  57. Stamm L. V. , Bergen H. L. , Walker R. L. . ( 2002; ). Molecular typing of papillomatous digital dermatitis-associated Treponema isolates based on analysis of 16S–23S ribosomal DNA intergenic spacer regions. . J Clin Microbiol 40:, 3463–3469. [CrossRef] [PubMed]
    [Google Scholar]
  58. Stewart F. J. , Cavanaugh C. M. . ( 2007; ). Intragenomic variation and evolution of the internal transcribed spacer of the rRNA operon in bacteria. . J Mol Evol 65:, 44–67. [CrossRef] [PubMed]
    [Google Scholar]
  59. Strouhal M. , Šmajs D. , Matějková P. , Sodergren E. , Amin A. G. , Howell J. K. , Norris S. J. , Weinstock G. M. . ( 2007; ). Genome differences between Treponema pallidum subsp. pallidum strain Nichols and T. paraluiscuniculi strain Cuniculi A. . Infect Immun 75:, 5859–5866. [CrossRef] [PubMed]
    [Google Scholar]
  60. Takahashi N. K. , Yamamoto K. , Kitamura Y. , Luo S.-Q. , Yoshikura H. , Kobayashi I. . ( 1992; ). Nonconservative recombination in Escherichia coli . . Proc Natl Acad Sci U S A 89:, 5912–5916. [CrossRef] [PubMed]
    [Google Scholar]
  61. Tamura K. , Dudley J. , Nei M. , Kumar S. . ( 2007; ). mega4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. . Mol Biol Evol 24:, 1596–1599. [CrossRef] [PubMed]
    [Google Scholar]
  62. Turner T. B. , Hollander D. H. . ( 1957; ). Biology of the treponematoses based on studies carried out at the International Treponematosis Laboratory Center of the Johns Hopkins University under the auspices of the World Health Organization. . Monogr Ser World Health Organ 35:, 3–266.[PubMed]
    [Google Scholar]
  63. Wendel G. D. Jr , Sánchez P. J. , Peters M. T. , Harstad T. W. , Potter L. L. , Norgard M. V. . ( 1991; ). Identification of Treponema pallidum in amniotic fluid and fetal blood from pregnancies complicated by congenital syphilis. . Obstet Gynecol 78:, 890–895.[PubMed]
    [Google Scholar]
  64. Wormser G. P. , Brisson D. , Liveris D. , Hanincová K. , Sandigursky S. , Nowakowski J. , Nadelman R. B. , Ludin S. , Schwartz I. . ( 2008; ). Borrelia burgdorferi genotype predicts the capacity for hematogenous dissemination during early Lyme disease. . J Infect Dis 198:, 1358–1364. [CrossRef] [PubMed]
    [Google Scholar]
  65. Woznicová V. , Šmajs D. , Wechsler D. , Matějková P. , Flasarová M. . ( 2007; ). Detection of Treponema pallidum subsp. pallidum from skin lesions, serum, and cerebrospinal fluid in an infant with congenital syphilis after clindamycin treatment of the mother during pregnancy. . J Clin Microbiol 45:, 659–661. [CrossRef] [PubMed]
    [Google Scholar]
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