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Volume 154, Issue 3

Clonal population structure of inferred from allelic profiling Free

Abstract

The population structure of was investigated by analysing nucleotide sequences from six loci (, , , , and ) of 335 globally distributed isolates from clinical and environmental sources over a 29-year period (1977–2006). Data were obtained from unrelated isolates from Europe (=270), Japan (=31), Canada (=7), the USA (=24) and Australia (=1). The country of origin of two strains was unknown. Analysis of these isolates indicated significant linkage disequilibrium between the six loci. Application of six sequence-based recombination detection tests did not reveal evidence of recombination, but estimates of rates of recombination and mutation made by a seventh test suggested that recombination could have occurred at a rate similar to, but probably lower than, that of mutation. Genealogies inferred under models with and without recombination were congruent with each other, providing no definitive evidence regarding recombination, and were in agreement with sequence clusters identified by graph methods. Further evidence supporting the distinct nature of two of the three subspecies of , subsp. and subsp. , was also found. The ratios of non-synonymous to synonymous nucleotide polymorphisms for each of the allele sets were examined and revealed that the putative virulence loci and are under diversifying pressure, while the allelic regions of three other loci linked to virulence ( and ) do not appear to be.

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  • Accepted:
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  • Published Online:
Keyword(s): BK, Bron–Kerbosch , EWGLI, European Working Group for Legionella Infections , MLST, multi-locus sequence typing , MST, minimum spanning tree , SBT, sequence-based typing and SLV, single-locus variant
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References

  1. Amemura-Maekawa J., Kura F., Chang B., Watanabe H. 2005; Legionella pneumophila serogroup 1 isolates from cooling towers in Japan form a distinct genetic cluster. Microbiol Immunol 49:1027–1033
     [Google Scholar]
  2. Benson R. F., Lucas C. E., Brown E. W., Cowgill K. D., Fields B. S. 2006; Molecular comparison of isolates from a recurring outbreak of Legionnaires' disease spanning 22 years. Chapter 37 in Legionella: State of the Art 30 Years after Its Recognition pp 139–145 Edited by Cianciotto N. P., Kwaik Y. Abu, Edelstein P. H., Fields B. S., Geary D. F., Harrison T. G., Joseph C. A., Ratcliff R. M., Stout J. E., Swanson M. S. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  3. Berman H. M., Westbrook J., Feng Z., Gilliland G., Bhat T. N., Weissig H., Shindyalov I. N., Bourne P. E. 2000; The Protein Data Bank. Nucleic Acids Res 28:235–242
     [Google Scholar]
  4. Bernander S., Claesson B. E. B., Hjelm E., Svensson N., Hjorth M. 2006; Serologic study of an outbreak of Legionnaires' disease: variation of sensitivity associated with the subgroup of Legionella pneumophila sg 1 antigen used and evidence of concurrent reactivity to other atypical pneumonia agents. Chapter 17 in Legionella: State of the Art 30 Years after Its Recognition pp 63–67 Edited by Cianciotto N. P., Kwaik Y. Abu, Edelstein P. H., Fields B. S., Geary D. F., Harrison T. G., Joseph C. A., Ratcliff R. M., Stout J. E., Swanson M. S. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  5. Black W. J., Quinn F. D., Tompkins L. S. 1990; Legionella pneumophila zinc metalloprotease is structurally and functionally homologous to Pseudomonas aeruginosa elastase. J Bacteriol 172:2608–2613
     [Google Scholar]
  6. Brenner D. J., Steigerwalt A. G., Epple P., Bibb W. F., McKinney R. M., Starnes R. W., Colville J. M., Selander R. K., Edelstein P. H., Moss C. W. 1988; Legionella pneumophila serogroup Lansing 3 isolated from a patient with fatal pneumonia, and descriptions of L.pneumophila subsp. pneumophila subsp. nov., L. pneumophila subsp. fraseri subsp. nov., and L. pneumophila subsp. pascullei subsp. nov. J Clin Microbiol 26:1695–1703
     [Google Scholar]
  7. Bron C., Kerbosch J. 1973; Finding all cliques of an undirected graph. Commun ACM 16:575–577
     [Google Scholar]
  8. Bumbaugh A. C., McGraw E. A., Page K. L., Selander R. K., Whittam T. S. 2002; Sequence polymorphism of dotA and mip alleles mediating invasion and intracellular replication of Legionella pneumophila . Curr Microbiol 44:314–322
     [Google Scholar]
  9. Cianciotto N. P., Fields B. S. 1992; Legionella pneumophila mip gene potentiates intracellular infection of protozoa and human macrophages. Proc Natl Acad Sci U S A 89:5188–5191
     [Google Scholar]
  10. Cohan F. M., Perry E. B. 2007; A systematics for discovering the fundamental units of bacterial diversity. Curr Biol 17:R373–R386
     [Google Scholar]
  11. Cohan F. M., Koeppel A., Krizanc D. 2006; Sequence-based discovery of ecological diversity within Legionella . Chapter 88 in Legionella: State of the Art 30 Years after Its Recognition pp 367–376 Edited by Cianciotto N. P., Kwaik Y. Abu, Edelstein P. H., Fields B. S., Geary D. F., Harrison T. G., Joseph C. A., Ratcliff R. M., Stout J. E., Swanson M. S. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  12. Coscollá M., González-Candelas F. 2007; Population structure and recombination in environmental isolates of Legionella pneumophila . Environ Microbiol 9:643–656
     [Google Scholar]
  13. Coscollá M., Gosalbes M. J., Catalan V., González-Candelas F. 2006; Genetic variability in environmental isolates of Legionella pneumophila from Comunidad Valenciana (Spain. Environ Microbiol 8:1056–1063
     [Google Scholar]
  14. Didelot X., Falush D. 2007; Inference of bacterial microevolution using multilocus sequence data. Genetics 175:1251–1266
     [Google Scholar]
  15. Dreyfus L. A., Iglewski B. H. 1986; Purification and characterization of an extracellular protease of Legionella pneumophila . Infect Immun 51:736–743
     [Google Scholar]
  16. Edelstein P. H., Nakahama C., Tobin J. O., Calarco K., Beer K. B., Joly J. R., Selander R. K. 1986; Paleoepidemiologic investigation of Legionnaires' disease at Wadsworth Veterans Administration Hospital by using three typing methods for comparison of legionellae from clinical and environmental sources. J Clin Microbiol 23:1121–1126
     [Google Scholar]
  17. Ehret W., Ruckdeschel G. 1985; Molecular weight of the major outer membrane protein of Legionella pneumophila . Eur J Clin Microbiol 4:592–593
     [Google Scholar]
  18. Engleberg N. C., Carter C., Weber D. R., Cianciotto N. P., Eisenstein B. I. 1989; DNA sequence of mip , a Legionella pneumophila gene associated with macrophage infectivity. Infect Immun 57:1263–1270
     [Google Scholar]
  19. Enright M. C., Spratt B. G. 1998; A multilocus sequence typing scheme for Streptococcus pneumoniae : identification of clones associated with serious invasive disease. Microbiology 144:3049–3060
     [Google Scholar]
  20. Feil E. J., Li B. C., Aanensen D. M., Hanage W. P., Spratt B. G. 2004; eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 186:1518–1530
     [Google Scholar]
  21. Fendukly F., Bernander S., Hanson H.-S. 2007; Nosocomial Legionnaires' disease caused by Legionella pneumophila serogroup 6: implication of the sequence-based typing method (SBT. Scand J Infect Dis 39:213–216
     [Google Scholar]
  22. Fischer G., Bang H., Ludwig B., Mann K., Hacker J. 1992; Mip protein of Legionella pneumophila exhibits peptidyl-prolyl- cis / trans isomerase (PPIase) activity. Mol Microbiol 6:1375–1383
     [Google Scholar]
  23. Fry N. K., Alexiou-Daniel S., Bangsborg J. M., Bernander S., Castellani Pastoris M., Etienne J., Forsblom B., Gaia V., Helbig J. H. other authors 1999; A multicenter evaluation of genotypic methods for the epidemiological typing of Legionella pneumophila serogroup 1: results of a pan-European study. Clin Microbiol Infect 5:462–477
     [Google Scholar]
  24. Fry N. K., Bangsborg J. M., Bernander S., Etienne J., Forsblom B., Gaia V., Hasenberger P., Lindsay D., Papoutsi A. other authors 2000; Assessment of intercentre reproducibility and epidemiological concordance of Legionella pneumophila serogroup 1 genotyping by amplified fragment length polymorphism analysis. Eur J Clin Microbiol Infect Dis 19:773–780
     [Google Scholar]
  25. Fry N. K., Bangsborg J. M., Bergmans A., Bernander S., Etienne J., Franzin L., Gaia V., Hasenberger P., Baladrón Jiménez B. other authors 2002; Designation of the European Working Group on Legionella Infection (EWGLI) amplified fragment length polymorphism types of Legionella pneumophila serogroup 1 and results of intercentre proficiency testing using a standard protocol. Eur J Clin Microbiol Infect Dis 21:722–728
     [Google Scholar]
  26. Gaia V., Fry N. K., Harrison T. G., Peduzzi R. 2003; Sequence-based typing of Legionella pneumophila serogroup 1 offers the potential for true portability in legionellosis outbreak investigation. J Clin Microbiol 41:2932–2939
     [Google Scholar]
  27. Gaia V., Fry N. K., Afshar B., Lück P. C., Meugnier H., Etienne J., Peduzzi R., Harrison T. G. 2005; Consensus sequence-based scheme for epidemiological typing of clinical and environmental isolates of Legionella pneumophila . J Clin Microbiol 43:2047–2052
     [Google Scholar]
  28. Gibbs M. J., Armstrong J. S., Gibbs A. J. 2000; Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16:573–582
     [Google Scholar]
  29. Gilmour M. W., Bernard K., Tracz D. M., Olson A. B., Corbett C. R., Burdz T., Ng B., Wiebe D., Broukhanski G. other authors 2007; Molecular typing of a Legionella pneumophila outbreak in Ontario, Canada. J Med Microbiol 56:336–341
     [Google Scholar]
  30. Giske C. G., Libisch B., Colinon C., Scoulica E., Pagani L., Füzi M., Kronvall G., Rossolini G. M. 2006; Establishing clonal relationships between VIM-1-like metallo- β -lactamase-producing Pseudomonas aeruginosa strains from four European countries by multilocus sequence typing. J Clin Microbiol 44:4309–4315
     [Google Scholar]
  31. Harb O. S., Abu Kwaik Y. 1998; Identification of the aspartate- β -semialdehyde dehydrogenase gene of Legionella pneumophila and characterization of a null mutant. Infect Immun 66:1898–1903
     [Google Scholar]
  32. Harrison T. G., Fry N. K., Afshar B., Bellamy W., Doshi N., Underwood A. P. 2006; Typing of Legionella pneumophila and its role in elucidating the epidemiology of Legionnaires' Disease. Chapter 25 in Legionella: State of the Art 30 Years after Its Recognition pp 94–99 Edited by Cianciotto N. P., Kwaik Y. Abu, Edelstein P. H., Fields B. S., Geary D. F., Harrison T. G., Joseph C. A., Ratcliff R. M., Stout J. E., Swanson M. S. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  33. Haubold B., Hudson R. R. 2000; LIAN 3.0: detecting linkage disequilibrium in multilocus data. Bioinformatics 16:847–848
     [Google Scholar]
  34. Heuner K., Bender-Beck L., Brand B. C., Lück P. C., Mann K.-H., Marre R., Ott M., Hacker J. 1995; Cloning and genetic characterization of the flagellum subunit gene ( flaA ) of Legionella pneumophila serogroup 1. Infect Immun 63:2499–2507
     [Google Scholar]
  35. Hoffman P. S., Houston L., Butler C. A. 1990; Legionella pneumophila htpAB heat shock operon: nucleotide sequence and expression of the 60-kilodalton antigen in L. pneumophila -infected HeLa cells. Infect Immun 58:3380–3387
     [Google Scholar]
  36. Hudson R. R. 1994; Analytical results concerning linkage disequilibrium in models with genetic transformation and conjugation. J Evol Biol 7:535–548
     [Google Scholar]
  37. Jolley K. A., Feil E. J., Chan M.-S., Maiden M. C. J. 2001; Sequence type analysis and recombinational tests (START. Bioinformatics 17:1230–1231
     [Google Scholar]
  38. Ko K. S., Hong S. K., Lee H. K., Park M.-Y., Kook Y.-H. 2003; Molecular evolution of the dotA gene in Legionella pneumophila . J Bacteriol 185:6269–6277
     [Google Scholar]
  39. Kruskal J. B. 1956; On the shortest spanning sub-tree of a graph and travelling salesman problem. Proc Am Math Soc 7:48–50
     [Google Scholar]
  40. Maiden M. C., Bygraves J. A., Feil E., Morelli G., Russell J. E., Urwin R., Zhang Q., Zhou J., Zurth K. other authors 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
     [Google Scholar]
  41. Marchler-Bauer A., Anderson J. B., Cherukuri P. F., DeWeese-Scott C., Geer L. Y., Gwadz M., He S., Hurwitz D. I., Jackson J. D. other authors 2005; CDD: a Conserved Domain Database for protein classification. Nucleic Acids Res 33:D192–D196
     [Google Scholar]
  42. Martin D., Rybicki E. 2000; RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563
     [Google Scholar]
  43. McDade J. E., Shepard C. C., Fraser D. W., Tsai T. R., Redus M. A., Dowdle W. R. 1977; Legionnaires' disease: isolation of a bacterium and demonstration of its role in other respiratory disease. N Engl J Med 297:1197–1203
     [Google Scholar]
  44. McVean G., Awadalla P., Fearnhead P. 2002; A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160:1231–1241
     [Google Scholar]
  45. Mengaud J. M., Horwitz M. A. 1993; The major iron-containing protein of Legionella pneumophila is an aconitase homologous with the human iron-responsive element-binding protein. J Bacteriol 175:5666–5676
     [Google Scholar]
  46. Moffat J. F., Edelstein P. H., Regula D. P., Cirillo J. D., Tompkins L. S. 1994; Effects of an isogenic Zn-metalloprotease-deficient mutant of Legionella pneumophila in a guinea-pig pneumonia model. Mol Microbiol 12:693–705
     [Google Scholar]
  47. Molofsky A. B., Shetron-Rama L. M., Swanson M. S. 2005; Components of the Legionella pneumophila flagellar regulon contribute to multiple virulence traits, including lysosome avoidance and macrophage death. Infect Immun 73:5720–5734
     [Google Scholar]
  48. Nei M., Gojobori T. 1986; Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426
     [Google Scholar]
  49. Padidam M., Sawyer S., Fauquet C. M. 1999; Possible emergence of new geminiviruses by frequent recombination. Virology 265:218–225
     [Google Scholar]
  50. Paraskevopoulos C., Bordenstein S. R., Wernegreen J. J., Werren J. H., Bourtzis K. 2006; Toward a Wolbachia multilocus sequence typing system: discrimination of Wolbachia strains present in Drosophila species. Curr Microbiol 53:388–395
     [Google Scholar]
  51. 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
     [Google Scholar]
  52. Ratzow S., Gaia V., Helbig J. H., Fry N. K., Lück P. C. 2007; Addition of neuA , the gene encoding N -acylneuraminate cytidylyl transferase, increases the discriminatory ability of the consensus sequence-based scheme for typing Legionella pneumophila serogroup 1 strains. J Clin Microbiol 45:1965–1968
     [Google Scholar]
  53. Ruiz-Garbajosa P., Bonten M. J. M., Robinson D. A., Top J., Nallapareddy S. R., Torres C., Coque T. M., Cantón R., Baquero F. other authors 2006; Multilocus sequence typing scheme for Enterococcus faecalis reveals hospital-adapted genetic complexes in a background of high rates of recombination. J Clin Microbiol 44:2220–2228
     [Google Scholar]
  54. Salminen M. O., Carr J. K., Burke D. S., McCutchan F. E. 1995; Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res Hum Retroviruses 11:1423–1425
     [Google Scholar]
  55. Sampson J. S., O'Connor S. P., Holloway B. P., Plikaytis B. B., Carlone G. M., Mayer L. W. 1990; Nucleotide sequence of htpB , the Legionella pneumophila gene encoding the 58-kilodalton (kDa) common antigen, formerly designated the 60-kDa common antigen. Infect Immun 58:3154–3157
     [Google Scholar]
  56. Saunders N. A., Harrison T. G., Haththotuwa A., Kachwalla N., Taylor A. G. 1990; A method for typing strains of Legionella pneumophila serogroup 1 by analysis of restriction fragment length polymorphisms. J Med Microbiol 31:45–55
     [Google Scholar]
  57. Scaturro M., Losardo M., De Ponte G., Ricci M. L. 2005; Comparison of three molecular methods used for subtyping of Legionella pneumophila strains isolated during an epidemic of legionellosis in Rome. J Clin Microbiol 43:5348–5350
     [Google Scholar]
  58. Schmidt H. A., Strimmer K., Vingron M., von Haeseler A. 2002; tree-puzzle: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504
     [Google Scholar]
  59. Schoonmaker D., Heimberger T., Birkhead G. 1992; Comparison of ribotyping and restriction enzyme analysis using pulsed-field gel electrophoresis for distinguishing Legionella pneumophila isolates obtained during a nosocomial outbreak. J Clin Microbiol 30:1491–1498
     [Google Scholar]
  60. Selander R. K., McKinney R. M., Whittam T. S., Bibb W. F., Brenner D. J., Nolte F. S., Pattison P. E. 1985; Genetic structure of populations of Legionella pneumophila . J Bacteriol 163:1021–1037
     [Google Scholar]
  61. Smith J. M. 1992; Analyzing the mosaic structure of genes. J Mol Evol 34:126–129
     [Google Scholar]
  62. Smith J. M., Smith N. H., O'Rourke M., Spratt B. G. 1993; How clonal are bacteria?. Proc Natl Acad Sci U S A 90:4384–4388
     [Google Scholar]
  63. Stern A., Doron-Faigenboim A., Erez E., Martz E., Bacharach E., Pupko T. 2007; Selecton 2007: advanced models for detecting positive and purifying selection using a Bayesian inference approach. Nucleic Acids Res 35:W506–W511
     [Google Scholar]
  64. Stone B. J., Abu Kwaik Y. 1998; Expression of multiple pili by Legionella pneumophila : identification and characterization of a type IV pilin gene and its role in adherence to mammalian and protozoan cells. Infect Immun 66:1768–1775
     [Google Scholar]
  65. Stone B. J., Abu Kwaik Y. 1999; Natural competence for DNA transformation by Legionella pneumophila and its association with expression of type IV pili. J Bacteriol 181:1395–1402
     [Google Scholar]
  66. Strimmer K., von Haeseler A. 1997; Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proc Natl Acad Sci U S A 94:6815–6819
     [Google Scholar]
  67. van Ketel R. J., ter Schegget J., Zanen H. C. 1984; Molecular epidemiology of Legionella pneumophila serogroup 1. J Clin Microbiol 20:362–364
     [Google Scholar]
  68. Vassileva M., Torii K., Oshimoto M., Okamoto A., Agata N., Yamada K., Hasegawa T., Ohta M. 2006; Phylogenetic analysis of Bacillus cereus isolates from severe systemic infections using multilocus sequence typing scheme. Microbiol Immunol 50:743–749
     [Google Scholar]
  69. Whatmore A. M., Dowson C. G. 1999; The autolysin-encoding gene ( lytA ) of Streptococcus pneumoniae displays restricted allelic variation despite localized recombination events with genes of pneumococcal bacteriophage encoding cell wall lytic enzymes. Infect Immun 67:4551–4556
     [Google Scholar]
  70. Wong S., Pabbaraju K., Burk V. F., Broukhanski G. C., Fox J., Louie T., Mah M. W., Bernard K., Tilley P. A. 2006; Use of sequence-based typing for investigation of a case of nosocomial legionellosis. J Med Microbiol 55:1707–1710
     [Google Scholar]
  71. Young M., Smith H., Gray B., Huang B., Barten J., Towner C., Plowman S., Afshar B., Fry N. other authors 2005; The public health implications of a sporadic case of culture-proven Legionnaires' disease. Aust N Z J Public Health 29:513–517
     [Google Scholar]
  72. Zhao X., Dreyfus L. A. 1990; Expression and nucleotide sequence analysis of the Legionella pneumophila recA gene. FEMS Microbiol Lett 58:227–231
     [Google Scholar]
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Clonal population structure of Legionella pneumophila inferred from allelic profiling
Microbiology 154, 852 (2008); https://doi.org/10.1099/mic.0.2007/012336-0
/content/journal/micro/10.1099/mic.0.2007/012336-0
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