A new Borrelia species defined by multilocus sequence analysis of housekeeping genes

Applied and Environmental Microbiology

Volumn 75, Issue 16, 2009, Pages 5410-5416

  Margos, Gabriele ^a   Vollmer, Stephanie A ^a   Cornet, Muriel ^b   Garnier, Martine ^b   Fingerle, Volker ^c   Wilske, Bettina ^d,h   Bormane, Antra ^e   Vitorino, Liliana ^f   Collares Pereira, Margarida ^f   Drancourt, Michel ^g   Kurtenbach, Klaus ^a  

^a University of Bath   (United Kingdom)

^b INSTITUT PASTEUR   (France)

^c National Reference Center for Borrelia   (Germany)

^d UNIVERSITY OF MUNICH   (Germany)

^e Public Health Agency   (Latvia)

^f INSTITUTO DE HIGIENE E MEDICINA TROPICAL   (Portugal)

^g AIX MARSEILLE UNIVERSITÉ   (France)

^h NONE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOTECHNOLOGY; MICROBIOLOGY;

BORRELIA; BORRELIA SPECIES; EVOLUTIONARY HISTORY; HOUSEKEEPING GENE; MULTILOCUS SEQUENCE ANALYSIS; PHYLOGENETIC TREES; SEROTYPES;

BACTERIA;

BACTERIUM; GENE EXPRESSION; GENETIC DIFFERENTIATION; PHYLOGENETICS; PHYLOGENY;

ARTICLE; BORRELIA; BORRELIA AFZELII; BORRELIA BURGDORFERI; BORRELIA GARINII; BORRELIA VALAISIANA; DNA HYBRIDIZATION; HOUSEKEEPING GENE; LYME DISEASE; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PHYLOGENY;

AVES; BORRELIA; BORRELIA GARINII; RODENTIA;

EID: 68549109626     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00116-09     Document Type: Article

References (53)

1. Achtman, M., K. Zurth, G. Morelli, G. Torrea, A. Guiyoule, and E. Carniel. 1999. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. USA 96:14043-14048.
2. Attie, O., J. F. Bruno, Y. Xu, D. Qiu, B. J. Luft, and W. G. Qiu. 2007. Co-evolution of the outer surface protein C gene (ospC) and intraspecific lineages of Borrelia burgdorferi sensu stricto in the northeastern United States. Infect. Genet. Evol. 7:1-12.
3. Baranton, G., D. Postic, I. Saint Girons, P. Boerlin, J. C. Piffaretti, M. Assous, and P. A. Grimont. 1992. Delineation of Borrelia burgdorferi sensu stricto, Borrelia garinii sp. nov., and group VS461 associated with Lyme borreliosis. Int. J. Syst. Bacteriol. 42:378-383.
4. Bishop, C. J., D. M. Aanensen, G. E. Jordan, M. Kilian, W. P. Hanage, and B. G. Spratt. 2009. Assigning strains to bacterial species via the internet. BMC Biol. 7:3.
5. Bunikis, J., U. Garpmo, J. Tsao, J. Berglund, D. Fish, and A. G. Barbour. 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.
6. Chu, C. Y., W. Liu, B. G. Jiang, D. M. Wang, W. J. Jiang, Q. M. Zhao, P. H. Zhang, Z. X. Wang, G. P. Tang, H. Yang, and W. C. Cao. 2008. Novel genospecies of Borrelia burgdorferi sensu lato from rodents and ticks in southwestern China. J. Clin. Microbiol. 46:3130-3133.
7. Collares-Pereira, M., S. Couceiro, I. Franca, K. Kurtenbach, S. M. Schafer, L. Vitorino, L. Goncalves, S. Baptista, M. L. Vieira, and C. Cunha. 2004. First isolation of Borrelia lusitaniae from a human patient. J. Clin. Microbiol. 42:1316-1318.
8. de Carvalho, I. L., J. E. Fonseca, J. G. Marques, A. Ullmann, A. Hojgaard, N. Zeidner, and M. S. Nuncio. 2008. Vasculitis-like syndrome associated with Borrelia lusitaniae infection. Clin. Rheumatol. 27:1587-1591.
9. Dykhuizen, D. E., and G. Baranton. 2001. The implications of a low rate of horizontal transfer in Borrelia. Trends Microbiol. 9:344-350.
10. Fingerle, V., U. C. Schulte-Spechtel, E. Ruzic-Sabljic, S. Leonhard, H. Hofmann, K. Weber, K. Pfister, F. Strle, and B. Wilske. 2008. Epidemiological aspects and molecular characterization of Borrelia burgdorferi s.l. from southern Germany with special respect to the new species Borrelia spielmanii sp. nov. Int. J. Med. Microbiol. 298:279-290.
11. Fukunaga, M., K. Okada, M. Nakao, T. Konishi, and Y. Sato. 1996. Phylogenetic analysis of Borrelia species based on flagellin gene sequences and its application for molecular typing of Lyme disease borreliae. Int. J. Syst. Bacteriol. 46:898-905.
12. Gern, L., and P. Humair. 2002. Ecology of Borrelia burgdorferi sensu lato in Europe, p. 149-174. In J. S. Gray, O. Kahl, R. S. Lane, and G. Stanek (ed.), Lyme borreliosis: biology of the infectious agents and epidemiology of disease. CABI Publishing, Wallingford, United Kingdom.
13. Gevers, D., P. Dawyndt, P. Vandamme, A. Willems, M. Vancanneyt, J. Swings, and P. De Vos. 2006. Stepping stones towards a new prokaryotic taxonomy. Philos. Trans. R. Soc. Lond. B 361:1911-1916.
14. Guy, E. C., and G. Stanek. 1991. Detection of Borrelia burgdorferi in patients with Lyme disease by the polymerase chain reaction. J. Clin. Pathol. 44:610-611.
15. Hanincova, K., S. M. Schafer, S. Etti, H. S. Sewell, V. Taragelova, D. Ziak, M. Labuda, and K. Kurtenbach. 2003. Association of Borrelia afzelii with rodents in Europe. Parasitology 126:11-20.
16. Hanincová, K., V. Taragelová, J. Koci, S. M. Schäfer, R. Hails, A. J. Ullmann, J. Piesman, M. Labuda, and K. Kurtenbach. 2003. Association of Borrelia garinii and B. valaisiana with songbirds in Slovakia. Appl. Environ. Microbiol. 69:2825-2830.
17. Hu, C. M., B. Wilske, V. Fingerle, Y. Lobet, and L. Gern. 2001. Transmission of Borrelia garinii OspA serotype 4 to BALB/c mice by Ixodes ricinus ticks collected in the field. J. Clin. Microbiol. 39:1169-1171.
18. Huegli, D., C. M. Hu, P. F. Humair, B. Wilske, and L. Gern. 2002. Apodemus species mice are reservoir hosts of Borrelia garinii OspA serotype 4 in Switzerland. J. Clin. Microbiol. 40:4735-4737.
19. Huelsenbeck, J. P., and F. Ronquist. 2005. Bayesian analysis of molecular evolution using MrBayes, p. 183-232. In R. Nielsen (ed.), Statistical methods in molecular evolution. Springer, New York, NY.
20. Kawabata, H., T. Masuzawa, and Y. Yanagihara. 1993. Genomic analysis of Borrelia japonica sp. nov. isolated from Ixodes ovatus in Japan. Microbiol. Immunol. 37:843-848.
21. Kumar, S., K. Tamura, and M. Nei. 2004. Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinformatics 5:150-163.
22. Kurtenbach, K., S. De Michelis, S. Etti, S. M. Schafer, H. S. Sewell, V. Brade, and P. Kraiczy. 2002. Host association of Borrelia burgdorferi sensu lato-the key role of host complement. Trends Microbiol. 10:74-79.
23. Kurtenbach, K., S. De Michelis, H. S. Sewell, S. Etti, S. M. Schafer, R. Hails, M. Collares-Pereira, M. Santos-Reis, K. Hanincova, M. Labuda, A. Bormane, and M. Donaghy. 2001. Distinct combinations of Borrelia burgdorferi sensu lato genospecies found in individual questing ticks from Europe. Appl. Environ. Microbiol. 67:4926-4929.
24. Kurtenbach, K., K. Hanincova, J. I. Tsao, G. Margos, D. Fish, and N. H. Ogden. 2006. Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nat. Rev. Microbiol. 4:660-669.
25. Kurtenbach, K., M. Peacey, S. G. Rijpkema, A. N. Hoodless, P. A. Nuttall, and S. E. Randolph. 1998. Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Appl. Environ. Microbiol. 64:1169-1174.
26. Kurtenbach, K., S. M. Schaefer, S. de Michelis, S. Etti, and H. S. Sewell. 2002. Borrelia burgdorferi s.l. in the vertebrate host, p. 117-148. In J. S. Gray, O. Kahl, R. S. Lane, and G. Stanek (ed.), Lyme borreliosis: biology of the infectious agents and epidemiology of disease. CABI Publishing, Wallingford, United Kingdom.
27. Maiden, M. C., J. A. Bygraves, E. Feil, G. Morelli, J. E. Russell, R. Urwin, Q. Zhang, J. Zhou, K. Zurth, D. A. Caugant, I. M. Feavers, M. Achtman, and B. G. Spratt. 1998. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. USA 95:3140-3145.
28. Marconi, R. T., S. Hohenberger, S. Jauris-Heipke, U. Schulte-Spechtel, C. P. LaVoie, D. Rossler, and B. Wilske. 1999. Genetic analysis of Borrelia garinii OspA serotype 4 strains associated with neuroborreliosis: evidence for extensive genetic homogeneity. J. Clin. Microbiol. 37:3965-3970.
29. Marconi, R. T., D. Liveris, and I. Schwartz. 1995. Identification of novel insertion elements, restriction fragment length polymorphism patterns, and discontinuous 23S rRNA in Lyme disease spirochetes: phylogenetic analyses of rRNA genes and their intergenic spacers in Borrelia japonica sp. nov. and genomic group 21038 (Borrelia andersonii sp. nov.) isolates. J. Clin. Microbiol. 33:2427-2434.
30. Margos, G., A. G. Gatewood, D. M. Aanensen, K. Hanincova, D. Terekhova, S. A. Vollmer, M. Cornet, J. Piesman, M. Donaghy, A. Bormane, M. A. Hurn, E. J. Feil, D. Fish, S. Casjens, G. P. Wormser, I. Schwartz, and K. Kurtenbach. 2008. MLST of housekeeping genes captures geographic population structure and suggests a European origin of Borrelia burgdorferi. Proc. Natl. Acad. Sci. USA 105:8730-8735.
31. Masuzawa, T. 2004. Terrestrial distribution of the Lyme borreliosis agent Borrelia burgdorferi sensu lato in East Asia. Jpn. J. Infect. Dis. 57:229-235.
32. Masuzawa, T., I. G. Kharitonenkov, T. Kadosaka, N. Hashimoto, M. Kudeken, N. Takada, K. Kaneda, and Y. Imai. 2005. Characterization of Borrelia burgdorferi sensu lato isolated in Moscow province-a sympatric region for Ixodes ricinus and Ixodes persulcatus. Int. J. Med. Microbiol. 294:455-464.
33. Masuzawa, T., N. Takada, M. Kudeken, T. Fukui, Y. Yano, F. Ishiguro, Y. Kawamura, Y. Imai, and T. Ezaki. 2001. Borrelia sinica sp. nov., a Lyme disease-related Borrelia species isolated in China. Int. J. Syst. Evol. Microbiol. 51:1817-1824.
34. Michel, H., B. Wilske, G. Hettche, G. Gottner, C. Heimerl, U. Reischl, U. Schulte-Spechtel, and V. Fingerle. 2004. An ospA-polymerase chain reaction/ restriction fragment length polymorphism-based method for sensitive detection and reliable differentiation of all European Borrelia burgdorferi sensu lato species and OspA types. Med. Microbiol. Immunol. 193:219-226.
35. Piesman, J., and L. Gern. 2004. Lyme borreliosis in Europe and North America. Parasitology 129(Suppl.):S191-S220.
36. Postic, D., M. V. Assous, P. A. Grimont, and G. Baranton. 1994. Diversity of Borrelia burgdorferi sensu lato evidenced by restriction fragment length polymorphism of rrf (5S)-rrl (23S) intergenic spacer amplicons. Int. J. Syst. Bacteriol. 44:743-752.
37. Postic, D., M. Garnier, and G. Baranton. 2007. Multilocus sequence analysis of atypical Borrelia burgdorferi sensu lato isolates-description of Borrelia californiensis sp. nov., and genomospecies 1 and 2. Int. J. Med. Microbiol. 297:263-271.
38. Postic, D., N. M. Ras, R. S. Lane, M. Hendson, and G. Baranton. 1998. Expanded diversity among Californian Borrelia isolates and description of Borrelia bissettii sp. nov. (formerly Borrelia group DN127). J. Clin. Microbiol. 36:3497-3504.
39. Qiu, W. G., S. E. Schutzer, J. F. Bruno, O. Attie, Y. Xu, J. J. Dunn, C. M. Fraser, S. R. Casjens, and B. J. Luft. 2004. Genetic exchange and plasmid transfers in Borrelia burgdorferi sensu stricto revealed by three-way genome comparisons and multilocus sequence typing. Proc. Natl. Acad. Sci. USA 101:14150-14155.
40. Richter, D., D. Postic, N. Sertour, I. Livey, F. R. Matuschka, and G. Baranton. 2006. Delineation of Borrelia burgdorferi sensu lato species by multilocus sequence analysis and confirmation of the delineation of Borrelia spielmanii sp. nov. Int. J. Syst. Evol. Microbiol. 56:873-881.
41. Rudenko, N., M. Golovchenko, L. Grubhoffer, and J. H. Oliver, Jr. 2009. Borrelia carolinensis sp. nov., a new (14th) member of Borrelia burgdorferi sensu lato complex from the southeastern region of the United States. J. Clin. Microbiol. 47:134-141.
42. Schulte-Spechtel, U., V. Fingerle, G. Goettner, S. Rogge, and B. Wilske. 2006. Molecular analysis of decorin-binding protein A (DbpA) reveals five major groups among European Borrelia burgdorferi sensu lato strains with impact for the development of serological assays and indicates lateral gene transfer of the dbpA gene. Int. J. Med. Microbiol. 296(Suppl. 40):250-266.
43. Schwartz, J. J., A. Gazumyan, and I. Schwartz. 1992. rRNA gene organization in the Lyme disease spirochete, Borrelia burgdorferi. J. Bacteriol. 174: 3757-3765.
44. Spratt, B. G. 1999. Multilocus sequence typing: molecular typing of bacterial pathogens in an era of rapid DNA sequencing and the Internet. Curr. Opin. Microbiol. 2:312-316.
45. Taragel'ová, V., J. Koči, K. Hanincová, K. Kurtenbach, M. Derdáková, N. H. Ogden, I. Literák, E. Kocianová, and M. Labuda. 2008. Blackbirds and song thrushes constitute a key reservoir of Borrelia garinii, the causative agent of borreliosis in Central Europe. Appl. Environ. Microbiol. 74:1289-1293.
46. van Dam, A. P. 2002. Diversity of Ixodes-borne Borrelia species-clinical, pathogenetic, and diagnostic implications and impact on vaccine development. Vector Borne Zoonotic Dis. 2:249-254.
47. Vitorino, L., I. M. Chelo, F. Bacellar, and L. Ze-Ze. 2007. Rickettsiae phylogeny: a multigenic approach. Microbiology 153:160-168.
48. Vitorino, L. R., G. Margos, E. J. Feil, M. Collares-Pereira, L. Ze-Ze, and K. Kurtenbach. 2008. Fine-scale phylogeographic structure of Borrelia lusitaniae revealed by multilocus sequence typing. PloS One 3:e4002.
49. Wang, G., A. P. van Dam, and J. Dankert. 1999. Evidence for frequent OspC gene transfer between Borrelia valaisiana sp. nov. and other Lyme disease spirochetes. FEMS Microbiol. Lett. 177:289-296.
50. Wang, G., A. P. van Dam, and J. Dankert. 2000. Two distinct ospA genes among Borrelia valaisiana strains. Res. Microbiol. 151:325-331.
51. Will, G., S. Jauris-Heipke, E. Schwab, U. Busch, D. Rossler, E. Soutschek, B. Wilske, and V. Preac-Mursic. 1995. Sequence analysis of ospA genes shows homogeneity within Borrelia burgdorferi sensu stricto and Borrelia afzelii strains but reveals major subgroups within the Borrelia garinii species. Med. Microbiol. Immunol. 184:73-80.
52. Wilske, B., U. Busch, H. Eiffert, V. Fingerle, H. W. Pfister, D. Rossler, and V. Preac-Mursic. 1996. Diversity of OspA and OspC among cerebrospinal fluid isolates of Borrelia burgdorferi sensu lato from patients with neuroborreliosis in Germany. Med. Microbiol. Immunol. 184:195-201.
53. Wilske, B., V. Preac-Mursic, U. B. Gobel, B. Graf, S. Jauris, E. Soutschek, E. Schwab, and G. Zumstein. 1993. An OspA serotyping system for Borrelia burgdorferi based on reactivity with monoclonal antibodies and ospA sequence analysis. J. Clin. Microbiol. 31:340-350.