Molecular Genetics, Microbiology and Virology

, Volume 32, Issue 4, pp 196–203 | Cite as

Multilocus Sequence Analysis of “Atypical” Borrelia burgdorferi sensu lato Isolated in Russia

  • V. V. Nefedova
  • E. I. Korenberg
  • N. B. Gorelova
Experimental Works


Seventeen isolates of Borrelia burgdorferi sensu lato with an unclear genetic characteristic isolated in Russia from various species of Ixodes ticks (I. persulcatus, I. ricinus, and I. pavlovskyi) have been studied by multilocus sequencing analysis. According to the results of typing, these isolates were identified as B. bavariensis (n = 7), B. garinii (n = 6), B. finlandensis (n = 3), and B. spielmanii (n = 1), that is, species that can cause ixodid tick-borne borreliosis diseases in human beings. The allelic polymorphism of five genes (rrs, fla, groEL, recA, and ospA) and spacer rrfArrlB of B. bavariensis and B. garinii isolates was analyzed in comparison with their diversity in the International Nucleotide Sequence Database Collaboration.


Borrelia butgdoferi sensu lato MLSA various species of Ixodes ticks 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Pritt, B.S., Respicio-Kingry, L.B., Sloan, L.M., Schriefer, M.E., Replogle, A.J., Bjork, J., et al., Borrelia mayonii sp. nov., a member of the Borrelia burgdorferi sensu lato complex, detected in patients and ticks in the upper Midwestern United States, Int. J. Syst. Evol. Microbiol., 2016, vol. 66, no. 11, pp. 4878–4880.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Rudenko, N., Golovchenko, M., Vancova, M., Clark, K., Grubhoffer, L., and Oliver, J.H., Isolation of live Borrelia burgdorferi sensu lato spirochaetes from patients with undefined disorders and symptoms not typical for Lyme borreliosis, Clin. Microbiol. Infect., 2016, vol. 22, no. 3, pp. 267.e9–267.e15. doi 10.1016/j.cmi.2015.11.009CrossRefGoogle Scholar
  3. 3.
    Mongodin, E.F., Casjens, S.R., Bruno, J.F., Xu, Y., Drabek, E.F., Riley, D.R., et al., Inter-and intra-specific pan-genomes of Borrelia burgdorferi sensu lato: genome stability and adaptive radiation, BMC Genomics, 2013, vol. 14, p.693.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Margos, G., Vollmer, S.A., Ogden, N.H., and Fish, D., Population genetics, taxonomy, phylogeny and evolution of Borrelia burgdorferi sensu lato, Infect., Genet. Evol., 2011, vol. 11, pp. 1545–1563.CrossRefGoogle Scholar
  5. 5.
    Ivanova, L.B., Tomova, A., González-Acuña, D., Murúa, R., Moreno, C.X., and Hernández, C., Borrelia chilensis, a new member of the Borrelia burgdorferi sensu lato complex that extends the range of this genospecies in the Southern Hemisphere, Environ. Microbiol., 2014, vol. 16, no. 4, pp. 1069–1080.CrossRefPubMedGoogle Scholar
  6. 6.
    Margos, G., Chu Chen-Yi, Takano Ai, Jiang Bao-Gui, Liu We, Kurtenbach, K., et al., Borrelia yangtzensis sp. nov., a rodent-associated species in Asia, is related to Borrelia valaisiana, Int. J. Syst. Evol. Microbiol., 2015, vol. 65, pp. 3836–3840.CrossRefPubMedGoogle Scholar
  7. 7.
    Casjens, S.R., Fraser-Liggett, C.M., Mongodin, E.F., Qiu, W.G., Dunn, J.J., Luft, B.J., and Schutzer, S.E., Whole genome sequence of an unusual Borrelia burgdorferi sensu lato isolate, J. Bacteriol., 2011, vol. 193, no. 6, pp. 1489–1490.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Postic, D., Garnier, M., and Baranton, G., 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., 2007, vol. 297, pp. 263–271.CrossRefPubMedGoogle Scholar
  9. 9.
    Vysotskii, V.V. and Kotlyarova, G.A., Poly(hetero) morphic forms of pathogenic bacteria in infectious pathology, Zh. Mikrobiol., Epidemiol. Immunobiol., 1999, no. 2, pp. 100–104.Google Scholar
  10. 10.
    Korenberg, E.I., Nefedova, V.V., Gorelova, N.B., Kovalevskii, Yu.V., Fadeeva, I.A., and Golubova, D.A., Etiological structure of southern taiga combinations of natural foci of ixodic tick-borne borrelioses, Vestn. Ross. Akad. Med. Nauk, 2011, no. 10, pp. 10–15.Google Scholar
  11. 11.
    Korenberg, E.I. and Nefedova, V.V., Borrelia—pathogens of tick-borne borrelioses and epidemic relapsing fever, in Rukovodstvo po meditsinskoi mikrobiologii. Chastnaya meditsinskaya mikrobiologiya i etiologicheskaya diagnostika infektsii (Guideline on Medical Microbiology. Special Medical Microbiology and Etiological Diagnostics of Infections), Labinskaya, A.S., Kostyukova, N.N., and Ivanova, S.M., Eds., Moscow: BINOM, 2010, pp. 844–866.Google Scholar
  12. 12.
    Korenberg, E.I., Pomelova, V.G., and Osin, N.S., Prirodnoochagovye infektsii, peredayushchiesya iksodovymi kleshchami (Natural Focal Infections Transmitted by Ixodic Ticks), Moscow: Kommentarii, 2013.Google Scholar
  13. 13.
    Margos, G., Vollmer, S.A., Cornet, M., Garnier, M., Fingerle, V., Wilske, B., et al., A new Borrelia species defined by Multilocus sequence analysis of housekeeping genes, Appl. Environ. Microbiol., 2009, vol. 75, no. 16, pp. 5410–5416.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Gorelova, N.B., Korenberg, E.I., Vorob’eva, N.N., Frizen, V.I., Nefedova, V.V., and Teterin, V.Yu., Isolating pathogen of ixodic tick borreliosis from the patients’ blood, Zh. Mikrobiol., Epidemiol. Immunobiol., 2009, no. 1, pp. 63–66.Google Scholar
  15. 15.
    Nefedova, V.V., Korenberg, E.I., and Gorelova, N.B., Genetic variants of Borrelia garinii, a widespread Eurasian pathogen of ixodic tick borreliosis, Mol. Genet., Microbiol. Virol., 2010, vol. 25, no. 3, pp. 95–100.CrossRefGoogle Scholar
  16. 16.
    Nefedova, V.V., Korenberg, E.I., Fadeeva, I.A., and Gorelova, N.B., Genetic characteristics of pathogenic for humans Borrelia isolated from Ixodes trianguliceps bir. and Ixodes pavlovskyi pom ticks, Med. Parazitol. Parazit. Bolezni, 2005, no. 2, pp. 9–12.Google Scholar
  17. 17.
    Nefedova, V.V., Korenberg, E.I., and Gorelova, N.B., Genotyping Borrelia burgdorferi sensu lato isolates from Ixodes Ricinus ticks in Russia and Ukraine, Mol. Genet., Microbiol. Virol., 2010, vol. 25, no. 1, pp. 25–30.CrossRefGoogle Scholar
  18. 18.
    Korenberg, E.I., Nefedova, V.V., Romanenko, V.N., and Gorelova, N.B., The tick Ixodes pavlovskyi as a host of spirochetes pathogenic for humans and its possible role in the epizootiology and epidemiology of Borrelioses, Vector Borne Zoonotic Dis., 2010, vol. 10, no. 5, pp. 453–458.CrossRefPubMedGoogle Scholar
  19. 19.
    Mukhacheva, T.A. and Kovalev, S.Y., Multilocus sequence analysis of Borrelia burgdorferi s.1. in Russia, Ticks Tick Borne Dis., 2013, vol. 4, no. 4, pp. 275–279.CrossRefPubMedGoogle Scholar
  20. 20.
    Richter, D., Schlee, D.B., Allgöwer, R., and Matuschka, F.-R., Relationships of a novel Lyme disease spirochete, Borrelia spielmani sp. nov., with its hosts in Central Europe, Appl. Environ. Microbiol., 2004, vol. 70, no. 11, pp. 6414–6419.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Wang, G., van Dam, A.P., and Dankert, J., Phenotypic and genetic characterization of a novel Borrelia burgdorferi sensu lato isolate from a patient with Lyme borreliosis, J. Clin. Microbiol., 1999, vol. 37, no. 9, pp. 3025–3028.PubMedPubMedCentralGoogle Scholar
  22. 22.
    Hao, Q., Hou, X., Geng, Z., and Wan, K., Distribution of Borrelia burgdorferi sensu lato in China, J. Clin. Microbiol., 2011, vol. 49, no. 2, pp. 647–650.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Gómez-Díaz, E., Boulinier, T., Sertour, N., Cornet, M., Ferquel, E., and McCoy, K.D., Genetic structure of marine Borrelia garinii and population admixture with the terrestrial cycle of Lyme borreliosis, Environ. Microbiol., 2011, vol. 13, no. 9, pp. 2453–2467.CrossRefPubMedGoogle Scholar
  24. 24.
    Margos, G., Gatewood, A.G., Aanensen, D.M., Hanincová, K., Terekhova, D., Vollmer, S.A., et al., MLST of housekeeping genes captures geographic population structure and suggests a European origin of Borrelia burgdorferi, Proc. Natl. Acad. Sci. U. S. A., 2008, vol. 105, no. 25, pp. 8730–8735.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Marti Ras, N., Postic, D., Foretz, M., and Baranton, G., Borrelia burgdorferi sensu stricto, a bacterial species “made in the U.S.A.”?, Int. J. Syst. Bacteriol., 1997, vol. 47, no. 4, pp. 1112–1117.CrossRefPubMedGoogle Scholar
  26. 26.
    Castillo-Ramírez, S., Fingerle, V., Jungnick, S., Straubinger, R.K., Krebs, S., Blum, H., et al., Trans-Atlantic exchanges have shaped the population structure of the Lyme disease agent Borrelia burgdorferi sensu stricto, Sci. Rep., 2016, vol. 6, p. 22794.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Margos, G., Wilske, B., Sing, A., Hizo-Teufel, C., Cao, W.C., Chu, C., et al., Borrelia bavariensis sp. nov. is widely distributed in Europe and Asia, Int. J. Syst. Evol. Microbiol., 2013, vol. 63, pp. 4284–4288.CrossRefPubMedGoogle Scholar
  28. 28.
    Huegli, D., Hu, C.M., Humair, P.-F., Wilske, B., and Gern, L., Apodemus species mice are reservoir hosts of Borrelia garinii OspA serotype 4 in Switzerland, J. Clin. Microbiol., 2002, vol. 40, no. 12, pp. 4735–4737.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Takano, A., Nakao, M., Masuzawa, T., Takada, N., Yano, Y., Ishiguro, F., Fujita, H., et al., Multilocus sequence typing implicates rodents as the main reservoir host of human-pathogenic Borrelia garinii in Japan, J. Clin. Microbiol., 2011, vol. 49, no. 5, pp. 2035–2039.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Scholz, H.C., Margos, G., Derschum, H., Speck, S., Tserennorov, D., Erdenebat, N., et al., High prevalence of genetically diverse Borrelia bavariensis-like strains in Ixodes persulcatus from Selenge Aimag, Mongolia, Ticks Tick Borne Dis., 2013, vol. 4, nos. 1–2, pp. 89–92.CrossRefGoogle Scholar
  31. 31.
    Filippova, N.A., Taezhnyy kleshch Ixodes persulcatus Schulze (Acrana, Ixodidae): morfologiya, sistematika, ekologiya, meditsinskoe znachenie (Taiga Tick Ixodes persulcatus Schulze (Acrana, Ixodidae): Morphology, Systematics, Ecology, Medical Significance), Leningrad: Nauka, 1985.Google Scholar
  32. 32.
    Tveten, A.-K., Exploring diversity among Norwegian Borrelia strains originating from Ixodes ricinus ticks, J. Microbiol., 2014, vol. 2014, Art. ID 397143. doi 10.1155/2014/397143

Copyright information

© Allerton Press, Inc. 2017

Authors and Affiliations

  • V. V. Nefedova
    • 1
  • E. I. Korenberg
    • 1
  • N. B. Gorelova
    • 1
  1. 1.Gamaleya Federal Research Center for Epidemiology and MicrobiologyMinistry of Health of the Russian FederationMoscowRussia

Personalised recommendations