NGS population genetics analyses reveal divergent evolution of a Lyme Borreliosis agent in Europe and Asia

Ticks and Tick-borne Diseases

Volumn 6, Issue 3, 2015, Pages 344-351

  Gatzmann, Fanny ^a   Metzler, Dirk ^a   Krebs, Stefan ^a   Blum, Helmut ^a   Sing, Andreas ^b   Takano, Ai ^c,d   Kawabata, Hiroki ^d,e   Fingerle, Volker ^b   Margos, Gabriele ^b   Becker, Noémie S ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b LMU Munich ^*  (Germany)

^c YAMAGUCHI UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^e GIFU UNIVERSITY   (Japan)

Author keywords

Borrelia bavariensis; Evolution; Ixodes persulcatus; Ixodes ricinus; Lyme disease; Population genetics

Indexed keywords

ARTICLE; ASIA; BACTERIAL CHROMOSOME; BACTERIAL GENETICS; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BORRELIA; BORRELIA BAVARIENSIS; CLONAL EVOLUTION; CONTROLLED STUDY; EUROPE; GENE IDENTIFICATION; GENETIC ANALYSIS; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NEXT GENERATION SEQUENCING; NONHUMAN; PLASMID; POPULATION GENETIC STRUCTURE; POPULATION GENETICS; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; ANIMAL; DNA SEQUENCE; GENETICS; HIGH THROUGHPUT SEQUENCING; HUMAN; ISOLATION AND PURIFICATION; IXODES; LYME DISEASE; MICROBIOLOGY; PARASITE VECTOR; PHYLOGENY;

BORRELIA; BORRELIA BURGDORFERI; IXODES PERSULCATUS; IXODES RICINUS; IXODIDA;

ANIMALS; ARACHNID VECTORS; ASIA; BORRELIA; CHROMOSOMES, BACTERIAL; EUROPE; GENETICS, POPULATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; IXODES; LYME DISEASE; PHYLOGENY; PLASMIDS; SEQUENCE ANALYSIS, DNA;

EID: 84928204701     PISSN: 1877959X     EISSN: 18779603     Source Type: Journal    
DOI: 10.1016/j.ttbdis.2015.02.008     Document Type: Article

References (57)

1. Barbour A.G., Travinsky B. Evolution and distribution of the ospC Gene, a transferable serotype determinant of Borrelia burgdorferi. MBio 2010, 1.
2. Benson D.A., Cavanaugh M., Clark K., Karsch-Mizrachi I., Lipman D.J., Ostell J., Sayers E.W. GenBank. Nucleic Acids Res. 2013, 41:D36-D42. 10.1093/nar/gks1195.
3. Blankenberg D., Von Kuster G., Coraor N., Ananda G., Lazarus R., Mangan M., Nekrutenko A., Taylor J. Galaxy: a web-based genome analysis tool for experimentalists. Curr. Protoc. Mol. Biol. 2010, 10-19.
4. Brenner E.V., Kurilshikov A.M., Stronin O.V., Fomenko N.V. Whole-genome sequencing of Borrelia garinii BgVir, isolated from Taiga ticks (Ixodes persulcatus). J. Bacteriol. 2012, 194:5713. 10.1128/JB.01360-12.
5. Didelot X., Falush D. Inference of bacterial microevolution using multilocus sequence data. Genetics 2007, 175(3):1251-1266.
6. Drummond A.J., Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007, 7:214. 10.1186/1471-2148-7-214.
7. Dubska L., Literak I., Kocianova E., Taragelova V., Sychra O. Differential role of passerine birds in distribution of Borrelia spirochetes, based on data from ticks collected from birds during the postbreeding migration period in Central Europe. Appl. Environ. Microbiol. 2009, 75:596-602.
8. Fingerle V., Schulte-Spechtel U.C., Ruzic-Sabljic E., Leonhard S., Hofmann H., Weber K., Pfister K., Strle F., Wilske B. 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. 2008, 298:279-290.
9. Fu Y.X., Li W.H. Statistical tests of neutrality of mutations. Genetics 1993, 133:693-709.
10. Geller J., Nazarova L., Katargina O., Golovljova I. Borrelia burgdorferi sensu lato prevalence in tick populations in Estonia. Parasit. Vectors 2013, 6:202. 10.1186/1756-3305-6-202.
11. Giardine B., Riemer C., Hardison R.C., Burhans R., Elnitski L., Shah P., Zhang Y., Blankenberg D., Albert I., Taylor J., Miller W.C., Kent W.J., Nekrutenko A. Galaxy: a platform for interactive large-scale genome analysis. Genome Res. 2005, 15:1451-1455.
12. Glöckner G., Lehmann R., Romualdi A., Pradella S., Schulte-Spechtel U., Schilhabel M., Wilske B., Sühnel J., Platzer M. Comparative analysis of the Borrelia garinii genome. Nucleic Acids Res. 2004, 32:6038-6046. 10.1093/nar/gkh953.
13. Goecks J., Nekrutenko A., Taylor J., Team T.G. Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol. 2010, 11:R86.
14. Hanincova K., Mukherjee P., Ogden N.H., Margos G., Wormser G.P., Reed K.D., Meece J.K., Vandermause M.F., Schwartz I. Multilocus sequence typing of Borrelia burgdorferi suggests existence of lineages with differential pathogenic properties in humans. PLOS ONE 2013, 8:e73066. 10.1371/journal.pone.0073066.
15. Hanincova K., Taragelova V., Koci J., Schafer S.M., Hails R., Ullmann A.J., Piesman J., Labuda M., Kurtenbach K. Association of Borrelia garinii and B. valaisiana with songbirds in Slovakia. Appl. Environ. Microbiol. 2003, 69:2825-2830.
16. Hu C.M., Wilske B., Fingerle V., Lobet Y., Gern L. Transmission of Borrelia garinii OspA serotype 4 to BALB/c mice by Ixodes ricinus ticks collected in the field. J. Clin. Microbiol. 2001, 39:1169-1171.
17. Hudson R.R., Kaplan N.L. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 1985, 111:147-164.
18. Huson D.H., Bryant D. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 2006, 23(2):254-267.
19. Huegli D., Hu C.M., Humair P.F., Wilske B., Gern L. Apodemus species mice are reservoir hosts of Borrelia garinii OspA serotype 4 in Switzerland. J. Clin. Microbiol. 2002, 40:4735-4737.
20. Innan H., Terauchi R., Kahl G., Tajima F. A method for estimating nucleotide diversity from AFLP data. Genetics 1999, 151:1157-1164.
21. Jiang B., Yao H., Tong Y., Yang X., Huang Y., Jiang J., Cao W. Genome sequence of Borrelia garinii strain NMJW1, isolated from China. J. Bacteriol. 2012, 194:6660-6661. 10.1128/JB.01844-12.
22. Korenberg E.I., Gorelova N.B., Kovalevskii Y.V. Ecology of Borrelia burgdorferi sensu lato in Russia. Lyme Borreliosis: Biology, Epidemiology and Control 2002, CABI Publishing, Wallingford. J. Gray, O. Kahl, R.S. Lane, G. Stanek (Eds.).
23. Kurtenbach K., Hanincová K., Tsao J.I., Margos G., Fish D., Ogden N.H. Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nat. Rev. Microbiol. 2006, 4:660-669.
24. Lassmann T., Sonnhammer E.L.L. Kalign - an accurate and fast multiple sequence alignment algorithm. BMC Bioinformatics 2005, 6:298. 10.1186/1471-2105-6-298.
25. Laursen B.S., Sørensen H.P., Mortensen K.K., Sperling-Petersen H.U. Initiation of protein synthesis in bacteria. Microbiol. Mol. Biol. Rev. 2005, 69:101-123. 10.1128/MMBR.69.1.101-123.2005.
26. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. The sequence alignment/map format and SAMtools. Bioinformatics 2009, 25:2078-2079. 10.1093/bioinformatics/btp352.
27. Li R., Zhu H., Ruan J., Qian W., Fang X., Shi Z., Li Y., Li S., Shan G., Kristiansen K., Li S., Yang H., Wang J., Wang J. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res. 2010, 20:265-272. 10.1101/gr.097261.109.
28. Lutz M. Learning Python 2009, O'Reilly Media. 4th ed.
29. Marconi R.T., Hohenberger S., Jauris-Heipke S., Schulte-Spechtel U., LaVoie C.P., Rossler D., Wilske B. Genetic analysis of Borrelia garinii OspA serotype 4 strains associated with neuroborreliosis: evidence for extensive genetic homogeneity. J. Clin. Microbiol. 1999, 37(12):3965-3970.
30. Margos G., Castillo-Ramírez S., Hoen A.G. Phylogeography of Lyme borreliosis-group spirochetes and methicillin-resistant Staphylococcus aureus. Parasitology 2012, 139:1952-1965. 10.1017/S0031182012000741.
31. Margos G., Vollmer S.A., Cornet M., Garnier M., Fingerle V., Wilske B., Bormane A., Vitorino L., Collares-Pereira M., Drancourt M., Kurtenbach K. A new Borrelia species defined by multilocus sequence analysis of housekeeping genes. Appl. Environ. Microbiol. 2009, 75:5410-5416.
32. Margos G., Wilske B., Sing A., Hizo-Teufel C., Cao W.-C., Chu C., Scholz H., Straubinger R.K., Fingerle V. Borrelia bavariensis sp. nov. is widely distributed in Europe and Asia. Int. J. Syst. Evol. Microbiol. 2013, 63:4284-4288.
33. Masuzawa T., Kharitonenkov I.G., Kadosaka T., Hashimoto N., Kudeken M., Takada N., Kaneda K., Imai Y. Characterization of Borrelia burgdorferi sensu lato isolated in Moscow province-a sympatric region for Ixodes ricinus and Ixodes persulcatus. Int. J. Med. Microbiol. 2005, 294:455-464.
34. Miyamoto K., Masuzawa T. Ecology of Borrelia burgdorferi sensu lato in Japan and East Asia. Lyme Borreliosis: Biology, Epidemiology and Control 2002, 201-222. CABI Publishing, Wallingford. J. Gray, O. Kahl, R.S. Lane, G. Stanek (Eds.).
35. Mongodin E.F., Casjens S.R., Bruno J.F., Xu Y., Drabek E.F., Riley D.R., Cantarel B.L., Pagan P.E., Hernandez Y.A., Vargas L.C., Dunn J.J., Schutzer S.E., Fraser C.M., Qiu W.-G., Luft B.J. Inter- and intra-specific pan-genomes of Borrelia burgdorferi sensu lato: genome stability and adaptive radiation. BMC Genomics 2013, 14:693. 10.1186/1471-2164-14-693.
36. Mukhacheva T.A., Kovalev S.Y. Multilocus sequence analysis of Borrelia burgdorferi s.l. in Russia. Ticks Tick Borne Dis. 2013, 4:275-279.
37. Nei M. Molecular Evolutionnary Genetics 1987, Columbia Univ. Press, New York.
38. Ojaimi C., Brooks C., Akins D., Casjens S., Rosa P., Elias A., Barbour A., Jasinskas A., Benach J., Katonah L., Radolf J., Caimano M., Skare J., Swingle K., Sims S., Schwartz I. Borrelia burgdorferi gene expression profiling with membrane-based arrays. Methods Enzymol. 2002, 358:165-177.
39. Pal U., Li X., Wang T., Montgomery R.R., Ramamoorthi N., Desilva A.M., Bao F., Yang X., Pypaert M., Pradhan D., Kantor F.S., Telford S., Anderson J.F., Fikrig E. TROSPA, an Ixodes scapularis receptor for Borrelia burgdorferi. Cell 2004, 119:457-468. 10.1016/j.cell.2004.10.027.
40. Paradis E. pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 2010, 26:419-420. 10.1093/bioinformatics/btp696.
41. Paradis E., Claude J., Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 2004, 20:289-290.
42. Ruzić-Sabljić E., Strle F. Comparison of growth of Borrelia afzelii, B. garinii, and B. burgdorferi sensu stricto in MKP and BSK-II medium. Int. J. Med. Microbiol. 2004, 294:407-412. 10.1016/j.ijmm.2004.08.002.
43. Scholz H.C., Margos G., Derschum H., Speck S., Tserennorov D., Erdenebat N., Undraa B., Enkhtuja M., Battsetseg J., Otgonchimeg C., Otgonsuren G., Nymadulam B., Romer A., Thomas A., Essbauer S., Wolfel R., Kiefer D., Zoller L., Otgonbaatar D., Fingerle V. High prevalence of genetically diverse Borrelia bavariensis-like strains in Ixodes persulcatus from Selenge Aimag, Mongolia. Ticks Tick Borne Dis. 2013, 4:89-92. 10.1016/j.ttbdis.2012.08.004.
44. Schwan T.G., Piesman J. Temporal changes in outer surface proteins A and C of the Lyme disease-associated spirochete. Borrelia burgdorferi, during the chain of infection in ticks and mice. J. Clin. Microbiol. 2000, 38:382-388.
45. Seinost G., Dykhuizen D.E., Dattwyler R.J., Golde W.T., Dunn J.J., Wang I.N., Wormser G.P., Schriefer M.E., Luft B.J. Four clones of Borrelia burgdorferi sensu stricto cause invasive infection in humans. Infect. Immun. 1999, 67:3518-3524.
46. Skuballa J., Oehme R., Hartelt K., Petney T., Bucher T., Kimmig P., Taraschewski H. European hedgehogs as hosts for Borrelia spp., Germany. Emerg. Infect. Dis. 2007, 13:952-953.
47. Stanek G., Fingerle V., Hunfeld K.-P., Jaulhac B., Kaiser R., Krause A., Kristoferitsch W., O'Connell S., Ornstein K., Strle F., Gray J. Lyme borreliosis: clinical case definitions for diagnosis and management in Europe. Clin. Microbiol. Infect. 2011, 17:69-79. 10.1111/j.1469-0691.2010.03175.x.
48. Stanek G., Strle F. Lyme borreliosis: a European perspective on diagnosis and clinical management. Curr. Opin. Infect. Dis. 2009, 22:450-454. 10.1097/QCO.0b013e32832ee880.
49. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989, 123:585-595.
50. Takano A., Nakao M., Masuzawa T., Takada N., Yano Y., Ishiguro F., Fujita H., Ito T., Ma X., Oikawa Y., Kawamori F., Kumagai K., Mikami T., Hanaoka N., Ando S., Honda N., Taylor K., Tsubota T., Konnai S., Watanabe H., Ohnishi M., Kawabata H. Multilocus sequence typing implicates rodents as the main reservoir host of human-pathogenic Borrelia garinii in Japan. J. Clin. Microbiol. 2011, 49:2035-2039.
51. Taragel'ova V., Koci J., Hanincova K., Kurtenbach K., Derdakova M., Ogden N.H., Literak I., Kocianova E., Labuda M. Blackbirds and song thrushes constitute a key reservoir of Borrelia garinii, the causative agent of borreliosis in Central Europe. Appl. Environ. Microbiol. 2008, 74:1289-1293.
52. Wang I.N., Dykhuizen D.E., Qiu W., Dunn J.J., Bosler E.M., Luft B.J. Genetic diversity of ospC in a local population of Borrelia burgdorferi sensu stricto. Genetics 1999, 151:15-30.
53. Wilske B., Busch U., Eiffert H., Fingerle V., Pfister H.W., Rossler D., Preac-Mursic V. Diversity of OspA and OspC among cerebrospinal fluid isolates of Borrelia burgdorferi sensu lato from patients with neuroborreliosis in Germany. Med. Microbiol. Immunol. 1996, 184:195-201.
54. Wormser G.P., Brisson D., Liveris D., Hanincová K., Sandigursky S., Nowakowski J., Nadelman R.B., Ludin S., Schwartz I. Borrelia burgdorferi genotype predicts the capacity for hematogenous dissemination during early Lyme disease. J. Infect. Dis. 2008, 198:1358-1364. 10.1086/592279.
55. Xu H., He M., Pang X., Xu Z.C., Piesman J., Yang X.F. Characterization of the highly regulated antigen BBA05 in the enzootic cycle of Borrelia burgdorferi. Infect. Immun. 2010, 78:100-107. 10.1128/IAI.01008-09.
56. Yang Z. PAML 4, phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 2007, 24:1586-1591. 10.1093/molbev/msm088.
57. Zerbino D.R., Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008, 18:821-829. 10.1101/gr.074492.107.