BACKGROUND: The controversy surrounding the potential impact of birds in spirochete transmission dynamics and their capacity to serve as a reservoir has existed for a long time. The majority of analyzed bird species are able to infect larval ticks with Borrelia. Dispersal of infected ticks due to bird migration is a key to the establishment of new foci of Lyme borreliosis. The dynamics of infection in birds supports the mixing of different species, the horizontal exchange of genetic information, and appearance of recombinant genotypes. METHODS: Four Borrelia burgdorferi sensu lato strains were cultured from Ixodes minor larvae and four strains were isolated from Ixodes minor nymphs collected from a single Carolina Wren (Thryothorus ludovicianus). A multilocus sequence analysis that included 16S rRNA, a 5S-23S intergenic spacer region, a 16S-23S internal transcribed spacer, flagellin, p66, and ospC separated 8 strains into 3 distinct groups. Additional multilocus sequence typing of 8 housekeeping genes, clpA, clpX, nifS, pepX, pyrG, recG, rplB, and uvrA was used to resolve the taxonomic status of bird-associated strains. RESULTS: Results of analysis of 14 genes confirmed that the level of divergence among strains is significantly higher than what would be expected for strains within a single species. The presence of cross-species recombination was revealed: Borrelia burgdorferi sensu stricto housekeeping gene nifS was incorporated into homologous locus of strain, previously assigned to B. americana. CONCLUSIONS: Genetically diverse Borrelia strains are often found within the same tick or same vertebrate host, presenting a wide opportunity for genetic exchange. We report the cross-species recombination that led to incorporation of a housekeeping gene from the B. burgdorferi sensu stricto strain into a homologous locus of another bird-associated strain. Our results support the hypothesis that recombination maintains a majority of sequence polymorphism within Borrelia populations because of the re-assortment of pre-existing sequence variants. Even if our findings of broad genetic diversity among 8 strains cultured from ticks that fed on a single bird could be the exception rather than the rule, they support the theory that the diversity and evolution of LB spirochetes is driven mainly by the host.

Biology Centre AS CR Institute of Parasitology České Budějovice 37005 Czech Republic

Zobrazit více v PubMed

Gern L. Borrelia burgdorferi sensu lato, the agent of Lyme borreliosis: life in the wilds. Parasite. 2008;15:244–247. doi: 10.1051/parasite/2008153244. PubMed DOI

Anderson JF, Magnarelli LA, Stafford KC 3rd. Bird-feeding ticks trans stadially transmit Borrelia burgdorferi that infect Syrian hamsters. J Wildl Dis. 1990;26:1–10. doi: 10.7589/0090-3558-26.1.1. PubMed DOI

Manweiler SA, Lane RS, Bloc WM, Morrison ML. Survey of birds and lizards for ixodid ticks (Acari) and spirochetal infection in northern California. J Med Entomol. 1990;27:1011–1015. PubMed

McLean RG, Ubico SR, Hughes CA, Engstrom SM, Johnson RC. Isolation and characterization of Borrelia burgdorferi from the blood of a bird captured in the Saint Croix River Halley, USA [abstract 235] Arlington, USA: Proceedings of the Vth International Conference on Lyme Borreliosis; 1992.

Olsen B, Jaenson TG, Bunikis J, Noppa L, Bergström S. The Lyme borreliosis spirochete found in ticks parasitizing sea birds [abstract 285] Arlington, USA: Proceedings of the Vth International Conference on Lyme Borreliosis; 1992.

Brinkerhoff RJ, Folsom-O’Keefe CM, Tsao K, Diuk-Wasser MA. Do birds affect Lyme disease risk? Range explansion of the vector-borne pathogen Borrelia burgdorferi. Front Ecol Environ. 2011;9:103–110. doi: 10.1890/090062. DOI

Norte AC, Ramos JA, Gern L, Núncio MS, Lopes de Carvalho I. Birds as reservoirs for Borrelia burgdorferi s.l. in Western Europe: circulation of B. turdi and other genospecies in bird-tick cycles in Portugal. Environ Microbiol. 2013;15:386–397. doi: 10.1111/j.1462-2920.2012.02834.x. PubMed DOI

Heylen D, Tijsse E, Fonville M, Matthysen E, Sprong H. Transmission dynamics of Borrelia burgdorferi s.l. in a bird tick community. Environ Microbiol. 2013;15:663–673. doi: 10.1111/1462-2920.12059. PubMed DOI

Ginsberg HS, Buckley PA, Balmforth MG, Zhioua E, Mitra S, Buckley FG. Reservoir competence of native North American birds for the lyme disease spirochete, Borrelia burgdorfieri. J Med Entomol. 2005;42:445–449. doi: 10.1603/0022-2585(2005)042[0445:RCONNA]2.0.CO;2. PubMed DOI

Rand PW, Lacombe EH, Smith RP, Ficker J. Participation of birds (Aves) in the emergence of Lyme disease in southern Maine. J Med Entomol. 1998;35:270–276. PubMed

Hamer SA, Hickling GJ, Sidge JL, Rosen ME, Walker ED, Tsao JI. Diverse Borrelia burgdorferi strains in a bird-tick cryptic cycle. Appl Environ Microbiol. 2011;77:1999–2007. doi: 10.1128/AEM.02479-10. PubMed DOI PMC

Olsen B, Duffy DC, Jaenson TG, Gylfe A, Bonnedahl J, Bergström S. Transhemispheric exchange of Lyme disease spirochetes by seabirds. J Clin Microbiol. 1995;33:3270–3274. PubMed PMC

Comstedt P, Bergström S, Olsen B, Garpmo U, Marjavaara L, Mejlon H, Barbour AG, Bunikis J. Migratory passerine birds as reservoirs of Lyme borreliosis in Europe. Emerg Infect Dis. 2006;12:1087–1095. doi: 10.3201/eid1207.060127. PubMed DOI PMC

Poupon MA, Lommano E, Humair PF, Douet V, Rais O, Schaad M, Jenni L, Gern L. Prevalence of Borrelia burgdorferi sensu lato in ticks collected from migratory birds in Switzerland. Appl Environ Microbiol. 2006;72:976–979. doi: 10.1128/AEM.72.1.976-979.2006. PubMed DOI PMC

Ogden NH, Lindsay LR, Hanincová K, Barker IK, Bigras-Poulin M, Charron DF, Heagy A, Francis CM, O’Callaghan CJ, Schwartz I, Thompson RA. Role of migratory birds in introduction and range expansion of Ixodes scapularis ticks and of Borrelia burgdorferi and Anaplasma phagocytophilum in Canada. Appl Environ Microbiol. 2008;74:1780–1790. doi: 10.1128/AEM.01982-07. PubMed DOI PMC

Anderson JF, Johnson RC, Magnarelli LA, Hyde FW. Involvement of birds in the epidemiology of the Lyme disease agent Borrelia burgdorferi. Infect Immun. 1986;51:394–396. PubMed PMC

Hanincová K, Taragelová V, Koci J, Schäfer SM, Hails R, Ullmann AJ, Piesman J, Labuda M, Kurtenbach K. Association of Borrelia garinii and B. valaisiana with songbirds in Slovakia. Appl Environ Microbiol. 2003;69:2825–2830. doi: 10.1128/AEM.69.5.2825-2830.2003. PubMed DOI PMC

Baranton G, Postic D, Saint Girons I, Boerlin P, Piffaretti JC, Assous M, Grimont PA. Delineation of Borrelia burgdorferi sensu stricto, Borrelia garinii sp. nov., and group VS461 associated with Lyme borreliosis. Int J Syst Bacteriol. 1992;42:378–383. doi: 10.1099/00207713-42-3-378. PubMed DOI

Canica MM, Nato F, du Merle L, Mazie JC, Baranton G, Postic D. Monoclonal antibodies for identification of Borrelia afzelii sp. nov. associated with late cutaneous manifestations of Lyme borreliosis. Scand J Infect Dis. 1993;25:441–448. doi: 10.3109/00365549309008525. PubMed DOI

Chu CY, Liu W, Jiang BG, Wang DM, Jiang WJ, Zhao QM, Zhang PH, Wang ZX, Tang GP, Yang H, Cao WC. Novel genospecies of Borrelia burgdorferi sensu lato from rodents and ticks in southwestern China. J Clin Microbiol. 2008;46:3130–3133. doi: 10.1128/JCM.01195-08. PubMed DOI PMC

Fukunaga M, Hamase A, Okada K, Nakao M. Borrelia tanukii sp. nov. and Borrelia turdae sp. nov. found from ixodid ticks in Japan: rapid species identification by 16S rRNA gene-targeted PCR analysis. Microbiol Immunol. 1996;40:877–881. doi: 10.1111/j.1348-0421.1996.tb01154.x. PubMed DOI

Kawabata H, Masuzawa T, Yanagihara Y. Genomic analysis of Borrelia japonica sp. nov. isolated from Ixodes ovatus in Japan. Microbiol Immunol. 1993;37:843–848. doi: 10.1111/j.1348-0421.1993.tb01714.x. PubMed DOI

Le Fleche A, Postic D, Girardet K, Peter O, Baranton G. Characterization of Borrelia lusitaniae sp. nov. by 16S ribosomal DNA sequence analysis. Int J Syst Bacteriol. 1997;47:921–925. doi: 10.1099/00207713-47-4-921. PubMed DOI

Marconi RT, Liveris D, Schwartz I. 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. 1995;33:2427–2434. PubMed PMC

Margos G, Hojgaard A, Lane RS, Cornet M, Fingerle V, Rudenko N, Ogden N, Aanensen DM, Fish D, Piesman J. Multilocus sequence analysis of Borrelia bissettii strains from North America reveals a new Borrelia species, Borrelia kurtenbachii. Ticks Tick Borne Dis. 2010;1:151–158. doi: 10.1016/j.ttbdis.2010.09.002. PubMed DOI PMC

Margos G, Vollmer SA, Kornet 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. doi: 10.1128/AEM.00116-09. PubMed DOI PMC

Masuzawa T, Takada N, Kudeken M, Fukui T, Yano Y, Ishiguro F, Kawamura Y, Imai Y, Ezaki T. Borrelia sinica sp. nov., a Lyme disease-related Borrelia species isolated in China. Int J Syst Evol Microbiol. 2001;51:1817–1824. doi: 10.1099/00207713-51-5-1817. PubMed DOI

Postic D, Garnier M, 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;297:263–271. doi: 10.1016/j.ijmm.2007.01.006. PubMed DOI

Postic D, Ras NM, Lane RS, Hendson M, Baranton G. Expanded diversity among Californian Borrelia isolates and description of Borrelia bissettii sp. nov. (formerly Borrelia group DN127) J Clin Microbiol. 1998;36:3497–3504. PubMed PMC

Richter D, Postic D, Sertour N, Livey I, Matuschka FR, Baranton G. 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. 2006;56:873–881. doi: 10.1099/ijs.0.64050-0. PubMed DOI

Rudenko N, Golovchenko M, Grubhoffer L, Oliver JH Jr. Borrelia carolinensis sp. nov., a new (14th) member of the Borrelia burgdorferi sensu lato complex from the southeastern region of the United States. J Clin Microbiol. 2009;47:134–141. doi: 10.1128/JCM.01183-08. PubMed DOI PMC

Rudenko N, Golovchenko M, Lin T, Gao L, Grubhoffer L, Oliver JH Jr. Delineation of a new species of the Borrelia burgdorferi sensu lato complex, Borrelia americana sp. nov. J Clin Microbiol. 2009;47:3875–3880. doi: 10.1128/JCM.01050-09. PubMed DOI PMC

Wang G, van Dam AP, Le Fleche A, Postic D, Peter O, Baranton G, de Boer R, Spanjaard L, Dankert J. Genetic and phenotypic analysis of Borrelia valaisiana sp. nov. (Borrelia genomic groups VS116 and M19) Int J Syst Bacteriol. 1997;47:926–932. doi: 10.1099/00207713-47-4-926. PubMed DOI

Casjens SR, Fraser-Liggett CM, Mongodin EF, Qiu WG, Dunn JJ, Luft BJ, Schutzer SE. Whole genome sequence of an unusual Borrelia burgdorferi sensu lato isolate. J Bacteriol. 2011;193:1489–1490. doi: 10.1128/JB.01521-10. PubMed DOI PMC

Urwin R, Maiden MC. Multi-locus sequence typing: a tool for global epidemiology. Trends Microbiol. 2003;11:479–487. doi: 10.1016/j.tim.2003.08.006. PubMed DOI

Kurtenbach K, De Michelis S, Etti S, Schäfer SM, Sewell HS, Brade V, Kraiczy P. Host association of Borrelia burgdorferi sensu lato–the key role of host complement. Trends Microbiol. 2002;10:74–79. doi: 10.1016/S0966-842X(01)02298-3. PubMed DOI

Kurtenbach K, De Michelis S, Sewell HS, Etti S, Schäfer SM, Holmes E, Hails R, Collares-Pereira M, Santos-Reis M, Hanincová K, Labuda M, Bormane A, Donaghy M. The key roles of selection and migration in the ecology of Lyme borreliosis. Int J Med Microbiol. 2002;33:152–154. PubMed

Skerka C, Brade V, Zipfel PF. Further characterization of complement regulator-acquiring surface proteins of Borrelia burgdorferi. Infect Immun. 2001;69:7800–7809. doi: 10.1128/IAI.69.12.7800-7809.2001. PubMed DOI PMC

Kraiczy P, Skerka C, Kirschfink M, Zipfel PF, Brade V. Mechanism of complement resistance of pathogenic Borrelia burgdorferi isolates. Int Immunopharmacol. 2001;1:393–401. doi: 10.1016/S1567-5769(00)00041-2. PubMed DOI

Kurtenbach K, Schäfer SM, Sewell HS, Peacey M, Hoodless A, Nuttall PA, Randolph SE. Differential survival of Lyme borreliosis spirochetes in ticks that feed on birds. Infect Immun. 2002;70:5893–5895. doi: 10.1128/IAI.70.10.5893-5895.2002. PubMed DOI PMC

Stevenson B, El-Hage N, Hines MA, Miller JC, Babb K. Differential binding of host complement inhibitor factor H by Borrelia burgdorferi Erp surface proteins: a possible mechanism underlying the expansive host range of Lyme disease spirochetes. Infect Immun. 2002;70:491–497. doi: 10.1128/IAI.70.2.491-497.2002. PubMed DOI PMC

Eggers CH, Kimmel BJ, Bono JL, Elias AF, Rosa P, Samuels DS. Transduction by phiBB-1, a bacteriophage of Borrelia burgdorferi. J Bacteriol. 2001;183:4771–4778. doi: 10.1128/JB.183.16.4771-4778.2001. PubMed DOI PMC

Kurtenbach K, Hanincová K, Tsao JI, Margos G, Fish D, Ogden NH. Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nat Rev Microbiol. 2006;4:660–669. doi: 10.1038/nrmicro1475. PubMed DOI

Brisson D, Dykhuizen DE. ospC diversity in Borrelia burgdorferi: different hosts are different niches. Genetics. 2004;168:713–722. doi: 10.1534/genetics.104.028738. PubMed DOI PMC

Brisson D, Vandermause MF, Meece JK, Reed KD, Dykhuizen DE. Evolution of northeastern and midwestern Borrelia burgdorferi, United States. Emerg Infect Dis. 2010;16:911–917. doi: 10.3201/eid1606.090329. PubMed DOI PMC

Guttman DS, Wang PW, Wang IN, Bosler EM, Luft BJ, Dykhuizen DE. Multiple infections of Ixodes scapularis ticks by Borrelia burgdorferi as revealed by single-strand conformation polymorphism analysis. J Clin Microbiol. 1996;34:652–656. PubMed PMC

Haven J, Vargas LC, Mongodin EF, Xue V, Hernandez Y, Pagan P, Fraser-Liggett CM, Schutzer SE, Luft BJ, Casjens SR, Qiu WG. Pervasive recombination and sympatric genome diversification driven by frequency-dependent selection in Borrelia burgdorferi, the Lyme disease bacterium. Genetics. 2011;189:951–966. doi: 10.1534/genetics.111.130773. PubMed DOI PMC

Postic D, Assous MV, Grimont PA, Baranton G. Diversity of Borrelia burgdorferi sensu lato evidenced by restriction fragment length polymorphism of rrf (5S)-rrl (23S) intergenic spacer amplicons. Int J Syst Bacteriol. 1994;44:743–752. doi: 10.1099/00207713-44-4-743. PubMed DOI

Güner ES, Hashimoto N, Takada N, Kaneda K, Omak Y, Masuzawa T. First isolation and characterization of Borrelia burgdorferi sensu lato strains from Ixodes ricinus ticks in Turkey. J Med Microbiol. 2003;52:807–813. doi: 10.1099/jmm.0.05205-0. PubMed DOI

Clark K, Hendricks A, Burge D. Molecular identification and analysis of Borrelia burgdorferi sensu lato in lizards in the southeastern United States. Appl Environ Microbiol. 2005;71:2616–2625. doi: 10.1128/AEM.71.5.2616-2625.2005. PubMed DOI PMC

Bunikis J, Garpmo U, Tsao J, Berglund J, Fish D, Barbour AG. Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe. Microbiology. 2004;150:1741–1755. doi: 10.1099/mic.0.26944-0. PubMed DOI

Margos G, Gatewood AG, Aanensen DM, Hanincová K, Terekhova D, Vollmer SA, Cornet M, Piesman J, Donaghy M, Bormane A, Hurn MA, Feil EJ, Fish D, Casjens S, Wormser GP, Schwartz I, Kurtenbach K. MLST of housekeeping genes captures geographic population structure and suggests a European origin of Borrelia burgdorferi. Proc Natl Acad Sci USA. 2008;105:8730–8735. doi: 10.1073/pnas.0800323105. PubMed DOI PMC

Bikandi J, San Millán R, Rementeria A, Garaizar J. In silico analysis of complete bacterial genomes: PCR, AFLP-PCR and endonuclease restriction. Bioinformatics. 2004;20:798–799. doi: 10.1093/bioinformatics/btg491. PubMed DOI

Hoogstraal H. Birds as tick hosts and as reservoirs and disseminators of tickborne infectious agents. Wiad Parazytol. 1972;18:703–706. PubMed

Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23:2947–2948. doi: 10.1093/bioinformatics/btm404. PubMed DOI

Nylander JAA. MrModeltest v2.3. Program distributed by the author. Uppsala, Sweden: Evolutionary Biology Centre: Uppsala University; 2008.

Akaike H. A new look at the statistical model identification. IEEE Trans Autom Contr. 1974;19:716–723. doi: 10.1109/TAC.1974.1100705. DOI

Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP. Bayesian inference of phylogeny and its impact on evolutionary biology. Science. 2001;294:2310–2314. doi: 10.1126/science.1065889. PubMed DOI

Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–1574. doi: 10.1093/bioinformatics/btg180. PubMed DOI

Nylander JAA, Wilgenbusch JC, Warren DL, Swofford DL. AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics. 2008;24:581–583. doi: 10.1093/bioinformatics/btm388. PubMed DOI

Larget BR, Kotha SK, Dewey CN, Ané C. BUCKy: gene tree/species tree reconciliation with Bayesian concordance analysis. Bioinformatics. 2010;26:2910–2911. doi: 10.1093/bioinformatics/btq539. PubMed DOI

Allman ES, Degnan JH, Rhodes JA. Identifying the rooted species tree from the distribution of unrooted gene trees under the coalescent. J Math Biol. 2011;62:833–862. doi: 10.1007/s00285-010-0355-7. PubMed DOI

Ané C, Larget B, Baum DA, Smith SD, Rokas A. Bayesian estimation of concordance among gene trees. Mol Biol Evol. 2007;24:412–426. PubMed

Rudenko N, Golovchenko M, Hönig V, Mallátová N, Krbková L, Mikulásek P, Fedorova N, Belfiore NM, Grubhoffer L, Lane RS, Oliver JH Jr. Detection of Borrelia burgdorferi sensu stricto ospC alleles associated with human Lyme borreliosis worldwide in non-human-biting tick Ixodes affinis and rodent hosts in southeastern United States. Appl Environ Microbiol. 2013;79:1444–1453. doi: 10.1128/AEM.02749-12. PubMed DOI PMC

Aanensen DM, Spratt BG. The multilocus sequence typing network: mlst.net. Nucleic Acids Res. 2005;33(Web Server issue):W728–W733. PubMed PMC

Margos G, Vollmer SA, Ogden NH, Fish D. Population genetics, taxonomy, phylogeny and evolution of Borrelia burgdorferi sensu lato. Infect Genet Evol. 2011;11:1545–1563. doi: 10.1016/j.meegid.2011.07.022. PubMed DOI PMC

Qiu WG, Dykhuizen DE, Acosta MS, Luft BJ. Geographic uniformity of the Lyme disease spirochete (Borrelia burgdorferi) and its shared history with tick vector (Ixodes scapularis) in the northeastern United States. Genetics. 2002;160:833–849. PubMed PMC

Wang IN, Dykhuizen DE, Qiu W, Dunn JJ, Bosler EM, Luft BJ. Genetic diversity of ospC in a local population of Borrelia burgdorferi sensu stricto. Genetics. 1999;151:15–30. PubMed PMC

Brisson D, Dykhuizen DE. A modest model explains the distribution and abundance of Borrelia burgdorferi strains. Am J Trop Med Hyg. 2006;74:615–622. PubMed PMC

Brinkerhoff RJ, Bent SJ, Folsom-O’Keefe CM, Tsao K, Hoen AG, Barbour AG, Diuk-Wasser MA. Genotypic diversity of Borrelia burgdorferi strains detected in Ixodes scapularis larvae collected from North American songbirds. Appl Environ Microbiol. 2010;76:8265–8268. doi: 10.1128/AEM.01585-10. PubMed DOI PMC

Humair PF, Postic D, Wallich R, Gern L. An avian reservoir (Turdus merula) of the Lyme borreliosis spirochetes. Zentralbl Bakteriol. 1998;287:521–538. PubMed

Ishiguro F, Takada N, Masuzawa T, Fukui T. Prevalence of Lyme disease Borrelia spp. in ticks from migratory birds on the Japanese mainland. Appl Environ Microbiol. 2000;66:982–986. doi: 10.1128/AEM.66.3.982-986.2000. PubMed DOI PMC

Kurtenbach K, Peacey M, Rijpkema SG, Hoodless AN, Nuttall PA, Randolph SE. Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Appl Environ Microbiol. 1998;64:1169–1174. PubMed PMC

Miyamoto K, Nakao M, Fujita H, Sato F. The Ixodid ticks on migratory birds in Japan and the isolation of Lyme disease spirochetes from bird-feeding ticks. Jpn J Sanit Zool. 1993;44:315–326.

Miyamoto K, Sato Y, Okada K, Fukunaga M, Sato F. Competence of a migratory bird, red-bellied thrush (Turdus chrysolaus), as an avian reservoir for the Lyme disease spirochetes in Japan. Acta Trop. 1997;65:43–51. doi: 10.1016/S0001-706X(97)00651-7. PubMed DOI

Nakao M, Miyamoto K, Fukunaga M. Lyme disease spirochetes in Japan: enzootic transmission cycles in birds, rodents, and Ixodes persulcatus ticks. J Infect Dis. 1994;170:878–882. doi: 10.1093/infdis/170.4.878. PubMed DOI

Smith RP Jr, Rand PW, Lacombe EH, Morris SR, Holme DW, Caporale DA. Role of bird migration in the long-distance dispersal of Ixodes dammini, the vector of Lyme disease. J Infect Dis. 1996;174:221–224. doi: 10.1093/infdis/174.1.221. PubMed DOI

Weisbrod AR, Johnson RC. Lyme disease and migrating birds in the Saint Croix River Valley. Appl Environ Microbiol. 1989;55:1921–1924. PubMed PMC

Morshed MG, Scott JD, Fernando K, Beati L, Mazerolle DF, Geddes G, Durden LA. Migratory songbirds disperse ticks across Canada, and first isolation of the Lyme disease spirochete, Borrelia burgdorferi, from the avian tick, Ixodes auritulus. J Parasitol. 2005;91:780–790. doi: 10.1645/GE-3437.1. PubMed DOI

Humair PF, Turrian N, Aeschlimann A, Gern L. Ixodes ricinus immatures on birds in a focus of Lyme borreliosis. Folia Parasitol (Praha) 1993;40:237–242. PubMed

Olsén B, Jaenson TG, Bergström S. Prevalence of Borrelia burgdorferi sensu lato-infected ticks on migrating birds. Appl Environ Microbiol. 1995;61:3082–3087. PubMed PMC

Rollend L, Fish D, Childs JE. Transovarial transmission of Borrelia spirochetes by Ixodes scapularis: a summary of the literature and recent observations. Ticks Tick Borne Dis. 2013;4:46–51. doi: 10.1016/j.ttbdis.2012.06.008. PubMed DOI

Kipp S, Goedecke A, Dorn W, Wilske B, Fingerle V. Role of birds in Thuringia, Germany, in the natural cycle of Borrelia burgdorferi sensu lato, the Lyme disease spirochaete. Int J Med Microbiol. 2006;40(296):125–128. PubMed

Yuval B, Spielman A. Duration and regulation of the developmental cycle of Ixodes dammini (Acari: Ixodidae) J Med Entomol. 1990;27:196–201. PubMed

Kuo MM, Lane RS, Giclas PC. A comparative study of mammalian and reptilian alternative pathway of complement-mediated killing of the Lyme disease spirochete (Borrelia burgdorferi) J Parasitol. 2000;86:1223–1228. PubMed

Lane RS, Quistad GB. Borreliacidal factor in the blood of the western fence lizard (Sceloporus occidentalis) J Parasitol. 1998;84:29–34. doi: 10.2307/3284524. PubMed DOI

Nelson DR, Rooney S, Miller NJ, Mather TN. Complement-mediated killing of Borrelia burgdorferi by non-immune sera from sika deer. J Parasitol. 2000;86:1232–1238. PubMed

Van Dam AP, Oei A, Jaspars R, Fijen C, Wilske B, Spanjaard L, Dankert J. Complement-mediated serum sensitivity among spirochetes that cause Lyme disease. Infect Immun. 1997;65:1228–1236. PubMed PMC

Morlon H, Kemps BD, Plotkin JB, Brisson D. Explosive radiation of a bacterial species group. Evolution. 2012;66:2577–2586. doi: 10.1111/j.1558-5646.2012.01598.x. PubMed DOI PMC

Banks CW, Oliver JH Jr, Philips JB, Clark KL. Life cycle of Ixodes minor (Acari: Ixodidae) in the laboratory. J Med Entomol. 1998;35:496–499. PubMed

Rudenko N, Golovchenko M, Grubhoffer L, Oliver JH Jr. The rare ospC allele L of Borrelia burgdorferi sensu stricto, commonly found among samples collected in a coastal plain area of the southeastern United States, is associated with Ixodes affinis ticks and local rodent hosts Peromyscus gossypinus and Sigmodon hispidus. Appl Environ Microbiol. 2013;79:1403–1406. doi: 10.1128/AEM.03362-12. PubMed DOI PMC

Beklemishev AB, Dobrotvorsky AK, Piterina AV, Ivanov ID, Nomokonova NY, Livanova NN. Detection and typing of Borrelia burgdorferi sensu lato genospecies in Ixodes persulcatus ticks in West Siberia, Russia. FEMS Microbiol Lett. 2003;227:157–161. doi: 10.1016/S0378-1097(03)00581-0. PubMed DOI

Chu CY, He J, Wang JB, Hasen GW, Zhang PH, Wu XM, Zhao QM, Jiang BG, Gao Y, Cao WC. Investigation on Borrelia burgdorferi sensu lato in ticks and rodents collected in Da Xing-An Mountains Forest areas of China. Zhonghua Liu Xing Bing Xue Za Zhi. 2006;27:681–684. PubMed

Demaerschalck I, Ben Messaoud A, De Kesel M, Hoyois B, Lobet Y, Hoet P, Bigaignon G, Bollen A, Godfroid E. Simultaneous presence of different Borrelia burgdorferi genospecies in biological fluids of Lyme disease patients. J Clin Microbiol. 1995;33:602–608. PubMed PMC

Fichet-Calvet E, Jomâa I, Ben Ismail R, Ashford RW. Patterns of infection of haemoparasites in the fat sand rat, Psammomys obesus, in Tunisia, and effect on the host. Ann Trop Med Parasitol. 2000;94:55–68. doi: 10.1080/00034980057617. PubMed DOI

Oksi J, Marjamäki M, Koski K, Nikoskelainen J, Viljanen MK. Bilateral facial palsy and meningitis caused by Borrelia double infection. Lancet. 1995;345:1583–1584. PubMed

Rudenko N, Golovchenko M, Růzek D, Piskunova N, Mallátová N, Grubhoffer L. Molecular detection of Borrelia bissettii DNA in serum samples from patients in the Czech Republic with suspected borreliosis. FEMS Microbiol Lett. 2009;292:274–281. doi: 10.1111/j.1574-6968.2009.01498.x. PubMed DOI

Rudenko N, Golovchenko M, Nemec J, Volkaert J, Mallátová N, Grubhoffer L. Improved method of detection and molecular typing of Borrelia burgdorferi sensu lato in clinical samples by polymerase chain reaction without DNA purification. Folia Microbiol (Praha) 2005;50:31–39. doi: 10.1007/BF02931291. PubMed DOI

Vennestrøm J, Egholm H, Jensen PM. Occurrence of multiple infections with different Borrelia burgdorferi genospecies in Danish Ixodes ricinus nymphs. Parasitol Int. 2008;57:32–37. doi: 10.1016/j.parint.2007.07.004. PubMed DOI

Gene encoding the CTP synthetase as an appropriate molecular tool for identification and phylogenetic study of the family Bifidobacteriaceae

Zobrazit více v PubMed

GENBANK
HM140981, HM146415, HM802215, HM802216, HM802219, HM802220, HM802221, HM802222, HM802223, HM802224, HM802225, HM802226, HM802227, HM802228, HM802229, HM802230, HM802231, HM802232, HM802233, HM802234, HM802235, HM802236, HM802237, HM802238, HM852908, HM852909, HM852910, HM852913, HQ012504, HQ012505, HQ012507, HQ012508, HQ012509