1887

Abstract

Recently, a novel species of the genus Borrelia was identified in Bothriocroton concolor and Ixodes holocyclus ticks from echidnas. Analyses of 16S rRNA and flaB genes identified three closely related genotypes of this bacterium ( Borrelia sp. Aus A-C) that were unique and distinct from previously described borreliae. Phylogenetic analyses of flaB (763 bp), groEL (1537 bp), gyrB (1702 bp) and glpQ (874 bp) gene sequences and concatenated sequences (3585 bp) of three gene loci (16S rRNA, flaB and gyrB) were consistent with previous findings and confirm that this novel species of the genus Borrelia is more closely related to, yet distinct from, the Reptile-associated (REP) and Relapsing Fever (RF) groups. At the flaB locus, genotypes A, B and C shared the highest percentage sequence similarities (87.9, 88 and 87.9 %, respectively) with B.orrelia turcica (REP), whereas at the groEL and gyrB loci, these genotypes were most similar (88.2–89.4 %) to B.orrelia hermsii (RF). At the glpQ locus, genotypes A and B were most similar (85.7 and 85.4 % respectively) to Borrelia sp. Tortoise14H1 (REP). The presence of the glpQ gene, which is absent in the Lyme Borreliosis group spirochaetes, further emphasises that the novel species of the genus Borrelia characterized in the present study does not belong to this group. Phylogenetic analyses at multiple loci produced consistent topographies revealing the monophyletic grouping of this bacterium, therefore providing strong support for its species status. We propose the name ‘Candidatus Borrelia tachyglossi’, and hypothesize that this species of the genus Borrelia may be endemic to Australia. The pathogenic potential of this bacterium is not yet known.

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2017-05-05
2019-12-08
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References

  1. Baranton G, Old IG. The spirochaetes: a different way of life. Bull Inst Pasteur 1995;93:63–95 [CrossRef]
    [Google Scholar]
  2. Ma DY, Giacani L, Centurión-Lara A. The molecular epidemiology of Treponema pallidum subspecies pallidum. Sex Health 2015;12:141–147 [CrossRef][PubMed]
    [Google Scholar]
  3. Mitjà O, Marks M, Konan DJP, Ayelo G, Gonzalez-Beiras C et al. Global epidemiology of yaws: a systematic review. Lancet Glob Health 2015;3:e324e331 [CrossRef][PubMed]
    [Google Scholar]
  4. Takano A, Goka K, Une Y, Shimada Y, Fujita H et al. Isolation and characterization of a novel Borrelia group of tick-borne borreliae from imported reptiles and their associated ticks. Environ Microbiol 2010;12:134–146 [CrossRef][PubMed]
    [Google Scholar]
  5. Margos G, Wilske B, Sing A, Hizo-Teufel C, Cao WC et al. Borrelia bavariensis sp. nov. is widely distributed in Europe and Asia. Int J Syst Evol Microbiol 2013;63:4284–4288 [CrossRef][PubMed]
    [Google Scholar]
  6. Pritt BS, Mead PS, Johnson DKH, Neitzel DF, Respicio-Kingry LB et al. Identification of a novel pathogenic Borrelia species causing Lyme borreliosis with unusually high spirochaetaemia: a descriptive study. Lancet Infect Dis 2016;16:556–564 [CrossRef][PubMed]
    [Google Scholar]
  7. Rudenko N, Golovchenko M, Grubhoffer L, Oliver JH. Updates on Borrelia burgdorferi sensu lato complex with respect to public health. Ticks Tick Borne Dis 2011;2:123–128 [CrossRef][PubMed]
    [Google Scholar]
  8. Takano A, Nakao M, Masuzawa T, Takada N, Yano Y et al. Multilocus sequence typing implicates rodents as the main reservoir host of human-pathogenic Borrelia garinii in japan. J Clin Microbiol 2011;49:2035–2039 [CrossRef][PubMed]
    [Google Scholar]
  9. Gern L, Humair P-F. Ecology of Borrelia burgdorferi sensu lato in Europe. In Gray JS, Kahl O, Lane RS, Stanek G. (editors) Lyme Borreliosis: Biology, Epidemiology and Control Wallingford, UK: CABI Publishing; 2002; pp.149–174[CrossRef]
    [Google Scholar]
  10. Trape JF, Diatta G, Arnathau C, Bitam I, Sarih M et al. The epidemiology and geographic distribution of relapsing fever borreliosis in West and North Africa, with a review of the Ornithodoros erraticus complex (Acari: Ixodida). PLoS One 2013;8:e78473 [CrossRef][PubMed]
    [Google Scholar]
  11. Assous MV, Wilamowski A. Relapsing fever borreliosis in Eurasia—forgotten, but certainly not gone!. Clin Microbiol Infec 2009;15:407–414 [CrossRef]
    [Google Scholar]
  12. Schwan TG, Raffel SJ, Schrumpf ME, Webster LS, Marques AR et al. Tick-borne relapsing fever and Borrelia hermsii, Los Angeles County, California, USA. Emerg Infect Dis 2009;15:1026–1031 [CrossRef][PubMed]
    [Google Scholar]
  13. Fukunaga M, Takahashi Y, Tsuruta Y, Matsushita O, Ralph D et al. Genetic and phenotypic analysis of Borrelia miyamotoi sp. nov., isolated from the ixodid tick Ixodes persulcatus, the vector for lyme disease in Japan. Int J Syst Bacteriol 1995;45:804–810 [CrossRef][PubMed]
    [Google Scholar]
  14. Fraenkel CJ, Garpmo U, Berglund J. Determination of novel Borrelia genospecies in Swedish Ixodes ricinus ticks. J Clin Microbiol 2002;40:3308–3312 [CrossRef][PubMed]
    [Google Scholar]
  15. Mun J, Eisen RJ, Eisen L, Lane RS. Detection of a Borrelia miyamotoi sensu lato relapsing-fever group spirochete from Ixodes pacificus in California. J Med Entomol 2006;43:120–123 [CrossRef][PubMed]
    [Google Scholar]
  16. Scoles GA, Papero M, Beati L, Fish D. A relapsing fever group spirochete transmitted by Ixodes scapularis ticks. Vector Borne Zoonotic Dis 2001;1:21–34 [CrossRef][PubMed]
    [Google Scholar]
  17. Barbour AG, Maupin GO, Teltow GJ, Carter CJ, Piesman J. Identification of an uncultivable Borrelia species in the hard tick Amblyomma americanum: possible agent of a Lyme disease-like illness. J Infect Dis 1996;173:403–409 [CrossRef][PubMed]
    [Google Scholar]
  18. Smith RD, Miranpuri GS, Adams JH, Ahrens EH. Borrelia theileri: isolation from ticks (Boophilus microplus) and tick-borne transmission between splenectomized calves. Am J Vet Res 1985;46:1396–1398[PubMed]
    [Google Scholar]
  19. Lin T, Gao L, Seyfang A, Oliver JH. 'Candidatus Borrelia texasensis', from the American dog tick Dermacentor variabilis. Int J Syst Evol Microbiol 2005;55:685–693 [CrossRef][PubMed]
    [Google Scholar]
  20. Güner ES, Hashimoto N, Kadosaka T, Imai Y, Masuzawa T. A novel, fast-growing Borrelia sp. isolated from the hard tick Hyalomma aegyptium in Turkey. Microbiology 2003;149:2539–2544 [CrossRef][PubMed]
    [Google Scholar]
  21. Güner ES, Watanabe M, Hashimoto N, Kadosaka T, Kawamura Y et al. Borrelia turcica sp. nov., isolated from the hard tick Hyalomma aegyptium in Turkey. Int J Syst Evol Microbiol 2004;54:1649–1652 [CrossRef][PubMed]
    [Google Scholar]
  22. Takano A, Fujita H, Kadosaka T, Konnai S, Tajima T et al. Characterization of reptile-associated Borrelia sp. in the vector tick, Amblyomma geoemydae, and its association with lyme disease and relapsing fever Borrelia spp. Environ Microbiol Rep 2011;3:632–637 [CrossRef][PubMed]
    [Google Scholar]
  23. Chalada MJ, Stenos J, Bradbury RS. Is there a Lyme-like disease in Australia? Summary of the findings to date. One Health 2016;2:42–54 [CrossRef]
    [Google Scholar]
  24. Mulhearn CR. A note on two blood parasites of cattle (Spirochaeta theileri and Bartonella bovis) recorded for the first time in Australia. Aust Vet J 1946;22:118–119 [CrossRef][PubMed]
    [Google Scholar]
  25. Callow LL, Hoyte HMD. Transmission experiments using babesia bigemina, Theileria mutans, Borrelia sp. and the cattle tick. Aust Vet J 1961;37:381–390 [CrossRef]
    [Google Scholar]
  26. Gorrie CJR. Vaccination against spirochaetosis in fowls. Aust Vet J 1950;26:308–315 [CrossRef][PubMed]
    [Google Scholar]
  27. Petney TN, Andrews RH, McDiarmid LA, Dixon BR. Argas persicus sensu stricto does occur in Australia. Parasitol Res 2004;93:296–299 [CrossRef][PubMed]
    [Google Scholar]
  28. Pope JH, Carley JG. Isolation of Borrelia from native rats in north-west Queensland. Aust J Science 1956;19:114
    [Google Scholar]
  29. Carley JG, Pope JH. A new species of Borrelia (B. queenslandica) from Rattus villosissimus in Queensland. Aust J Exp Biol Med Sci 1962;40:255–261 [CrossRef][PubMed]
    [Google Scholar]
  30. Enright MC, Spratt BG. Multilocus sequence typing. Trends Microbiol 1999;7:482–487 [CrossRef][PubMed]
    [Google Scholar]
  31. Urwin R, Maiden MC. Multi-locus sequence typing: a tool for global epidemiology. Trends Microbiol 2003;11:479–487 [CrossRef][PubMed]
    [Google Scholar]
  32. Margos G, Gatewood AG, Aanensen DM, Hanincová K, Terekhova D et al. 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 [CrossRef][PubMed]
    [Google Scholar]
  33. Toledo A, Anda P, Escudero R, Larsson C, Bergstrom S et al. Phylogenetic analysis of a virulent Borrelia species isolated from patients with relapsing fever. J Clin Microbiol 2010;48:2484–2489 [CrossRef][PubMed]
    [Google Scholar]
  34. Schwan TG, Anderson JM, Lopez JE, Fischer RJ, Raffel SJ et al. Endemic foci of the tick-borne relapsing fever spirochete Borrelia crocidurae in Mali, West Africa, and the potential for human infection. PLoS Negl Trop Dis 2012;6:e1924 [CrossRef][PubMed]
    [Google Scholar]
  35. Jacquot M, Bisseux M, Abrial D, Marsot M, Ferquel E et al. High-throughput sequence typing reveals genetic differentiation and host specialization among populations of the Borrelia burgdorferi species complex that infect rodents. PLoS One 2014;9:e88581 [CrossRef][PubMed]
    [Google Scholar]
  36. Jungnick S, Margos G, Rieger M, Dzaferovic E, Bent SJ et al. Borrelia burgdorferi sensu stricto and Borrelia afzelii: population structure and differential pathogenicity. Int J Med Microbiol 2015;305:673–681 [CrossRef][PubMed]
    [Google Scholar]
  37. Loh SM, Gofton AW, Lo N, Gillett A, Ryan UM et al. Novel Borrelia species detected in echidna ticks, Bothriocroton concolor, in Australia. Parasit Vectors 2016;9:339 [CrossRef][PubMed]
    [Google Scholar]
  38. Gofton AW, Oskam CL, Lo N, Beninati T, Wei H et al. Inhibition of the endosymbiont “Candidatus Midichloria mitochondrii” during 16S rRNA gene profiling reveals potential pathogens in Ixodes ticks from Australia. Parasit Vectors 2015;8:345 [CrossRef][PubMed]
    [Google Scholar]
  39. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002;30:3059–3066 [CrossRef][PubMed]
    [Google Scholar]
  40. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004;32:1792–1797 [CrossRef][PubMed]
    [Google Scholar]
  41. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013;30:2725–2729 [CrossRef][PubMed]
    [Google Scholar]
  42. Huelsenbeck JP, Ronquist F. MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 2001;17:754–755 [CrossRef][PubMed]
    [Google Scholar]
  43. Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees.. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November New Orleans, LA: 2010;1–8www.phylo.org/sub_sections/portal/cite.php
    [Google Scholar]
  44. Trinachartvanit W, Hirunkanokpun S, Sudsangiem R, Lijuan W, Boonkusol D et al. Borrelia sp. phylogenetically different from lyme disease- and relapsing fever-related Borrelia spp. in Amblyomma varanense from Python reticulatus. Parasit Vectors 2016;9:359 [CrossRef][PubMed]
    [Google Scholar]
  45. 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 [CrossRef][PubMed]
    [Google Scholar]
  46. Oliver JH, Lin T, Gao L, Clark KL, Banks CW et al. An enzootic transmission cycle of lyme borreliosis spirochetes in the southeastern United States. Proc Natl Acad Sci USA 2003;100:11642–11645 [CrossRef]
    [Google Scholar]
  47. Thompson RC. Parasite zoonoses and wildlife: one health, spillover and human activity. Int J Parasitol 2013;43:1079–1088 [CrossRef][PubMed]
    [Google Scholar]
  48. Roberts FHS. Australian Ticks, 2nd ed. Melbourne: CSIRO; 1970
    [Google Scholar]
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