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A phylogenomic and molecular marker based proposal for the division of the genus Borrelia into two genera: the emended genus Borrelia containing only the members of the relapsing fever Borrelia, and the genus Borreliella gen. nov. containing the members of the Lyme disease Borrelia (Borrelia burgdorferi sensu lato complex)

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Abstract

The genus Borrelia contains two groups of organisms: the causative agents of Lyme disease and their relatives and the causative agents of relapsing fever and their relatives. These two groups are morphologically indistinguishable and are difficult to distinguish biochemically. In this work, we have carried out detailed comparative genomic analyses on protein sequences from 38 Borrelia genomes to identify molecular markers in the forms of conserved signature inserts/deletions (CSIs) that are specifically found in the Borrelia homologues, and conserved signature proteins (CSPs) which are uniquely present in Borrelia species. Our analyses have identified 31 CSIs and 82 CSPs that are uniquely shared by all sequenced Borrelia species, providing molecular markers for this group of organisms. In addition, our work has identified 7 CSIs and 21 CSPs which are uniquely found in the Lyme disease Borrelia species and eight CSIs and four CSPs that are specific for members of the relapsing fever Borrelia group. Additionally, 38 other CSIs, in proteins which are uniquely found in Borrelia species, also distinguish these two groups of Borrelia. The identified CSIs and CSPs provide novel and highly specific molecular markers for identification and distinguishing between the Lyme disease Borrelia and the relapsing fever Borrelia species. We also report the results of average nucleotide identity (ANI) analysis on Borrelia genomes and phylogenetic analysis for these species based upon 16S rRNA sequences and concatenated sequences for 25 conserved proteins. These analyses also support the distinctness of the two Borrelia clades. On the basis of the identified molecular markers, the results from ANI and phylogenetic studies, and the distinct pathogenicity profiles and arthropod vectors used by different Borrelia spp. for their transmission, we are proposing a division of the genus Borrelia into two separate genera: an emended genus Borrelia, containing the causative agents of relapsing fever and a novel genus, Borreliella gen. nov., containing the causative agents of Lyme disease.

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References

  • Adams DA, Gallagher KM, Jajosky RA, Kriseman J, Sharp P, Anderson WJ, Aranas AE, Mayes M, Wodajo MS, Onweh DH et al (2013) Summary of notifiable diseases—United States, 2011. MMWR Morb Mortal Wkly Rep 60(53):1–117

    PubMed  Google Scholar 

  • Adeolu M, Gupta RS (2013) Phylogenomics and molecular signatures for the order Neisseriales: proposal for division of the order Neisseriales into the emended family Neisseriaceae and Chromobacteriaceae fam nov. Antonie Van Leeuwenhoek Int J G 104(1):1–24

    Article  Google Scholar 

  • Ahmod NZ, Gupta RS, Shah HN (2011) Identification of a Bacillus anthracis specific indel in the yeaC gene and development of a rapid pyrosequencing assay for distinguishing B. anthracis from the B. cereus group. J Microbiol Methods 87(3):278–285

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Baranton G, Postic D, Saint Girons I, Boerlin P, Piffaretti J-C, Assous M, Grimont PAD (1992) Delineation of Borrelia burgdorferi Sensu Stricto, Borrelia garinii sp. nov., and Group VS461 associated with Lyme borreliosis. Int J Syst Bacteriol 42(3):378–383

    Article  CAS  PubMed  Google Scholar 

  • Barbour AG (1984) Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med 57(4):521

    CAS  PubMed Central  PubMed  Google Scholar 

  • Barbour AG (2005) Relapsing fever. In: Goodman JL, Dennis DT, Sonenshine DE (eds) Tick-borne diseases of humans. ASM Press, Washington, pp 268–291

    Chapter  Google Scholar 

  • Barbour AG, Miller SC (2014) Genome sequence of Borrelia parkeri, an agent of enzootic relapsing fever in Western North America. Genome Announc 2(1):e00018

    Google Scholar 

  • Bergey DH (1925) Bergey’s manual of determinative bacteriology, 2nd edn. The Williams and Wilkins Co, Baltimore

    Google Scholar 

  • Bhandari V, Gupta RS (2012) Molecular signatures for the phylum Synergistetes and some of its subclades. Antonie Van Leeuwenhoek 102(4):517–540

    Article  CAS  PubMed  Google Scholar 

  • Bhandari V, Gupta RS (2014) Molecular signatures for the phylum (class) Thermotogae and a proposal for its division into three orders (Thermotogales, Kosmotogales ord. nov. and Petrotogales ord. nov.) containing four families (Thermotogaceae, Fervidobacteriaceae fam. nov., Kosmotogaceae fam. nov. and Petrotogaceae fam. nov.) and a new genus Pseudothermotoga gen. nov. with five new combinations. Antonie Van Leeuwenhoek 105(1):143–168

    Article  PubMed  Google Scholar 

  • Bhandari V, Ahmod NZ, Shah HN, Gupta RS (2013) Molecular signatures for Bacillus species: demarcation of the Bacillus subtilis and Bacillus cereus clades in molecular terms and proposal to limit the placement of new species into the genus Bacillus. Int J Syst Evol Microbiol 63:2712–2726

    Article  CAS  PubMed  Google Scholar 

  • Brenner EV, Kurilshikov AM, Stronin OV, Fomenko NV (2012) Whole-genome sequencing of Borrelia garinii BgVir, isolated from Taiga ticks (Ixodes persulcatus). J Bacteriol 194(20):5713

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Canica MM, Du Merle L, Mazie JC, Baranton G, Postic D (1994) Borrelia afzelii sp. nov. Validation of the publication of new names and new combinations previously effectively published outside the IJSB, list no 48. Int J Syst Bacteriol 44:182–183

    Article  Google Scholar 

  • Casjens SR, Fraser-Liggett CM, Mongodin EF, Qiu WG, Dunn JJ, Luft BJ, Schutzer SE (2011a) Whole genome sequence of an unusual Borrelia burgdorferi sensu lato isolate. J Bacteriol 193(6):1489–1490

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Casjens SR, Mongodin EF, Qiu WG, Dunn JJ, Luft BJ, Fraser-Liggett CM, Schutzer SE (2011b) Whole-genome sequences of two Borrelia afzelii and two Borrelia garinii Lyme disease agent isolates. J Bacteriol 193(24):6995–6996

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17(4):540–552

    Article  CAS  PubMed  Google Scholar 

  • Chaconas G (2005) Hairpin telomeres and genome plasticity in Borrelia: all mixed up in the end. Mol Microbiol 58(3):625–635

    Article  CAS  PubMed  Google Scholar 

  • Chaconas G, Kobryn K (2010) Structure, function, and evolution of linear replicons in Borrelia. Annu Rev Microbiol 64:185–202

    Article  CAS  PubMed  Google Scholar 

  • Charlebois RL, Doolittle WF (2004) Computing prokaryotic gene ubiquity: rescuing the core from extinction. Genome Res 14(12):2469–2477

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ciccarelli FD, Doerks T, Von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311(5765):1283–1287

    Article  CAS  PubMed  Google Scholar 

  • Cutler SJ (2010) Relapsing fever: a forgotten disease revealed. J Appl Microbiol 108(4):1115–1122

    Article  CAS  PubMed  Google Scholar 

  • Dai Q, Restrepo BI, Porcella SF, Raffel SJ, Schwan TG, Barbour AG (2006) Antigenic variation by Borrelia hermsii occurs through recombination between extragenic repetitive elements on linear plasmids. Mol Microbiol 60(6):1329–1343

    Article  CAS  PubMed  Google Scholar 

  • Dunaj J, Moniuszko A, Zajkowska J, Pancewicz S (2013) The role of PCR in diagnostics of Lyme borreliosis. Przegl Epidemiol 67(1): 35–39, 119–123

    Google Scholar 

  • Elbir H, Gimenez G, Robert C, Bergström S, Cutler S, Raoult D, Drancourt M (2012) Complete genome sequence of Borrelia crocidurae. J Bacteriol 194(14):3723–3724

    Article  PubMed Central  PubMed  Google Scholar 

  • Elbir H, Larsson P, Normark J, Upreti M, Korenberg E, Larsson C, Bergstrom S (2014a) Genome sequence of the Asiatic species Borrelia persica. Genome Announc 2(1):e01127

  • Elbir H, Larsson P, Upreti M, Normark J, Bergstrom S (2014b) Genome sequence of the relapsing fever borreliosis species Borrelia hispanica. Genome Announc 2(1):e01171

    Google Scholar 

  • Fraser CM, Casjens S, Huang WM, Sutton GG, Clayton R, Lathigra R, White O, Ketchum KA, Dodson R, Hickey EK et al (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390(6660):580–586

    Article  CAS  PubMed  Google Scholar 

  • Fukunaga M, Okada K, Nakao M, Konishi T, Sato Y (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(4):898–905

    Article  CAS  PubMed  Google Scholar 

  • Fukunaga M, Hamase A, Okada K, Nakao M (1997a) Borrelia tanukii sp. nov. Validation of the publication of new names and new combinations previously effectively published outside the IJSB, list no 63. Int J Syst Bacteriol 47:1274

    Article  Google Scholar 

  • Fukunaga M, Hamase A, Okada K, Nakao M (1997b) Borrelia turdi sp. nov. Validation of the publication of new names and new combinations previously effectively published outside the IJSB, list no 63. Int J Syst Bacteriol 47:1274

    Article  Google Scholar 

  • Gao B, Gupta R (2007) Phylogenomic analysis of proteins that are distinctive of Archaea and its main subgroups and the origin of methanogenesis. BMC Genom 8(1):86

    Article  Google Scholar 

  • Gao B, Gupta RS (2012a) Microbial systematics in the post-genomics era. Antonie Van Leeuwenhoek 101(1):45–54

    Article  PubMed  Google Scholar 

  • Gao B, Gupta RS (2012b) Phylogenetic framework and molecular signatures for the main clades of the phylum Actinobacteria. Microbiol Mol Biol Rev 76(1):66–112

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Glöckner G, Lehmann R, Romualdi A, Pradella S, Schulte-Spechtel U, Schilhabel M, Wilske B, Sühnel J, Platzer M (2004) Comparative analysis of the Borrelia garinii genome. Nucleic Acids Res 32(20):6038–6046

    Article  PubMed Central  PubMed  Google Scholar 

  • Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57(1):81–91

    Article  CAS  PubMed  Google Scholar 

  • Gupta RS (1998) Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol Mol Biol Rev 62(4):1435

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gupta RS (2010) Applications of conserved indels for understanding microbial phylogeny. In: Oren A, Papke RT (eds) Molecular phylogeny of microorganisms. Caister Academic Press, Norfolk, pp 135–150

    Google Scholar 

  • Gupta RS, Griffiths E (2006) Chlamydiae-specific proteins and indels: novel tools for studies. Trends Microbiol 14(12):527–535

    Article  CAS  PubMed  Google Scholar 

  • Gupta RS, Lali R (2013) Molecular signatures for the phylum Aquificae and its different clades: proposal for division of the phylum Aquificae into the emended order Aquificales, containing the families Aquificaceae and Hydrogenothermaceae, and a new order Desulfurobacteriales ord. nov., containing the family Desulfurobacteriaceae. Antonie Van Leeuwenhoek 104(3):349–368

    Article  PubMed  Google Scholar 

  • Gupta RS, Chander P, George S (2013a) Phylogenetic framework and molecular signatures for the class Chloroflexi and its different clades; proposal for division of the class Chloroflexia class. nov. [corrected] into the suborder Chloroflexineae subord. nov., consisting of the emended family Oscillochloridaceae and the family Chloroflexaceae fam. nov., and the suborder Roseiflexineae subord. nov., containing the family Roseiflexaceae fam. nov. Antonie Van Leeuwenhoek 103(1):99–119

    Article  PubMed  Google Scholar 

  • Gupta RS, Mahmood S, Adeolu M (2013b) A phylogenomic and molecular signature based approach for characterization of the phylum Spirochaetes and its major clades: proposal for a taxonomic revision of the phylum. Front Microbiol 4:217

    PubMed Central  PubMed  Google Scholar 

  • Harris JK, Kelley ST, Spiegelman GB, Pace NR (2003) The genetic core of the universal ancestor. Genome Res 13(3):407–412

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hue F, Ghalyanchi Langeroudi A, Barbour AG (2013) Chromosome sequence of Borrelia miyamotoi, an uncultivable tick-borne agent of human infection. Genome Announc 1(5):e00713

    Google Scholar 

  • Ibba M, Bono JL, Rosa PA, Soll D (1997) Archaeal-type lysyl-tRNA synthetase in the Lyme disease spirochete Borrelia burgdorferi. Proc Natl Acad Sci USA 94(26):14383–14388

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23(10):403

    Article  CAS  PubMed  Google Scholar 

  • Jiang B, Yao H, Tong Y, Yang X, Huang Y, Jiang J, Cao W (2012a) Genome sequence of Borrelia garinii strain NMJW1, isolated from China. J Bacteriol 194(23):6660–6661

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jiang BG, Zheng YC, Tong YG, Jia N, Huo QB, Fan H, Ni XB, Ma L, Yang XF, Jiang JF et al (2012b) Genome sequence of Borrelia afzelii Strain HLJ01, isolated from a patient in China. J Bacteriol 194(24):7014–7015

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Johnson RC, Schmid GP, Hyde FW, Steigerwalt AG, Brenner DJ (1984) Borrelia burgdorferi sp. nov.: etiologic agent of Lyme disease. Int J Syst Bacteriol 34(4):496–497

    Article  Google Scholar 

  • Kawabata H, Masuzawa T, Yanagihara Y (1994) Borrelia japonica sp. nov. Validation of the publication of new names and new combinations previously effectively published outside the IJSB, list no 50. Int J Syst Bacteriol 44:595

    Article  Google Scholar 

  • Lapage SP, Sneath PHA, Lessel EF, Skerman VBD, Seeliger HPR, Clark WA (1992) International code of nomenclature of bacteria: bacteriological code, 1990 revision. ASM Press International Union of Microbiological Societies, Washington

    Google Scholar 

  • Le Fleche A, Postic D, Girardet K, Peter O, Baranton G (1997) Characterization of Borrelia lusitaniae sp. nov. by 16S ribosomal DNA sequence analysis. Int J Syst Bacteriol 47(4):921–925

    Article  PubMed  Google Scholar 

  • Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25(7):1307–1320

    Article  CAS  PubMed  Google Scholar 

  • Lescot M, Audic S, Robert C, Nguyen TT, Blanc G, Cutler SJ, Wincker P, Couloux A, Claverie JM, Raoult D (2008) The genome of Borrelia recurrentis, the agent of deadly louse-borne relapsing fever, is a degraded subset of tick-borne Borrelia duttonii. PLoS Genet 4(9):e1000185

    Article  PubMed Central  PubMed  Google Scholar 

  • Lindgren E, Jaenson TG (2006) Lyme borreliosis in Europe: influences of climate and climate change, epidemiology, ecology and adaptation measures. WHO Regional Office for Europe, Copenhagen

    Google Scholar 

  • Ljostad U, Mygland A (2013) Chronic Lyme; diagnostic and therapeutic challenges. Acta Neurol Scand 127 Suppl(196):38–47

    Google Scholar 

  • Margos G, Vollmer SA, Cornet M, Garnier M, Fingerle V, Wilske B, Bormane A, Vitorino L, Collares-Pereira M, Drancourt M et al (2009) A new Borrelia species defined by multilocus sequence analysis of housekeeping genes. Appl Environ Microbiol 75(16):5410–5416

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Margos G, Vollmer SA, Ogden NH, Fish D (2011) Population genetics, taxonomy, phylogeny and evolution of Borrelia burgdorferi sensu lato. Infect Genet Evol 11(7):1545–1563

    Article  PubMed Central  PubMed  Google Scholar 

  • Margos G, Piesman J, Lane RS, Ogden NH, Sing A, Straubinger RK, Fingerle V (2013a). Borrelia kurtenbachii sp. nov.: a widely distributed member of the Borrelia burgdorferi sensu lato species complex in North America. Int J Syst Evol Microbiol 64(Pt 1):128–30. doi:10.1099/ijs.0.054593-0

    Google Scholar 

  • Margos G, Wilske B, Sing A, Hizo-Teufel C, Cao WC, Chu C, Scholz H, Straubinger RK, Fingerle V (2013b) Borrelia bavariensis sp. nov. is widely distributed in Europe and Asia. Int J Syst Evol Microbiol 63(Pt 11):4284–4288

    Article  PubMed  Google Scholar 

  • Masuzawa T, Takada N, Kudeken M, Fukui T, Yano Y, Ishiguro F, Kawamura Y, Imai Y, Ezaki T (2001) Borrelia sinica sp. nov., a lyme disease-related Borrelia species isolated in China. Int J Syst Evol Microbiol 51(Pt 5):1817–1824

    Article  CAS  PubMed  Google Scholar 

  • Naushad HS, Lee B, Gupta RS (2014) Conserved signature indels and signature proteins as novel tools for understanding microbial phylogeny and systematics: identification of molecular signatures that are specific for the phytopathogenic genera Dickeya, Pectobacterium and Brenneria. Int J Syst Evol Microbiol 64(2):366–383

    Article  PubMed  Google Scholar 

  • NCBI (2014) NCBI genome database. http://www.ncbi.nlm.nih.gov/genome/

  • Parte AC (2014) LPSN—list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 42(D1):D613–D616

    Google Scholar 

  • Paster BJ (2011) Phylum XV. Spirochaetes Garrity and Holt 2001. In Brenner DJ, Krieg NR, Garrity GM, Staley JT (eds) Bergey’s Manual of Systematic Bacteriology, 2nd edn, vol 3. Springer, New York, pp 471–471 (reprinted from: not in File)

  • Postic D, Edlinger C, Richaud C, Grimont F, Dufresne Y, Perolat P, Baranton G, Grimont PAD (1990) Two genomic species in Borrelia burgdorferi. Res Microbiol 141(4):465–475

    Article  CAS  PubMed  Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41(D1):D590–D596

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ras NM, Lascola B, Postic D, Cutler SJ, Rodhain F, Baranton G, Raoult D (1996) Phylogenesis of relapsing fever Borrelia spp. Int J Syst Bacteriol 46(4):859–865

    Article  CAS  PubMed  Google Scholar 

  • Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci 106(45):19126–19131

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Richter D, Postic D, Sertour N, Livey I, Matuschka FR, Baranton G (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(Pt 4):873–881

    Article  CAS  PubMed  Google Scholar 

  • Rokas A, Holland PWH (2000) Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15(11):454–459

    Article  PubMed  Google Scholar 

  • Rokas A, Williams BL, King N, Carroll SB (2003) Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425(6960):798–804

    Article  CAS  PubMed  Google Scholar 

  • Rosselló-Mora R (2006) DNA–DNA reassociation methods applied to microbial taxonomy and their critical evaluation. In: Stackebrandt E (ed) Molecular identification, systematics, and population structure of prokaryotes. Springer, Berlin, pp 23–50

  • Rudenko N, Golovchenko M, Lin T, Gao L, Grubhoffer L, Oliver JH Jr (2010) Borrelia americana sp. nov. List of new names and new combinations previously effectively, but not validly, published, list no 135. Int J Syst Evol Microbiol 60:1985–1986

    Article  Google Scholar 

  • Rudenko N, Golovchenko M, Grubhoffer L, Oliver JH Jr (2011) Borrelia carolinensis sp. nov., a novel species of the Borrelia burgdorferi sensu lato complex isolated from rodents and a tick from the south-eastern USA. Int J Syst Evol Microbiol 61(Pt 2):381–383

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schutzer SE, Fraser-Liggett CM, Casjens SR, Qiu WG, Dunn JJ, Mongodin EF, Luft BJ (2011) Whole-genome sequences of thirteen isolates of Borrelia burgdorferi. J Bacteriol 193(4):1018–1020

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schutzer SE, Fraser-Liggett CM, Qiu WG, Kraiczy P, Mongodin EF, Dunn JJ, Luft BJ, Casjens SR (2012) Whole-genome sequences of Borrelia bissettii, Borrelia valaisiana, and Borrelia spielmanii. J Bacteriol 194(2):545–546

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Segata N, Bornigen D, Morgan XC, Huttenhower C (2013) PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat Commun 4:2304

    Article  PubMed Central  PubMed  Google Scholar 

  • Skerman VBD, McGowan V, Sneath PHA (1980) Approved lists of bacterial names. Int J Syst Bacteriol 30(1):225–420

    Article  Google Scholar 

  • Swellengrebel NH (1907) Sur la cytologie comparée des spirochètes et des spirilles. Ann Inst Pasteur (Paris) 21:562–586

    Google Scholar 

  • Takano A, Goka K, Une Y, Shimada Y, Fujita H, Shiino T, Watabane H, Kawabata H (2010) Isolation and characterization of a novel Borrelia group of tick-borne borreliae from imported reptiles and their associated ticks. Environ Microbiol 12(1):134–146

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    Article  CAS  PubMed  Google Scholar 

  • Tavaré S (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. In Miura RM (ed) Lectures on mathematics in the life sciences, 17th edn. American Mathematical Society, Providence, pp 57–86 (reprinted from: not in file)

  • Thompson CC, Chimetto L, Edwards RA, Swings J, Stackebrandt E, Thompson FL (2013) Microbial genomic taxonomy. BMC Genom 14(1):913

    Article  Google Scholar 

  • Valsangiacomo C, Balmelli T, Piffaretti JC (1997) A phylogenetic analysis of Borrelia burgdorferi sensu lato based on sequence information from the hbb gene, coding for a histone-like protein. Int J Syst Bacteriol 47(1):1–10

    Article  CAS  PubMed  Google Scholar 

  • Vinuesa P (2010) Multilocus sequence analysis and bacterial species phylogeny estimation. In: Oren A, Papke RT (eds) Molecular phylogeny of microorganisms. Caister Academic Press, Norfolk, pp 41–64

    Google Scholar 

  • Wang G, Schwartz I (2011) Genus II. Borrelia Swellengrebel 1907, 582AL. In: Brenner DJ, Krieg NR, Garrity GM, Staley JT (eds) Bergey’s manual of systematic bacteriology, vol 3, 2nd edn. Springer, New York, pp 484–498

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang G, van Dam AP, Schwartz I, Dankert J (1999) Molecular typing of Borrelia burgdorferi sensu lato: taxonomic, epidemiological, and clinical implications. Clin Microbiol Rev 12(4):633–653

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wright WF, Riedel DJ, Talwani R, Gilliam BL (2012) Diagnosis and management of Lyme disease. Am Fam Physician 85(11):1086–1093

    PubMed  Google Scholar 

  • Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, Kunin V, Goodwin L, Wu M, Tindall BJ (2009) A phylogeny-driven genomic encyclopaedia of bacteria and archaea. Nature 462(7276):1056–1060

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Adeolu, M., Gupta, R.S. A phylogenomic and molecular marker based proposal for the division of the genus Borrelia into two genera: the emended genus Borrelia containing only the members of the relapsing fever Borrelia, and the genus Borreliella gen. nov. containing the members of the Lyme disease Borrelia (Borrelia burgdorferi sensu lato complex). Antonie van Leeuwenhoek 105, 1049–1072 (2014). https://doi.org/10.1007/s10482-014-0164-x

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