1887

Abstract

Lyme borreliosis is a vector-borne infection caused by bacteria under the sensu lato complex, both in Europe and North America. Differential gene expression at different times throughout its infectious cycle allows the spirochete to survive very diverse environments within different mammalian hosts as well as the tick vector. To date, the vast majority of data about spirochetal proteins and their functions are from genetic studies carried out on North American strains of a single species, i.e. . The whole-genome sequences recently obtained for several European species/strains make it feasible to adapt and use genetic techniques to study inherent differences between them. This review highlights the crucial need to undertake independent studies of genospecies within Europe, given their varying genetic content and pathogenic potential, and differences in clinical manifestation.

Funding
This study was supported by the:
  • Ryan Oliver Marino Rego , Grantová Agentura České Republiky , (Award 17-21244S)
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000899
2020-03-03
2020-06-04
Loading full text...

Full text loading...

/deliver/fulltext/micro/166/5/428.html?itemId=/content/journal/micro/10.1099/mic.0.000899&mimeType=html&fmt=ahah

References

  1. Drecktrah D, Samuels DS. Genetic manipulation of Borrelia spp. Curr Top Microbiol Immunol 2018; 415:113–140
    [Google Scholar]
  2. Fraser CM, Casjens S, Huang WM, Sutton GG, Clayton R et al. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi . Nature 1997; 390:580–586 [CrossRef]
    [Google Scholar]
  3. Di L, Pagan PE, Packer D, Martin CL, Akther S et al. BorreliaBase: a phylogeny-centered browser of Borrelia genomes. BMC Bioinformatics 2014; 15:233 [CrossRef]
    [Google Scholar]
  4. Casjens SR, Di L, Akther S, Mongodin EF, Luft BJ et al. Primordial origin and diversification of plasmids in Lyme disease agent bacteria. BMC Genomics 2018; 19:218 [CrossRef]
    [Google Scholar]
  5. Margos G, Fingerle V, Reynolds S. Borrelia bavariensis: vector switch, niche invasion, and geographical spread of a tick-borne bacterial parasite. Front Ecol Evol Epub ahead of print 2019; 7: [CrossRef]
    [Google Scholar]
  6. Stanek G, Wormser GP, Gray J, Strle F et al. Lyme borreliosis. The Lancet 2012; 379:461–473 [CrossRef]
    [Google Scholar]
  7. Pritt BS, Respicio-Kingry LB, Sloan LM, Schriefer ME, Replogle AJ 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; 66:4878–4880 [CrossRef]
    [Google Scholar]
  8. Strle F, Picken RN, Cheng Y et al. Clinical findings for patients with Lyme borreliosis caused by Borrelia burgdorferi sensu lato with genotypic and phenotypic similarities to strain 25015. Clin Infect Dis Off Publ Infect Dis Soc Am 1997; 25:273–280
    [Google Scholar]
  9. Margos G, Lane RS, Fedorova N, Koloczek J, Piesman J et al. Borrelia bissettiae sp. nov. and Borrelia californiensis sp. nov. prevail in diverse enzootic transmission cycles. Int J Syst Evol Microbiol 2016; 66:1447–1452 [CrossRef]
    [Google Scholar]
  10. Collares-Pereira M, Couceiro S, Franca I, Kurtenbach K, Schafer SM et al. First isolation of Borrelia lusitaniae from a human patient. J Clin Microbiol 2004; 42:1316–1318 [CrossRef]
    [Google Scholar]
  11. Diza E, Papa A, Vezyri E, Tsounis S, Milonas I et al. Borrelia valaisiana in cerebrospinal Fluid. Emerg Infect Dis 2004; 10:1692–1693 [CrossRef]
    [Google Scholar]
  12. Margos G, Sing A, Fingerle V. Published data do not support the notion that Borrelia valaisiana is human pathogenic. Infection 2017; 45:567–569 [CrossRef]
    [Google Scholar]
  13. Tilly K, Rosa PA, Stewart PE. Biology of infection with Borrelia burgdorferi . Infect Dis Clin North Am 2008; 22:217–234 [CrossRef]
    [Google Scholar]
  14. Strnad M, Hönig V, Růžek D, Grubhoffer L, Rego ROM et al. Europe-Wide meta-analysis of Borrelia burgdorferi sensu lato prevalence in questing Ixodes ricinus ticks. Appl Environ Microbiol 2017; 83: [CrossRef]
    [Google Scholar]
  15. Stanek G, Fingerle V, Hunfeld K-P, Jaulhac B, Kaiser R et al. Lyme borreliosis: clinical case definitions for diagnosis and management in Europe. Clin Microbiol Infect 2011; 17:69–79 [CrossRef]
    [Google Scholar]
  16. Mead PS. Epidemiology of Lyme disease. Infect Dis Clin North Am 2015; 29:187–210 [CrossRef]
    [Google Scholar]
  17. Stanek G, Strle F. Lyme borreliosis–from tick bite to diagnosis and treatment. FEMS Microbiol Rev 2018; 42:233–258 [CrossRef]
    [Google Scholar]
  18. Strle F, Ružić-Sabljić E, Cimperman J, Lotric-Furlan S, Maraspin V et al. Comparison of findings for patients with Borrelia garinii and Borrelia afzelii isolated from cerebrospinal fluid. Clinical Infectious Diseases 2006; 43:704–710 [CrossRef]
    [Google Scholar]
  19. Maraspin V, Nahtigal Klevišar M, Ružić-Sabljić E, Lusa L, Strle F et al. Borrelial Lymphocytoma in adult patients. Clinical Infectious Diseases 2016; 63:914–921 [CrossRef]
    [Google Scholar]
  20. Rijpkema SGT, Tazelaar DJ, Molkenboer MJCH, Noordhoek GT, Plantinga G et al. Detection of Borrelia afzelii, Borrelia burgdorferi sensu stricto, Borrelia garinii and group VS116 by PCR in skin biopsies of patients with erythema migrans and acrodermatitis chronica atrophicans. Clinical Microbiology and Infection 1997; 3:109–116 [CrossRef]
    [Google Scholar]
  21. 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]
    [Google Scholar]
  22. Kuehn BM. CDC estimates 300 000 US cases of Lyme disease annually. JAMA 2013; 310:1110 [CrossRef]
    [Google Scholar]
  23. Rego ROM, Trentelman JJA, Anguita J, Nijhof AM, Sprong H et al. Counterattacking the tick bite: towards a rational design of anti-tick vaccines targeting pathogen transmission. Parasit Vectors 2019; 12:229 [CrossRef]
    [Google Scholar]
  24. Smith R, Takkinen J. Lyme borreliosis: Europe-wide coordinated surveillance and action needed?. Euro Surveill 2006; 11:E060622.1 [CrossRef][PubMed]
    [Google Scholar]
  25. Stricker RB, Johnson L. Lyme disease: call for a “Manhattan Project” to combat the epidemic. PLoS Pathog 2014; 10:e1003796 [CrossRef]
    [Google Scholar]
  26. 177570 CAB International W 2011; United K eng, Halperin JJ 178318 (ed). Lyme disease: an evidence-based approach. http://agris.fao.org/agris-search/search.do?recordID=XF2015037262 29 May 2019
  27. Strnad M, Grubhoffer L, Rego ROM. Novel targets and strategies to combat borreliosis. Appl Microbiol Biotechnol 2020; 104:1915–1925 [CrossRef][PubMed]
    [Google Scholar]
  28. Burgdorfer W, Barbour A, Hayes S, Benach J, Grunwaldt E et al. Lyme disease-a tick-borne spirochetosis?. Science 1982; 216:1317–1319 [CrossRef]
    [Google Scholar]
  29. Burgdorfer W, Barbour AG, Anderson JR, Lane RS, Gresbrink RA et al. The Western black-legged tick, Ixodes pacificus: a vector of Borrelia burgdorferi . Am J Trop Med Hyg 1985; 34:925–930 [CrossRef]
    [Google Scholar]
  30. Laaksonen M, Klemola T, Feuth E, Sormunen JJ, Puisto A et al. Tick-borne pathogens in Finland: comparison of Ixodes ricinus and I. persulcatus in sympatric and parapatric areas. Parasit Vectors 2018; 11:556 [CrossRef]
    [Google Scholar]
  31. Pal U, de Silva AM, Montgomery RR, Fish D, Anguita J et al. Attachment of Borrelia burgdorferi within Ixodes scapularis mediated by outer surface protein A. J Clin Invest 2000; 106:561–569 [CrossRef]
    [Google Scholar]
  32. Schwan TG, Piesman J, Golde WT, Dolan MC, Rosa PA et al. Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc Natl Acad Sci U S A 1995; 92:2909–2913 [CrossRef]
    [Google Scholar]
  33. Dunham-Ems SM, Caimano MJ, Pal U, Wolgemuth CW, Eggers CH et al. Live imaging reveals a biphasic mode of dissemination of Borrelia burgdorferi within ticks. J Clin Invest 2009; 119:3652–3665 [CrossRef]
    [Google Scholar]
  34. Radolf JD, Caimano MJ, Stevenson B, Hu LT et al. Of ticks, mice and men: understanding the dual-host lifestyle of Lyme disease spirochaetes. Nat Rev Microbiol 2012; 10:87–99 [CrossRef]
    [Google Scholar]
  35. Strnad M, Elsterová J, Schrenková J, Vancová M, Rego ROM et al. Correlative cryo-fluorescence and cryo-scanning electron microscopy as a straightforward tool to study host-pathogen interactions. Sci Rep 2015; 5:18029 [CrossRef]
    [Google Scholar]
  36. Pospisilova T, Urbanova V, Hes O, Kopacek P, Hajdusek O et al. Tracking of Borrelia afzelii transmission from Infected Ixodes ricinus Nymphs to Mice. Infect Immun 2019; 87:e00896–18 [CrossRef]
    [Google Scholar]
  37. Schwan TG, 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
    [Google Scholar]
  38. de Silva AM, Fikrig E. Growth and migration of Borrelia burgdorferi in Ixodes ticks during blood feeding. Am J Trop Med Hyg 1995; 53:397–404 [CrossRef]
    [Google Scholar]
  39. Ohnishi J, Piesman J, de Silva AM. Antigenic and genetic heterogeneity of Borrelia burgdorferi populations transmitted by ticks. Proc Natl Acad Sci U S A 2001; 98:670–675 [CrossRef]
    [Google Scholar]
  40. Piesman J. Dispersal of the Lyme disease spirochete Borrelia burgdorferi to salivary glands of feeding nymphal Ixodes scapularis (Acari: Ixodidae). J Med Entomol 1995; 32:519–521 [CrossRef]
    [Google Scholar]
  41. Piesman J, Schneider BS, Zeidner NS. Use of quantitative PCR to measure density of Borrelia burgdorferi in the midgut and salivary glands of feeding tick vectors. J Clin Microbiol 2001; 39:4145–4148 [CrossRef]
    [Google Scholar]
  42. des Vignes F, Piesman J, Heffernan R, Schulze TL, Stafford III KC et al. Effect of tick removal on transmission of Borrelia burgdorferi and Ehrlichia phagocytophila by Ixodes scapularis nymphs. J Infect Dis 2001; 183:773–778 [CrossRef]
    [Google Scholar]
  43. Lebet N, Gern L. Histological examination of Borrelia burgdorferi infections in unfed Ixodes ricinus nymphs. Exp Appl Acarol 1994; 18:177–183 [CrossRef]
    [Google Scholar]
  44. Leuba-Garcia S, Kramer MD, Wallich R, Gern L et al. Characterization of Borrelia burgdorferi isolated from different organs of Ixodes ricinus ticks collected in nature. Zentralblatt für Bakteriologie 1994; 280:468–475 [CrossRef]
    [Google Scholar]
  45. Kahl O, Janetzki-Mittmann C, Gray JS, Jonas R, Stein J et al. Risk of infection with Borrelia burgdorferi sense lato for a host in relation to the duration of nymphal Ixodes ricinus feeding and the method of tick removal. Zentralblatt für Bakteriologie 1998; 287:41–52 [CrossRef]
    [Google Scholar]
  46. Crippa M, Rais O, Gern L. Investigations on the mode and dynamics of transmission and infectivity of Borrelia burgdorferi sensu stricto and Borrelia afzelii in Ixodes ricinus ticks. Vector Borne Zoonotic Dis Larchmt N 2002; 2:3–9 [CrossRef]
    [Google Scholar]
  47. Piesman J, Oliver JR, Sinsky RJ. Growth kinetics of the Lyme disease spirochete (Borrelia burgdorferi) in vector ticks (Ixodes dammini). Am J Trop Med Hyg 1990; 42:352–357 [CrossRef]
    [Google Scholar]
  48. Samuels DS, Mach KE, Garon CF. Genetic transformation of the Lyme disease agent Borrelia burgdorferi with coumarin-resistant gyrB. J Bacteriol 1994; 176:6045–6049 [CrossRef]
    [Google Scholar]
  49. Stewart PE, Hoff J, Fischer E, Krum JG, Rosa PA et al. Genome-wide transposon mutagenesis of Borrelia burgdorferi for identification of phenotypic mutants. Appl Environ Microbiol 2004; 70:5973–5979 [CrossRef]
    [Google Scholar]
  50. Lin T, Gao L, Zhang C, Odeh E, Jacobs MB et al. Analysis of an ordered, comprehensive STM mutant library in infectious Borrelia burgdorferi: insights into the genes required for mouse infectivity. PLoS One 2012; 7:e47532 [CrossRef]
    [Google Scholar]
  51. Lin TYao, Lin T et al. Transposon mutagenesis as an approach to improved understanding of Borrelia pathogenesis and biology. Front Cell Infect Microbiol 4: [CrossRef]
    [Google Scholar]
  52. Lin T, Gao L, Zhao X, Liu J, Norris SJ et al. Mutations in the Borrelia burgdorferi flagellar type III secretion system genes fliH and fliI profoundly affect spirochete flagellar assembly, morphology, motility, structure, and cell division. mBio 2015; 6: [CrossRef]
    [Google Scholar]
  53. Bestor A, Stewart PE, Jewett MW, Sarkar A, Tilly K et al. Use of the cre-lox recombination system to investigate the lp54 gene requirement in the infectious cycle of Borrelia burgdorferi. Infect Immun 2010; 78:2397–2407 [CrossRef]
    [Google Scholar]
  54. Sohaskey CD, Arnold C, Barbour AG. Analysis of promoters in Borrelia burgdorferi by use of a transiently expressed reporter gene. J Bacteriol 1997; 179:6837–6842 [CrossRef]
    [Google Scholar]
  55. Hayes BM, Jewett MW, Rosa PA. lacZ reporter system for use in Borrelia burgdorferi. Appl Environ Microbiol 2010; 76:7407–7412 [CrossRef]
    [Google Scholar]
  56. Hayes BM, Dulebohn DP, Sarkar A et al. Regulatory protein BBD18 of the Lyme disease spirochete: essential role during tick acquisition?. mBio 5:
    [Google Scholar]
  57. Blevins JS, Revel AT, Smith AH, Bachlani GN, Norgard MV et al. Adaptation of a luciferase gene reporter and lac expression system to Borrelia burgdorferi . Appl Environ Microbiol 2007; 73:1501–1513 [CrossRef]
    [Google Scholar]
  58. Skare JT, Shaw DK, Trzeciakowski JP, Hyde JA et al. In vivo imaging demonstrates that Borrelia burgdorferi ospC is uniquely expressed temporally and spatially throughout experimental infection. PLoS One 11:e0162501 [CrossRef]
    [Google Scholar]
  59. Carroll JA, Stewart PE, Rosa P, Elias AF, Garon CF et al. An enhanced GFP reporter system to monitor gene expression in Borrelia burgdorferi . Microbiology 2003; 149:1819–1828 [CrossRef]
    [Google Scholar]
  60. Jutras BL, Bowman A, Brissette CA, Adams CA, Verma A et al. EbfC (YbaB) is a new type of bacterial nucleoid-associated protein and a global regulator of gene expression in the Lyme disease spirochete. J Bacteriol 2012; 194:3395–3406 [CrossRef]
    [Google Scholar]
  61. Whetstine CR, Slusser JG, Zückert WR. Development of a single-plasmid-based regulatable gene expression system for Borrelia burgdorferi. Appl Environ Microbiol 2009; 75:6553–6558 [CrossRef]
    [Google Scholar]
  62. Gilbert MA, Morton EA, Bundle SF, Samuels DS et al. Artificial regulation of ospC expression in Borrelia burgdorferi . Mol Microbiol 2007; 63:1259–1273 [CrossRef]
    [Google Scholar]
  63. Ouyang Z, Zhou J, Norgard MV. Synthesis of rpoS is dependent on a putative enhancer binding protein Rrp2 in Borrelia burgdorferi. PLoS One 2014; 9:e96917 [CrossRef]
    [Google Scholar]
  64. Stewart PE, Thalken R, Bono JL, Rosa P et al. Isolation of a circular plasmid region sufficient for autonomous replication and transformation of infectious Borrelia burgdorferi . Mol Microbiol 2001; 39:714–721 [CrossRef]
    [Google Scholar]
  65. Elias AF, Bono JL, Kupko III JJ, Stewart PE, Krum JG et al. New antibiotic resistance cassettes suitable for genetic studies in Borrelia burgdorferi . J Mol Microbiol Biotechnol 2003; 6:29–40 [CrossRef]
    [Google Scholar]
  66. Hübner A, Yang X, Nolen DM, Popova TG, Cabello FC et al. Expression of Borrelia burgdorferi OspC and DbpA is controlled by a RpoN-RpoS regulatory pathway. Proc Natl Acad Sci U S A 2001; 98:12724–12729 [CrossRef]
    [Google Scholar]
  67. Winslow C, Coburn J. Recent discoveries and advancements in research on the Lyme disease spirochete Borrelia burgdorferi. F1000 . Research 8:
    [Google Scholar]
  68. Hillman C, Stewart PE, Strnad M, Stone H, Starr T et al. Visualization of spirochetes by labeling membrane proteins with fluorescent biarsenical dyes. Front Cell Infect Microbiol 9: [CrossRef]
    [Google Scholar]
  69. Siegel C, Schreiber J, Haupt K, Skerka C, Brade V et al. Deciphering the ligand-binding sites in the Borrelia burgdorferi complement regulator-acquiring surface protein 2 required for interactions with the human immune regulators factor H and factor H-like protein 1. J Biol Chem 2008; 283:34855–34863 [CrossRef]
    [Google Scholar]
  70. Hallström T, Siegel C, Mörgelin M, Kraiczy P, Skerka C et al. Cspa from Borrelia burgdorferi inhibits the terminal complement pathway. mBio 2013; 4: [CrossRef]
    [Google Scholar]
  71. Fingerle V, Goettner G, Gern L, Wilske B, Schulte-Spechtel U et al. Complementation of a Borrelia afzelii OspC mutant highlights the crucial role of OspC for dissemination of Borrelia afzelii in Ixodes ricinus. Int J Med Microbiol IJMM 2007; 297:97–107 [CrossRef]
    [Google Scholar]
  72. Tilly K, Krum JG, Bestor A, Jewett MW, Grimm D et al. Borrelia burgdorferi OspC protein required exclusively in a crucial early stage of mammalian infection. Infect Immun 2006; 74:3554–3564 [CrossRef]
    [Google Scholar]
  73. Bontemps-Gallo S, Lawrence KA, Richards CL, Gherardini FC et al. Genomic and phenotypic characterization of Borrelia afzelii BO23 and Borrelia garinii CIP 103362. PLoS One 2018; 13:e0199641 [CrossRef]
    [Google Scholar]
  74. Vechtova P, Sterbova J, Sterba J, Vancova M, Rego ROM et al. A bite so sweet: the glycobiology interface of tick-host-pathogen interactions. Parasit Vectors 2018; 11:594 [CrossRef]
    [Google Scholar]
  75. Salo J, Loimaranta V, Lahdenne P, Viljanen MK, Hytönen J et al. Decorin binding by DbpA and B of Borrelia garinii, Borrelia afzelii, and Borrelia burgdorferi sensu stricto. J Infect Dis 2011; 204:65–73 [CrossRef]
    [Google Scholar]
  76. Salo J, Pietikäinen A, Söderström M, Auvinen K, Salmi M et al. Flow-Tolerant adhesion of a bacterial pathogen to human endothelial cells through interaction with biglycan. J Infect Dis. 2016; 213:1623–1631 [CrossRef]
    [Google Scholar]
  77. Hart T, Nguyen NTT, Nowak NA, Zhang F, Linhardt RJ et al. Polymorphic factor H-binding activity of CspA protects Lyme borreliae from the host complement in feeding ticks to facilitate tick-to-host transmission. PLoS Pathog 2018; 14:e1007106 [CrossRef]
    [Google Scholar]
  78. Lin Y-P, Benoit V, Yang X, Martínez-Herranz R, Pal U et al. Strain-Specific variation of the decorin-binding adhesin DbpA influences the tissue tropism of the Lyme disease spirochete. PLoS Pathog 2014; 10:e1004238 [CrossRef]
    [Google Scholar]
  79. Shi Y, Xu Q, McShan K, Liang FT et al. Both decorin-binding proteins A and B are critical for the overall virulence of Borrelia burgdorferi. Infect Immun 2008; 76:1239–1246 [CrossRef]
    [Google Scholar]
  80. Heikkilä T, Seppälä I, Saxen H, Panelius J, Yrjanainen H et al. Species-Specific serodiagnosis of Lyme arthritis and neuroborreliosis due to Borrelia burgdorferi sensu stricto, B. afzelii, and B. garinii by using decorin binding protein A. J Clin Microbiol 2002; 40:453–460 [CrossRef]
    [Google Scholar]
  81. Tufts DM, Hart TM, Chen GF, Kolokotronis S-O, Diuk-Wasser MA et al. Outer surface protein polymorphisms linked to host-spirochete association in Lyme borreliae. Mol Microbiol 2019; 111:868–882 [CrossRef][PubMed]
    [Google Scholar]
  82. Caine JA, Lin Y-P, Kessler JR, Sato H, Leong JM et al. Borrelia burgdorferi outer surface protein C (OspC) binds complement component C4b and confers bloodstream survival. Cell Microbiol 2017; 19:e12786 [CrossRef]
    [Google Scholar]
  83. Vancová M, Rudenko N, Vaněček J, Golovchenko M, Strnad M et al. Pleomorphism and viability of the Lyme disease pathogen Borrelia burgdorferi exposed to physiological stress conditions: a correlative Cryo-Fluorescence and Cryo-Scanning electron microscopy study. Front Microbiol 2017; 8:596 [CrossRef]
    [Google Scholar]
  84. Hammerschmidt C, Koenigs A, Siegel C, Hallström T, Skerka C et al. Versatile roles of CspA orthologs in complement inactivation of serum-resistant Lyme disease spirochetes. Infect Immun 2014; 82:380–392 [CrossRef]
    [Google Scholar]
  85. Rudenko N, Golovchenko M, Grubhoffer L, Oliver JH et al. Updates on Borrelia burgdorferi sensu lato complex with respect to public health. Ticks Tick Borne Dis 2011; 2:123–128 [CrossRef]
    [Google Scholar]
  86. Margos G, Vollmer SA, Cornet M, Garnier M, Fingerle V et al. A new Borrelia species defined by multilocus sequence analysis of housekeeping genes. Appl Environ Microbiol 2009; 75:5410–5416 [CrossRef]
    [Google Scholar]
  87. Margos G, Wilske B, Sing A, Hizo-Teufel C, Cao W-C et al. Borrelia bavariensis sp. nov. is widely distributed in Europe and Asia. Int J Syst Evol Microbiol 2013; 63:4284–4288 [CrossRef]
    [Google Scholar]
  88. Kraiczy P, Stevenson B. Complement regulator-acquiring surface proteins of Borrelia burgdorferi: structure, function and regulation of gene expression. Ticks Tick Borne Dis 2013; 4:26–34 [CrossRef]
    [Google Scholar]
  89. Rosa PA, Tilly K, Stewart PE. The burgeoning molecular genetics of the Lyme disease spirochaete. Nat Rev Microbiol 2005; 3:129–143 [CrossRef][PubMed]
    [Google Scholar]
  90. Chan K, Awan M, Barthold SW, Parveen N. Comparative molecular analyses of Borrelia burgdorferi sensu stricto strains B31 and N40D10/E9 and determination of their pathogenicity. BMC Microbiol 2012; 12:157 [CrossRef][PubMed]
    [Google Scholar]
  91. Smetanick MT, Zellis SL, Ermolovich T. Acrodermatitis chronica atrophicans: a case report and review of the literature. Cutis 2010; 85:247–252[PubMed]
    [Google Scholar]
  92. Casjens SR, Mongodin EF, Qiu W-G, Dunn JJ, Luft BJ et al. Whole-Genome sequences of two Borrelia afzelii and two Borrelia garinii Lyme disease agent isolates. J Bacteriol 2011; 193:6995–6996 [CrossRef]
    [Google Scholar]
  93. Schüler W, Bunikis I, Weber-Lehman J, Comstedt P, Kutschan-Bunikis S et al. Complete genome sequence of Borrelia afzelii K78 and comparative genome analysis. PLoS One 2015; 10:e0120548 [CrossRef]
    [Google Scholar]
  94. Schutzer SE, Fraser-Liggett CM, Casjens SR, Qiu W-G, Dunn JJ et al. Whole-genome sequences of thirteen isolates of Borrelia burgdorferi . J Bacteriol 2011; 193:1018–1020 [CrossRef]
    [Google Scholar]
  95. Margos G, Gofton A, Wibberg D, Dangel A, Marosevic D et al. The genus Borrelia reloaded. PLoS One 2018; 13:e0208432 [CrossRef]
    [Google Scholar]
  96. Casjens SR, Fraser-Liggett CM, Mongodin EF, Qiu W-G, Dunn JJ et al. Whole genome sequence of an unusual Borrelia burgdorferi sensu lato isolate. J Bacteriol 2011; 193:1489–1490 [CrossRef]
    [Google Scholar]
  97. Schutzer SE, Fraser-Liggett CM, Qiu W-G, Kraiczy P, Mongodin EF et al. Whole-Genome sequences of Borrelia bissettii, Borrelia valaisiana, and Borrelia spielmanii . J Bacteriol 2012; 194:545–546 [CrossRef]
    [Google Scholar]
  98. Margos G, Becker NS, Fingerle V, Sing A, Ramos JA et al. Core genome phylogenetic analysis of the avian associated Borrelia turdi indicates a close relationship to Borrelia garinii . Mol Phylogenet Evol 2019; 131:93–98 [CrossRef]
    [Google Scholar]
  99. Cotté V, Sabatier L, Schnell G, Carmi-Leroy A, Rousselle J-C et al. Differential expression of Ixodes ricinus salivary gland proteins in the presence of the Borrelia burgdorferi sensu lato complex. J Proteomics 2014; 96:29–43 [CrossRef]
    [Google Scholar]
  100. Sertour N, Cotté V, Garnier M et al. Infection kinetics and tropism of Borrelia burgdorferi sensu lato in mouse after natural (via ticks) or artificial (needle) infection depends on the bacterial strain. Front Microbiol 1722; 2018:9
    [Google Scholar]
  101. Tonetti N, Voordouw MJ, Durand J, Monnier S, Gern L et al. Genetic variation in transmission success of the Lyme borreliosis pathogen Borrelia afzelii. Ticks Tick Borne Dis 2015; 6:334–343 [CrossRef]
    [Google Scholar]
  102. Lagal V, Postic D, Ruzic-Sabljic E, Baranton G et al. Genetic diversity among Borrelia strains determined by single-strand conformation polymorphism analysis of the ospC gene and its association with invasiveness. J Clin Microbiol 2003; 41:5059–5065 [CrossRef]
    [Google Scholar]
  103. Heylen DJA, Sprong H, Krawczyk A, Van Houtte N, Genné D et al. Inefficient co-feeding transmission of Borrelia afzelii in two common European songbirds. Sci Rep 2017; 7:39596 [CrossRef]
    [Google Scholar]
  104. Cuellar J, Pietikäinen A, Glader O, Liljenbäck H, Söderström M et al. Borrelia burgdorferi infection in biglycan knockout mice. J Infect Dis 2019; 220:116–126 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000899
Loading
/content/journal/micro/10.1099/mic.0.000899
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error