The genome of Borrelia recurrentis, the agent of deadly louse-borne relapsing fever, is a degraded subset of tick-borne Borrelia duttonii

PLoS Genetics

Volumn 4, Issue 9, 2008, Pages

  Lescot, Magali ^a   Audic, Stéphane ^a   Robert, Catherine ^b   Nguyen, Thi Tien ^b   Blanc, Guillaume ^a   Cutler, Sally J ^c   Wincker, Patrick ^d   Couloux, Arnaud ^d   Claverie, Jean Michel ^a   Raoult, Didier ^b   Drancourt, Michel ^b  

^a CNRS Aix Marseille University   (France)

^b CNRS   (France)

^c UNIVERSITY OF EAST LONDON   (United Kingdom)

^d CENTRE NATIONAL DE SÉQUENÇAGE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPROTEIN; POLYTHYMIDYLIC ACID; RESOLVASE; VIRULENCE FACTOR; BACTERIAL PROTEIN;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BASE PAIRING; BORRELIA; BORRELIA DUTTONII; BORRELIA INFECTION; BORRELIA RECURRENTIS; EVOLUTION; GENE LOSS; GENE SEQUENCE; GENOME SIZE; MUTS GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PROMOTER REGION; RECA GENE; SEQUENCE ANALYSIS; TELOMERE; UNINDEXED SEQUENCE; ANIMAL; ANTIGENIC VARIATION; CLASSIFICATION; COMPARATIVE STUDY; GENETICS; IMMUNOLOGY; LOUSE; LYME DISEASE; MICROBIOLOGY; PATHOGENICITY; TICK;

BORRELIA; BORRELIA DUTTONII; BORRELIA RECURRENTIS; IXODIDA; PEDICULUS HUMANUS; PHTHIRAPTERA; RICKETTSIA PROWAZEKII;

ANIMALS; ANTIGENIC VARIATION; BACTERIAL PROTEINS; BORRELIA; BORRELIA INFECTIONS; GENOME, BACTERIAL; LICE; LYME DISEASE; RELAPSING FEVER; TICKS;

EID: 52949138281     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000185     Document Type: Article

References (89)

1. Fraser CM, Casjens S, Huang WM, Sutton GG, Clayton R, et al. (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390: 580-586.
2. Casjens S, Palmer N, van Vugt R, Huang WM, Stevenson B, et al. (2000) A bacterial genome in flux: the twelve linear and nine circular extrachromosomal DNAs in an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol 35: 490-516.
3. Glockner G, Lehmann R, Romualdi A, Pradella S, Schulte-Spechtel U, et al. (2004) Comparative analysis of the Borrelia garinii genome. Nucleic Acids Res 32: 6038-6046.
4. Glockner G, Schulte-Spechtel U, Schilhabel M, Felder M, Suhnel J, et al. (2006) Comparative genome analysis: selection pressure on the Borrelia vls cassettes is essential for infectivity. BMC Genomics 7: 211.
5. Scott J, Wright D, Cutler S (2005) Typing African relapsing fever spirochetes. Emerg Infect Dis 11: 1722-1729.
6. Ras NM, Lascola B, Postic D, Cutler SJ, Rodhain F, et al. (1996) Phylogenesis of relapsing fever Borrelia spp. Int J Syst Bacteriol 46: 859-865.
7. Vial L, Diatta G, Tall A, Ba el H, Bouganali H, et al. (2006) Incidence of tickborne relapsing fever in west Africa: longitudinal study. Lancet 368: 37-43.
8. Raoult D, Roux V (1999) The body louse as a vector of reemerging human diseases. Clin Infect Dis 29: 888-911.
9. Southern PM, Sandford JP (1969) Relapsing fever: a clinical and microbiological review. Med 48: 129-143.
10. Bryceson AD, Parry EH, Perine PL, Warrell DA, Vukotich D, et al. (1970) Louse-borne relapsing fever. Q J Med 39: 129-170.
11. Andersson SG, Zomorodipour A, Andersson JO, Sicheritz-Ponten T, Alsmark UC, et al. (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396: 133-140.
12. Alsmark CM, Frank AC, Karlberg EO, Legault BA, Ardell DH, et al. (2004) The louse-borne human pathogen Bartonella quintana is a genomic derivative of the zoonotic agent Bartonella henselae. Proc Natl Acad Sci U S A 101: 9716-9721.
13. Ogata H, Audic S, Renesto-Audiffren P, Fournier PE, Barbe V, et al. (2001) Mechanisms of evolution in Rickettsia conorii and R. prowazekii. Science 293: 2093-2098.
14. Barbour AG (1993) Linear DNA of Borrelia species and antigenic variation. Trends Microbiol 1: 236-239.
15. Barbour AG, Putteet-Driver AD, Bunikis J (2005) Horizontally acquired genes for purine salvage in Borrelia spp. causing relapsing fever. Infect Immun 73: 6165-6168.
16. Pettersson J, Schrumpf ME, Raffel SJ, Porcella SF, Guyard C, et al. (2007) Purine salvage pathways among Borrelia species. Infect Immun 75: 3877-3884.
17. Sohaskey CD, Zuckert WR, Barbour AG (1999) The extended promoters for two outer membrane lipoprotein genes of Borrelia spp. uniquely include a T-rich region. Mol Microbiol 33: 41-51.
18. Vidal V, Cutler S, Scragg IG, Wright DJ, Kwiatkowski D (2002) Characterisation of silent and active genes for a variable large protein of Borrelia recurrentis. BMC Infect Dis 2: 25.
19. Chaconas G, Stewart PE, Tilly K, Bono JL, Rosa P (2001) Telomere resolution in the Lyme disease spirochete. Embo J 20: 3229-3237.
20. Kobryn K, Chaconas G (2002) ResT, a telomere resolvase encoded by the Lyme disease spirochete. Mol Cell 9: 195-201.
21. Rocha EP, Cornet E, Michel B (2005) Comparative and evolutionary analysis of the bacterial homologous recombination systems. PLoS Genet 1: e15.
22. Mortier-Barriere I, Velten M, Dupaigne P, Mirouze N, Pietrement O, et al. (2007) A key presynaptic role in transformation for a widespread bacterial protein: DprA conveys incoming ssDNA to RecA. Cell 130: 824-836.
23. Hinnebusch BJ, Barbour AG, Restrepo BI, Schwan TG (1998) Population structure of the relapsing fever spirochete Borrelia hermsii as indicated by polymorphism of two multigene families that encode immunogenic outer surface lipoproteins. Infect Immun 66: 432-440.
24. Dai Q, Restrepo BI, Porcella SF, Raffel SJ, Schwan TG, et al. (2006) Antigenic variation by Borrelia hermsii occurs through recombination between extragenic repetitive elements on linear plasmids. Mol Microbiol 60: 1329-1343.
25. Roberts DM, Carlyon JA, Theisen M, Marconi RT (2000) The bdr gene families of the Lyme disease and relapsing fever spirochetes: potential influence on biology, pathogenesis, and evolution. Emerg Infect Dis 6: 110-122.
26. Seshadri R, Myers GS, Tettelin H, Eisen JA, Heidelberg JF, et al. (2004) Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. Proc Natl Acad Sci U S A 101: 5646-5651.
27. Zhong J, Skouloubris S, Dai Q, Myllykallio H, Barbour AG (2006) Function and evolution of plasmid-borne genes for pyrimidine biosynthesis in Borrelia spp. J Bacteriol 188: 909-918.
28. Setubal JC, Reis M, Matsunaga J, Haake DA (2006) Lipoprotein computational prediction in spirochaetal genomes. Microbiology 152: 113-121.
29. Goodner B, Hinkle G, Gattung S, Miller N, Blanchard M, et al. (2001) Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294: 2323-2328.
30. Wood DW, Setubal JC, Kaul R, Monks DE, Kitajima JP, et al. (2001) The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294: 2317-2323.
31. Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, et al. (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21: 526-531.
32. Heuts DP, van Hellemond EW, Janssen DB, Fraaije MW (2007) Discovery, characterization, and kinetic analysis of an alditol oxidase from Streptomyces coelicolor. J Biol Chem 282: 20283-20291.
33. Fraser CM, Norris SJ, Weinstock GM, White O, Sutton GG, et al. (1998) Complete genome sequence of Treponema pallidum, the syphilis spirochete. Science 281: 375-388.
34. Ren SX, Fu G, Jiang XG, Zeng R, Miao YG, et al. (2003) Unique physiological and pathogenic features of Leptospira interrogans revealed by whole-genome sequencing. Nature 422: 888-893.
35. Bulach DM, Zuerner RL, Wilson P, Seemann T, McGrath A, et al. (2006) Genome reduction in Leptospira borgpetersenii reflects limited transmission potential. Proc Natl Acad Sci U S A 103: 14560-14565.
36. Picardeau M, Bulach DM, Bouchier C, Zuerner RL, Zidane N, et al. (2008) Genome Sequence of the Saprophyte Leptospira biflexa Provides Insights into the Evolution of Leptospira and the Pathogenesis of Leptospirosis. PLoS ONE 3: e1607.
37. Hinnebusch J, Tilly K (1993) Linear plasmids and chromosomes in bacteria. Mol Microbiol 10: 917-922.
38. Casjens S (1999) Evolution of the linear DNA replicons of the Borrelia spirochetes. Curr Opin Microbiol 2: 529-534.
39. Nosek J, Kosa P, Tomaska L (2006) On the origin of telomeres: a glimpse at the pre-telomerase world. Bioessays 28: 182-190.
40. Picardeau M, Lobry JR, Hinnebusch BJ (1999) Physical mapping of an origin of bidirectional replication at the centre of the Borrelia burgdorferi linear chromosome. Mol Microbiol 32: 437-445.
41. Beaurepaire C, Chaconas G (2005) Mapping of essential replication functions of the linear plasmid lp17 of B. burgdorferi by targeted deletion walking. Mol Microbiol 57: 132-142.
42. Byram R, Stewart PE, Rosa P (2004) The essential nature of the ubiquitous 26-kilobase circular replicon of Borrelia burgdorferi. J Bacteriol 186: 3561-3569.
43. Tourand Y, Lee L, Chaconas G (2007) Telomere resolution by Borrelia burgdorferi rest through the collaborative efforts of tethered DNA binding domains. Mol Microbiol 64: 580-590.
44. Jewett MW, Byram R, Bestor A, Tilly K, Lawrence K, et al. (2007) Genetic basis for retention of a critical virulence plasmid of Borrelia burgdorferi. Mol Microbiol 66: 975-990.
45. Bankhead T, Chaconas G (2004) Mixing active-site components: a recipe for the unique enzymatic activity of a telomere resolvase. Proc Natl Acad Sci U S A 101: 13768-13773.
46. Picardeau M, Lobry JR, Hinnebusch BJ (2000) Analyzing DNA strand compositional asymmetry to identify candidate replication origins of Borrelia burgdorferi linear and circular plasmids. Genome Res 10: 1594-1604.
47. Cutler SJ, Scott JC, Wright DJM (2008) Phylogenetic origins of Borrelia recurrentis. Int J Med Microbiol; S1438-4221(07)00197-X.
48. Marais A, Bove JM, Renaudin J (1996) Characterization of the recA gene regions of Spiroplasma citri and Spiroplasma melliferum. J Bacteriol 178: 7003-7009.
49. Gil R, Silva FJ, Zientz E, Delmotte F, Gonzalez-Candelas F, et al. (2003) The genome sequence of Blochmannia floridanus: comparative analysis of reduced genomes. Proc Natl Acad Sci U S A 100: 9388-9393.
50. Klasson L, Andersson SG (2006) Strong asymmetric mutation bias in endosymbiont genomes coincide with loss of genes for replication restart pathways. Mol Biol Evol 23: 1031-1039.
51. Bradshaw JS, Kuzminov A (2003) RdgB acts to avoid chromosome fragmentation in Escherichia coli. Mol Microbiol 48: 1711-1725.
52. Kouzminova EA, Kuzminov A (2004) Chromosomal fragmentation in dUTPase-deficient mutants of Escherichia coli and its recombinational repair. Mol Microbiol 51: 1279-1295.
53. Shuman S, Glickman MS (2007) Bacterial DNA repair by non-homologous end joining. Nat Rev Microbiol 5: 852-861.
54. Blanc G, Ogata H, Robert C, Audic S, Suhre K, et al. (2007) Reductive Genome Evolution from the Mother of Rickettsia. PLoS Genet 3: e14.
55. Ochman H, Elwyn S, Moran NA (1999) Calibrating bacterial evolution. Proc Natl Acad Sci U S A 96: 12638-12643.
56. Reed DL, Light JE, Allen JM, Kirchman JJ (2007) Pair of lice lost or parasites regained: the evolutionary history of anthropoid primate lice. BMC Biol 5: 7.
57. Ahmed N, Dobrindt U, Hacker J, Hasnain SE (2008) Genomic fluidity and pathogenic bacteria: applications in diagnostics, epidemiology and intervention. Nat Rev Microbiol 6: 387-394.
58. Pallen MJ, Wren BW (2007) Bacterial pathogenomics. Nature 449: 835-842.
59. Vidal V, Scragg IG, Cutler SJ, Rockett KA, Fekade D, et al. (1998) Variable major lipoprotein is a principal TNF-inducing factor of louse-borne relapsing fever. Nat Med 4: 1416-1420.
60. Pennington PM, Cadavid D, Barbour AG (1999) Characterization of VspB of Borrelia turicatae, a major outer membrane protein expressed in blood and tissues of mice. Infect Immun 67: 4637-4645.
61. Cadavid D, Pachner AR, Estanislao L, Patalapati R, Barbour AG (2001) Isogenic serotypes of Borrelia turicatae show different localization in the brain and skin of mice. Infect Immun 69: 3389-3397.
62. Plasterk RH, Simon MI, Barbour AG (1985) Transposition of structural genes to an expression sequence on a linear plasmid causes antigenic variation in the bacterium Borrelia hermsii. Nature 318: 257-263.
63. Kitten T, Barbour AG (1990) Juxtaposition of expressed variable antigen genes with a conserved telomere in the bacterium Borrelia hermsii. Proc Natl Acad Sci U S A 87: 6077-6081.
64. Barbour AG, Burman N, Carter CJ, Kitten T, Bergstrom S (1991) Variable antigen genes of the relapsing fever agent Borrelia hermsii are activated by promoter addition. Mol Microbiol 5: 489-493.
65. Barbour AG, Dai Q, Restrepo BI, Stoenner HG, Frank SA (2006) Pathogen escape from host immunity by a genome program for antigenic variation. Proc Natl Acad Sci U S A 103: 18290-18295.
66. Schwan TG, Battisti JM, Porcella SF, Raffel SJ, Schrumpf ME, et al. (2003) Glycerol-3-phosphate acquisition in spirochetes: distribution and biological activity of glycerophosphodiester phosphodiesterase (GlpQ) among Borrelia species. J Bacteriol 185: 1346-56.
67. Cutler SJ, Fekade D, Hussein K, Knox KA, Melka A, et al. (1994) Successful invitro cultivation of Borrelia recurrentis. Lancet 343: 242.
68. Schwan TG, Schrumpf ME, Hinnebusch BJ, Anderson DE, Konkel ME (1996) GlpQ: an antigen for serological discrimination between relapsing fever and Lyme borreliosis. J Clin Microbiol 34: 2483-92.
69. Cutler SJ (2001) Molecular biology of the relapsing fever borrelia. In: Sussman R, ed. Molecular medical microbiology. Oxford: Academic Press. pp 2093-2113.
70. Parent MA, Goenka R, Murphy E, Levier K, Carreiro N, et al. (2007) Brucella abortus bacA mutant induces greater pro-inflammatory cytokines than the wild-type parent strain. Microbes Infect 9: 55-62.
71. Wang XG, Kidder JM, Scagliotti JP, Klempner MS, Noring R, et al. (2004) Analysis of differences in the functional properties of the substrate binding proteins of the Borrelia burgdorferi oligopeptide permease (Opp) operon. J Bacteriol 186: 51-60.
72. Frees D, Savijoki K, Varmanen P, Ingmer H (2007) Clp ATPases and ClpP proteolytic complexes regulate vital biological processes in low GC, Gram-positive bacteria. Mol Microbiol 63: 1285-1295.
73. Audic S, Robert C, Campagna B, Parinello H, Claverie JM, et al. (2007) Genome analysis of Minibacterium massiliensis highlights the convergent evolution of water-living bacteria. PLoS Genet 3: e138.
74. Cutler SJ, Akintunde CO, Moss J, Fukunaga M, Kurtenbach K, et al. (1999) Successful in vitro cultivation of Borrelia duttonii and its comparison with Borrelia recurrentis. Int J Syst Bacteriol 49: 1793-1799.
75. Ogata H, Renesto P, Audic S, Robert C, Blanc G, et al. (2005) The genome sequence of Rickettsia felis identifies the first putative conjugative plasmid in an obligate intracellular parasite. PLoS Biol 3: e248.
76. Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8: 186-194.
77. Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8: 175-185.
78. Gordon D, Desmarais C, Green P (2001) Automated finishing with autofinish. Genome Res 11: 614-625.
79. Audic S, Claverie JM (1998) Self-identification of protein-coding regions in microbial genomes. Proc Natl Acad Sci U S A 95: 10026-10031.
80. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
81. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32: D277-280.
82. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, et al. (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4: 41.
83. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955-964.
84. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, et al. (2004) Versatile and open software for comparing large genomes. Genome Biol 5: R12.
85. Enright AJ, Van Dongen S, Ouzounis CA (2002) An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 30: 1575-1584.
86. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
87. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540-552.
88. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. CABIOS 13: 555-556.
89. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.