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

Frontiers in Microbiology

Volumn 4, Issue JUL, 2013, Pages

  Gupta, Radhey S ^a   Mahmood, Sharmeen ^a   Adeolu, Mobolaji ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Borreliaceae; Brachyspiriales; Conserved signature indels; Leptospiriales; Molecular signatures; Spirochaetaceae; Spirochaetes; Spirochaetes phylogeny and taxonomy

Indexed keywords

BACTERIAL PROTEIN; FLGC PROTEIN; MOLECULAR MARKER; RNA 16S; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENOME; BORRELIA; BRACHYSPIRACEAE; BRACHYSPIRIALES; BREVINEMATALES; CLADISTICS; COMPARATIVE STUDY; CRISTISPIRA; GENE SEQUENCE; GENETIC VARIABILITY; LEPTOSPIRA; LEPTOSPIRIALES; MOLECULAR BIOLOGY; MOLECULAR SIGNATURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENOMICS; PHYLOGENY; SPHAEROCHAETA; SPIROCHAETA; SPIROCHETE; TREPONEMA;

BORRELIA; BRACHYSPIRACEAE; CRISTISPIRA; LEPTOSPIRACEAE; SPIROCHAETA; SPIROCHAETACEAE; SPIROCHAETALES; SPIROCHAETES; TREPONEMA;

EID: 84885352440     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2013.00217     Document Type: Article

References (81)

1. Abt, B., Göker, M., Scheuner, C., Han, C., Lu, M., Misra, M., et al. (2013). Genome sequence of the thermophilic fresh-water bacterium Spirochaeta caldaria type strain (H1 T), reclassification of Spirochaeta caldaria and Spirochaeta stenostrepta in the genus Treponema as Treponema caldaria comb. nov., Treponema stenostrepta comb. nov., and Treponema zuelzerae comb. nov., and emendation of the genus Treponema. Stand. Genomic Sci. 8. doi: 10.4056/sigs.3096473.
2. Abt, B., Han, C., Scheuner, C., Lu, M., Lapidus, A., Nolan, M., et al. (2012). Complete genome sequence of the termite hindgut bacterium Spirochaeta coccoides type strain (SPN1T), reclassification in the genus Sphaerochaeta as Sphaerochaeta coccoides comb. nov. and emendations of the family Spirochaetaceae and the genus Sphaerochaeta. Stand. Genomic Sci. 6, 194. doi: 10.4056/sigs.2796069
3. Adeolu, M., and Gupta, R. S. (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 104, 1-24. doi: 10.1007/s10482-013-9920-6
4. Adler, B., and de la Peña Moctezuma, A. (2010). Leptospira and leptospirosis. Vet. Microbiol. 140, 287-296. doi: 10.1016/j.vetmic.2009.03.012
5. Akiva, E., Itzhaki, Z., and Margalit, H. (2008). Built-in loops allow versatility in domain? Domain interactions: lessons from self-interacting domains. Proc. Natl. Acad. Sci. U.S.A. 105, 13292. doi: 10.1073/pnas.0801207105
6. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., et al. (1997). Gapped, BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402. doi: 10.1093/nar/25.17.3389
7. Anthony, N. E., Blackwell, J., Ahrens, W., Lovell, R., and Scobey, M. W. (2013). Intestinal spirochetosis: an Enigmatic disease. Dig. Dis. Sci. 58, 202-208. doi: 10.1007/s10620-012-2305-2
8. Baldauf, S. L., and Palmer, J. D. (1993). Animals and fungi are each other's closest relatives: congruent evidence from multiple proteins. Proc. Natl. Acad. Sci. U.S.A. 90, 11558-11562. doi: 10.1073/pnas.90.24.11558
9. Bellgard, M. I., Wanchanthuek, P., La, T., Ryan, K., Moolhuijzen, P., Albertyn, Z., et al. (2009). Genome sequence of the pathogenic intestinal spirochete Brachyspira hyodysenteriae reveals adaptations to its lifestyle in the porcine large intestine. PloS ONE 4:e4641. doi: 10.1371/journal.pone.0004641
10. Bermudes, D., Chase, D., and Margulis, L. (1988). Morphology as a basis for taxonomy of large Spirochetes symbiotic in wood-eating cockroaches and termites: Pillotina gen. nov., nom. rev.; Pillotina calotermitidis sp. nov., nom. rev.; Diplocalyx gen. nov., nom. rev.; Diplocalyx calotermitidis sp. nov., nom. rev.; Hollandina gen. nov., nom. rev.; Hollandina pterotermitidis sp. nov., nom. rev.; and Clevelandina reticulitermitidis gen. nov., sp. nov. Int. J. Syst. Bacteriol. 38, 291-302. doi: 10.1099/00207713-38-3-291
11. Bhandari, V., Ahmod, N. Z., Shah, H. N., and Gupta, R. S. (2013). Molecular signatures for the 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. doi: 10.1099/ijs.0.048488-0
12. Buchanan, R. E. (1917). Studies in the nomenclature and classification of bacteria. II. The primary subdivisions of the Schizomycetes. J. Bacteriol. 2, 155-164.
13. Bulach, D. M., Zuerner, R. L., Wilson, P., Seemann, T., McGrath, A., Cullen, P. A., et al. (2006). Genome reduction in Leptospira borgpetersenii reflects limited transmission potential. Proc. Natl. Acad. Sci. U.S.A. 103, 14560-14565. doi: 10.1073/pnas.0603979103
14. Casjens, S. R., Fraser-Liggett, C. M., Mongodin, E. F., Qiu, W. G., Dunn, J. J., Luft, B. J., et al. (2011). Whole genome sequence of an unusual Borrelia burgdorferi sensu lato isolate. J. Bacteriol. 193, 1489-1490. doi: 10.1128/JB.01521-10
15. Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540-552. doi: 10.1093/oxfordjournals.molbev.a026334
16. Cavalier-Smith, T. (2002). The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. Int. J. Syst. Evol. Microbiol. 52, 7-76.
17. Chaconas, G. (2005). Hairpin telomeres and genome plasticity in Borrelia: all mixed up in the end. Mol. Microbiol. 58, 625-635. doi: 10.1111/j.1365-2958.2005.04872.x
18. Chaconas, G., and Kobryn, K. (2010). Structure, function, and evolution of linear replicons in Borrelia. Annu. Rev. Microbiol. 64, 185-202. doi: 10.1146/annurev.micro.112408.134037
19. Chou, L. F., Chen, Y. T., Lu, C. W., Ko, Y. C., Tang, C. Y., Pan, M. J., et al. (2012). Sequence of Leptospira santarosai serovar Shermani genome and prediction of virulence-associated genes. Gene. 511, 364-370. doi: 10.1016/j.gene.2012.09.074
20. Ciccarelli, F. D., Doerks, T., Von Mering, C., Creevey, C. J., Snel, B., and Bork, P. (2006). Toward automatic reconstruction of a highly resolved tree of life. Science 311, 1283-1287. doi: 10.1126/science.1123061
21. Cutler, S. J. (2010). Relapsing fever: a forgotten disease revealed. J. Appl. Microbiol. 108, 1115-1122. doi: 10.1111/j.1365-2672.2009.04598.x
22. Dai, Q., Restrepo, B. I., Porcella, S. F., Raffel, S. J., Schwan, T. G., and Barbour, A. G. (2006). Antigenic variation by Borrelia hermsii occurs through recombination between extragenic repetitive elements on linear plasmids. Mol. Microbiol. 60, 1329-1343. doi: 10.1111/j.1365-2958.2006.05177.x
23. Dworkin, M. S., Schwan, T. G., Anderson, D. E. Jr., and Borchardt, S. M. (2008). Tick-borne relapsing fever. Infect. Dis. Clin. North Am. 22, 449. doi: 10.1016/j.idc.2008.03.006
24. Ehrenberg, C. G. (1835). "Dritter Beitrag zur Erkenntniss grosser Organisation in der Richtung des kleinsten Raumes," in Abhandlungen der Preussischen Akademie der Wissenschaften (Berlin) aus den Jahre 1833-1835, 143-336.
25. Elbir, H., Gimenez, G, Robert, C., Bergström, S., Cutler, S., Raoult, D., et al. (2012). Complete genome sequence of Borrelia crocidurae. J. Bacteriol. 194, 3723-3724. doi: 10.1128/JB.00118-12
26. Ellen, R. P., and Galimanas, V. B. (2005). Spirochetes at the forefront of periodontal infections. periodontology 2000 38, 13-32. doi: 10.1111/j.1600-0757.2005.00108.x
27. Euzéby, J. P. (2013). List of Prokaryotic names with Standing in Nomenclature. Available online at: www.bacterio.net
28. Fraser, C. M., Casjens, S., Huang, W. M., Sutton, G. G., Clayton, R., Lathigra, R., et al. (1997). Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390, 580-586. doi: 10.1038/37551
29. Gao, B., and Gupta, R. S. (2012a). Microbial systematics in the post-genomics era. Antonie Van Leeuwenhoek 101, 45-54. doi: 10.1007/s10482-011-9663-1
30. Gao, B., and Gupta, R. S. (2012b). Phylogenetic framework and molecular signatures for the main clades of the phylum Actinobacteria. Microbiol. Mol. Biol. Rev. 76, 66-112. doi: 10.1128/MMBR.05011-11
31. Gerbase, A. C., Rowley, J. T., Heymann, D. H. L., Berkley, S. F. B., and Piot, P. (1998). Global prevalence and incidence estimates of selected curable STDs. Sex. Transm. Infect. 74, S12.
32. Glöckner, G., Lehmann, R., Romualdi, A., Pradella, S., Schulte-Spechtel, U., Schilhabel, M., et al. (2004). Comparative analysis of the Borrelia garinii genome. Nucleic Acids Res. 32, 6038-6046. doi: 10.1093/nar/gkh953
33. Gogarten, J. P., Doolittle, W. F., and Lawrence, J. G. (2002). Prokaryotic evolution in light of gene transfer. Mol. Biol. Evol. 19, 2226-2238. doi: 10.1093/oxfordjournals.molbev.a004046
34. Goodner, B., Hinkle, G., Gattung, S., Miller, N., Blanchard, M., Qurollo, B., et al. (2001). Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294, 2323-2328. doi: 10.1126/science.1066803
35. Griffiths, E., and Gupta, R. S. (2004). Signature sequences in diverse proteins provide evidence for the late divergence of the order Aquificales. Int. Microbiol. 7, 41-52.
36. Gupta, R. S. (1998). Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol. Mol. Biol. Rev. 62, 1435.
37. Gupta, R. S. (2009). Protein signatures (molecular synapomorphies) that are distinctive characteristics of the major cyanobacterial clades. Int. J. Syst. Evol. Microbiol. 59, 2510.
38. Gupta, R. S. (2010). Molecular signatures for the main phyla of photosynthetic bacteria and their subgroups. Photosyn. Res. 104, 357-372. doi: 10.1007/s11120-010-9553-9
39. Gupta, R. S., Chander, P., and George, S. (2012). Phylogenetic framework and molecular signatures for the class Chloroflexi and its different clades; proposal for division of the class Chloroflexi class. nov. 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, 99-119. doi: 10.1007/s10482-012-9790-3
40. Gupta, R. S., Chen, W. J., Adeolu, M., and Chai, Y. (2013). Molecular signatures for the class Coriobacteriia and its different clades; Proposal for division of the class Coriobacteriia into the emended order Coriobacteriales, containing the emended family Coriobacteriaceae and Atopobiaceae fam. nov., and Eggerthellales ord. nov., containing the family Eggerthellaceae fam. nov. Int. J. Syst. Evol. Microbiol. doi: 10.1099/ijs.0.048371-0.
41. Gupta, R. S., and Griffiths, E. (2002). Critical issues in bacterial phylogeny. Theor. Popul. Biol. 61, 423-434. doi: 10.1006/tpbi.2002.1589
42. Håfström, T., Jansson, D. S., and Segerman, B. (2011). Complete genome sequence of Brachyspira intermedia reveals unique genomic features in Brachyspira species and phage-mediated horizontal gene transfer. BMC Genomics 12:395. doi: 10.1186/1471-2164-12-395
43. Han, C., Gronow, S., Teshima, H., Lapidus, A., Nolan, M., Lucas, S., et al. (2011). Complete genome sequence of Treponema succinifaciens type strain (6091T). Stand. Genomic Sci. 4, 361. doi: 10.4056/sigs.1984594
44. Harris, J. K., Kelley, S. T., Spiegelman, G. B., and Pace, N. R. (2003). The genetic core of the universal ancestor. Genome Res. 13, 407-412. doi: 10.1101/gr.652803
45. Harwood, C. S., and Canale-Parola, E. (1984). Ecology of spirochetes. Annu. Rev. Microbiol. 38, 161-192. doi: 10.1146/annurev.mi.38.100184.001113
46. Homma, M., DeRosier, D. J., and Macnab, R. M. (1990). Flagellar hook and hook-associated proteins of Salmonella typhimurium and their relationship to other axial components of the flagellum. J. Mol. Biol. 213, 819-832. doi: 10.1016/S0022-2836(05)80266-9
47. Hovind-Hougen, K., Birch-Andersen, A., Hendrik-Nielsen, R., Orholm, M., Pedersen, J. O., Teglbaerg, P. S., et al. (1982). Intestinal spirochetosis: morphological characterization and cultivation of the spirochete Brachyspira aalborgi gen. nov., sp. nov. J. Clin. Microbiol. 6, 1127-1136.
48. Jeanmougin, F., Thompson, J. D., Gouy, M., Higgins, D. G., and Gibson, T. J. (1998). Multiple sequence alignment with Clustal, X. Trends Biochem. Sci. 23, 403. doi: 10.1016/S0968-0004(98)01285-7
49. Jones, D. T., Taylor, W. R., and Thornton, J. M. (1992). The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8, 275-282.
50. Kobryn, K. (2007). "The linear hairpin replicons of Borrelia burgdorferi," in Microbial Linear Plasmids, eds F. Meinhardt, and R. Klassen (Heidelberg: Springer), 117-140.
51. Lescot, M., Audic, S., Robert, C., Nguyen, T. T., Blanc, G., Cutler, S. J., et al. (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:e1000185. doi: 10.1371/journal.pgen.1000185
52. Li, C., Wolgemuth, C. W., Marko, M., Morgan, D. G., and Charon, N. W. (2008). Genetic analysis of spirochete flagellin proteins and their involvement in motility, filament assembly, and flagellar morphology. J. Bacteriol. 190, 5607-5615. doi: 10.1128/JB.00319-08
53. Lin, C., den Bakker, H. C., Suzuki, H., Lefébure, T., Ponnala, L., Sun, Q., et al. (2013). Complete genome sequence of the porcine strain Brachyspira pilosicoli P43/6/78T. Genome Announc. 1. doi: 10.1128/genomeA.00215-12.
54. Ludwig, W., and Klenk, H. P. (2001). "Overview: a phylogenetic backbone and taxonomic framework for prokaryotic systematics," in Bergey's Manual of Systematic Bacteriology, ed G. M. Garrity (New York, NY: Springer), 49-65.
55. Macnab, R. M. (2003). How bacteria assemble flagella. Annu. Rev. Microbiol. 57, 77-100. doi: 10.1146/annurev.micro.57.030502.090832
56. Mavromatis, K., Yasawong, M., Chertkov, O., Lapidus, A., Lucas, S., Nolan, M., et al. (2010). Complete genome sequence of Spirochaeta smaragdinae type strain (SEBR 4228T). Stand. Genomic Sci. 3, 136. doi: 10.4056/sigs.1143106
57. Nau, R., Christen, H. J., and Eiffert, H. (2009). Lyme disease: ?current state of knowledge. Dtsch. Arztebl. Int. 106, 72. doi: 10.3238/arztebl.2009.0072
58. NCBI. (2013). NCBI Genome Database. Available online at: http://www.ncbi.nlm.nih.gov/genome/
59. Noguchi, H. (1917). Spirochaeta icterohaemorrhagiae in American wild rats and its relation to the Japanese and European strains. J. Exp. Med. 25, 755-763.
60. Olsen, I., Paster, B. J., and Dewhirst, F. E. (2000). Taxonomy of spirochetes. Anaerobe 6, 39-57. doi: 10.1006/anae.1999.0319
61. Paster, B. J. (2011a). "Phylum XV. Spirochaetes Garrity and Holt (2001)," in Bergey's Manual of Systematic Bacteriology, eds D. J. Brenner, N. R. Krieg, G. M. Garrity, and J. T. Staley (New York, NY: Springer), 471.
62. Paster, B. J. (2011b). "Family I. Spirochaetaceae Swellengrebel 1907, 581AL," in Bergey's Manual of Systematic Bacteriology, eds D. J. Brenner, N. R. Krieg, G. M. Garrity, and J. T. Staley (New York, NY: Springer), 473-531.
63. Paster, B. J., and Dewhirst, F. E. (2000). Phylogenetic foundation of spirochetes. J. Mol. Microbiol. Biotechnol. 2, 341-344.
64. Paster, B. J., Dewhirst, F. E., Weisburg, W. G., Tordoff, L. A., Fraser, G. J., Hespell, R. B., et al. (1991). Phylogenetic analysis of the spirochetes. J. Bacteriol. 173, 6101-6109.
65. Pati, A., Sikorski, J., Gronow, S., Munk, C., Lapidus, A., Copeland, A., et al. (2010). Complete genome sequence of Brachyspira murdochii type strain (56-150T). Stand. Genomic Sci. 2, 260.
66. Picardeau, M., Bulach, D. M., Bouchier, C., Zuerner, R. L., Zidane, N., Wilson, P. J., 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. doi: 10.1371/journal.pone.0001607
67. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., et al. (2013). The, SILVA ribosomal, RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590-D596. doi: 10.1093/nar/gks1219
68. Ren, S. X., Fu, G., Jiang, X. G., Zeng, R., Miao, Y. G., Xu, H., et al. (2003). Unique physiological and pathogenic features of Leptospira interrogans revealed by whole-genome sequencing. Nature 422, 888-893. doi: 10.1038/nature01597
69. Rokas, A., and Holland, P. W. H. (2000). Rare genomic changes as a tool for phylogenetics. Trends Ecol. Evol. 15, 454-459. doi: 10.1016/S0169-5347(00)01967-4
70. Rokas, A., Williams, B. L., King, N., and Carroll, S. B. (2003). Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425, 798-804. doi: 10.1038/nature02053
71. Schutzer, S. E., Fraser-Liggett, C. M., Qiu, W. G., Kraiczy, P., Mongodin, E. F., Dunn, J. J., et al. (2012). Whole-genome sequences of Borrelia bissettii, Borrelia valaisiana, and Borrelia spielmanii. J. Bacteriol. 194, 545-546. doi: 10.1128/JB.06263-11
72. Seshadri, R., Myers, G. S. A., Tettelin, H., Eisen, J. A., Heidelberg, J. F., Dodson, R. J., 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. doi: 10.1073/pnas.0307639101
73. Singh, B., and Gupta, R. S. (2009). Conserved inserts in the Hsp60 (GroEL) and Hsp70 (DnaK) proteins are essential for cellular growth. Mol. Genet. Genomics 281, 361-373. doi: 10.1007/s00438-008-0417-3
74. Smajs, D., Norris, S. J., and Weinstock, G. M. (2012). Genetic diversity in Treponema pallidum: implications for pathogenesis, evolution and molecular diagnostics of syphilis and yaws. Infect. Genet. Evol. 12, 191-202. doi: 10.1016/j.meegid.2011.12.001
75. Smajs, D., Zobaníková, M., Strouhal, M., Cjková, D., Dugan-Rocha, S., Pospísilová, P., et al. (2011). Complete genome sequence of Treponema paraluiscuniculi, strain Cuniculi A: the loss of infectivity to humans is associated with genome decay. PLoS ONE 6:e20415. doi: 10.1371/journal.pone.0020415
76. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739. doi: 10.1093/molbev/msr121
77. Tavaré, S. (1986). "Some probabilistic and statistical problems in the analysis of, DNA sequences," in Lectures on Mathematics in the Life Sciences, ed R. M. Miura (Providence, RI: American Mathematical Society), 57-86.
78. Visser, M. B., and Ellen, R. P. (2011). New insights into the emerging role of oral spirochaetes in periodontal disease. Clin. Microbiol. Infect. 17, 502-512. doi: 10.1111/j.1469-0691.2011.03460.x
79. Whelan, S., and Goldman, N. (2001). A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18, 691-699. doi: 10.1093/oxfordjournals.molbev.a003851
80. Wu, D., Hugenholtz, P., Mavromatis, K., Pukall, R., Dalin, E., Ivanova, N. N., et al. (2009). A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462, 1056-1060. doi: 10.1038/nature08656
81. Zhong, J., and Barbour, A. G. (2004). Cross species hybridization of a Borrelia burgdorferi DNA array reveals infection and culture associated genes of the unsequenced genome of the relapsing fever agent Borrelia hermsii. Mol. Microbiol. 51, 729-748. doi: 10.1046/j.1365-2958.2003.03849.x