Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis

Science

Volumn 282, Issue 5389, 1998, Pages 754-759

  Stephens, Richard S ^a,b   Kalman, Sue ^c   Lammel, Claudia ^a,b   Fan, Jun ^c   Marathe, Rekha ^c   Aravind, L ^d   Mitchell, Wayne ^a,b   Olinger, Lynn ^b   Tatusov, Roman L ^d   Zhao, Qixun ^b   Koonin, Eugene V ^d   Davis, Ronald W ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STANFORD UNIVERSITY   (United States)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; VIRULENCE FACTOR;

ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; CHLAMYDIA TRACHOMATIS; CHROMATIN CONDENSATION; GENE SEQUENCE; GENOME; HUMAN; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL;

AEROBIOSIS; AMINO ACID SEQUENCE; AMINO ACIDS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CHLAMYDIA TRACHOMATIS; DNA REPAIR; ENERGY METABOLISM; ENZYMES; EVOLUTION; GENOME, BACTERIAL; HUMANS; LIPIDS; MOLECULAR SEQUENCE DATA; PEPTIDOGLYCAN; PHYLOGENY; PROTEIN BIOSYNTHESIS; RECOMBINATION, GENETIC; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION, GENETIC; TRANSFORMATION, BACTERIAL; VIRULENCE;

BACTERIA (MICROORGANISMS); CHLAMYDIA TRACHOMATIS; CHLAMYDIAE; EUKARYOTA; MAMMALIA; PROKARYOTA;

EID: 0032561496     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.282.5389.754     Document Type: Article

References (60)

1. Morb. Mortal. Wkly Rep. 46, 193 (1997).
2. M. Laga, N. Nzila, J. Goeman, AIDS (suppl. 1) 5, S55 (1991).
3. N. R. Pace, Science 276, 734 (1997); W. C. Weisburg, T. P. Hatch, C. R. Woese, J. Bacteriol. 167, 570 (1986). Chlamydia are classified in the order Chlamydiales, with one family (Chlamydiaceae) that contains a single genus [J. W. Moulder et al., Chlamydia, Bergey's Manual of Systematic Bacteriology, N. R. Krieg, Ed. (Williams & Wilkins, Baltimore, MD, 1984), vol. 1, p. 729].
4. N. R. Pace, Science 276, 734 (1997); W. C. Weisburg, T. P. Hatch, C. R. Woese, J. Bacteriol. 167, 570 (1986). Chlamydia are classified in the order Chlamydiales, with one family (Chlamydiaceae) that contains a single genus [J. W. Moulder et al., Chlamydia, Bergey's Manual of Systematic Bacteriology, N. R. Krieg, Ed. (Williams & Wilkins, Baltimore, MD, 1984), vol. 1, p. 729].
5. N. R. Pace, Science 276, 734 (1997); W. C. Weisburg, T. P. Hatch, C. R. Woese, J. Bacteriol. 167, 570 (1986). Chlamydia are classified in the order Chlamydiales, with one family (Chlamydiaceae) that contains a single genus [J. W. Moulder et al., Chlamydia, Bergey's Manual of Systematic Bacteriology, N. R. Krieg, Ed. (Williams & Wilkins, Baltimore, MD, 1984), vol. 1, p. 729].
6. R. S. Stephens, Infect. Agents Dis. 1, 279 (1992).
7. Genome sequencing and annotation methodologies are available at the Science Web site (www. sciencemag.org/feature/data/982604.shl)
8. R. L. Tatusov, E. V. Koonin, D. J. Lipman, Science 278, 631 (1997); E. V. Koonin et al., Mol. Microbiol. 25, 619 (1997); S. E. Brenner et al., Nature 378, 140 (1995).
9. R. L. Tatusov, E. V. Koonin, D. J. Lipman, Science 278, 631 (1997); E. V. Koonin et al., Mol. Microbiol. 25, 619 (1997); S. E. Brenner et al., Nature 378, 140 (1995).
10. R. L. Tatusov, E. V. Koonin, D. J. Lipman, Science 278, 631 (1997); E. V. Koonin et al., Mol. Microbiol. 25, 619 (1997); S. E. Brenner et al., Nature 378, 140 (1995).
11. E. A. Wagar et al. J. Bacteriol. 177, 5179 (1995).
12. M. Ibba, A. W. Curnow, D. Soll, Trends Biochem. Sci. 22, 39 (1997).
13. A. W. Curnow et al., Proc. Natl. Acad. Sci. U.S.A. 94, 11819 (1997).
14. M. Hayashi, Y. Nakayama, T. Unemoto, FEBS Lett. 381, 174 (1996).
15. J. W. Moulder, Microbiol. Rev. 55, 143 (1991); T. P. Hatch, E. Al-Hossainy, J. A. Silverman, J. Bacteriol. 150, 662 (1982).
16. J. W. Moulder, Microbiol. Rev. 55, 143 (1991); T. P. Hatch, E. Al-Hossainy, J. A. Silverman, J. Bacteriol. 150, 662 (1982).
17. C. M. Fraser et al., Science 281, 375 (1998); C. M. Fraser et al., ibid. 270, 397 (1995); K. Yokoyama et al., J. Biol. Chem. 269, 12248 (1994); K. Takase et al., ibid., p. 11037.
18. C. M. Fraser et al., Science 281, 375 (1998); C. M. Fraser et al., ibid. 270, 397 (1995); K. Yokoyama et al., J. Biol. Chem. 269, 12248 (1994); K. Takase et al., ibid., p. 11037.
19. C. M. Fraser et al., Science 281, 375 (1998); C. M. Fraser et al., ibid. 270, 397 (1995); K. Yokoyama et al., J. Biol. Chem. 269, 12248 (1994); K. Takase et al., ibid., p. 11037.
20. C. M. Fraser et al., Science 281, 375 (1998); C. M. Fraser et al., ibid. 270, 397 (1995); K. Yokoyama et al., J. Biol. Chem. 269, 12248 (1994); K. Takase et al., ibid., p. 11037.
21. W. L. Beatty et al., Infect. Immun. 62, 3705 (1994).
22. J. L. Wylie, G. M. Hatch, G. McClarty, J. Bacteriol. 179, 7233 (1997).
23. R. A. Heinzen and T. Hackstadt, Infect. Immun. 65, 1088 (1997).
24. T. E. Letain and K. Postle, Mol. Microbiol. 24, 271 (1997).
25. A. Dufour and W. C. Haldenwang, J. Bacteriol. 176, 1813 (1994); U. Voelker, A. Dufour, W. G. Haldenwang, ibid. 177, 114 (1995).
26. A. Dufour and W. C. Haldenwang, J. Bacteriol. 176, 1813 (1994); U. Voelker, A. Dufour, W. G. Haldenwang, ibid. 177, 114 (1995).
27. B. S. Powell et al., J. Biol. Chem. 270, 4822 (1995).
28. A. Fox et al., Infect. Immun. 58, 835 (1990); H. Su, Y. X. Zhang, R. Li, Kexue Tongbao 30, 695 (1985).
29. A. Fox et al., Infect. Immun. 58, 835 (1990); H. Su, Y. X. Zhang, R. Li, Kexue Tongbao 30, 695 (1985).
30. J. W. Moulder, Microbiol. Rev. 55, 143 (1991).
31. W. J. Newhall and R. B. Jones, J. Bacteriol. 154, 998 (1983); T. P. Hatch, M. Miceli, J. E. Sublett, ibid. 165, 379 (1986).
32. W. J. Newhall and R. B. Jones, J. Bacteriol. 154, 998 (1983); T. P. Hatch, M. Miceli, J. E. Sublett, ibid. 165, 379 (1986).
33. D. Longbottom et al., FEMS Microbiol. Lett. 142, 277 (1996).
34. A. Webster and G. Kemp, J. Gen. Virol. 74, 1415 (1993).
35. C. J. Hueck, Microbiol. Mol. Biol. Rev. 62, 379 (1998).
36. R. C. Hsia, et al., Mol. Microbiol. 25, 351 (1997).
37. D. D. Rockey et al., ibid. 24, 217 (1997).
38. C. P. Ponting and I. D. Kerr, Protein Sci. 5, 914 (1996); E. V. Koonin, Trends Biochem. Sci. 21, 242 (1996).
39. C. P. Ponting and I. D. Kerr, Protein Sci. 5, 914 (1996); E. V. Koonin, Trends Biochem. Sci. 21, 242 (1996).
40. G. M. Hatch and G. McClarty, Infect. Immun. 66, 3727 (1998); T. Hackstadt, M. A. Scidmore, D. D. Rockey, Proc. Natl. Acad. Sci. U.S.A. 92, 4877 (1995).
41. G. M. Hatch and G. McClarty, Infect. Immun. 66, 3727 (1998); T. Hackstadt, M. A. Scidmore, D. D. Rockey, Proc. Natl. Acad. Sci. U.S.A. 92, 4877 (1995).
42. G. Tipples and G. McClarty, Mol. Microbiol. 8, 1105 (1993); J. Biol. Chem. 270, 7908 (1995); T. P. Hatch, J. Bacteriol. 125, 706 (1976).
43. G. Tipples and G. McClarty, Mol. Microbiol. 8, 1105 (1993); J. Biol. Chem. 270, 7908 (1995); T. P. Hatch, J. Bacteriol. 125, 706 (1976).
44. G. Tipples and G. McClarty, Mol. Microbiol. 8, 1105 (1993); J. Biol. Chem. 270, 7908 (1995); T. P. Hatch, J. Bacteriol. 125, 706 (1976).
45. R. L. Tatusov, E. V. Koonin, D. J. Lipman, Science 278, 631 (1997).
46. E. A. Wagar, S. Safarians, M. Pang, FEMS Microbiol. Lett. 77, 161 (1992).
47. Phylogenetic trees were constructed from multiple alignments of protein sequences using the neighbor-joining method and the Fitch-Margoliash method as implemented in the KITSCH program, with 1000 bootstrap replications [J. Felsenstein, Methods Enzymol. 266, 418 (1996)].
48. Taxonomic distribution of database hits was evaluated using the TAX_COLLECTOR program from the SEALS package [D. R. Walker and E. V. Koonin, Ismb 5, 333 (1997)]. The analysis detected 35 chlamydial proteins, for which the similarity to eukaryotic homologs was significantly greater than that to bacterial homologs (e-values differed by at least a factor of 100). For more than 20 of these, the eukaryotic or archaeal origin was unequivocally supported by phylogenetic tree analysis. In comparable analyses of the genomes of other pathogenic bacteria such as spirochetes or Helicobacter pylori, only three or four genes were linked to eukaryotic origins (L. Aravind, unpublished observation).
49. Taxonomic distribution of database hits was evaluated using the TAX_COLLECTOR program from the SEALS package [D. R. Walker and E. V. Koonin, Ismb 5, 333 (1997)]. The analysis detected 35 chlamydial proteins, for which the similarity to eukaryotic homologs was significantly greater than that to bacterial homologs (e-values differed by at least a factor of 100). For more than 20 of these, the eukaryotic or archaeal origin was unequivocally supported by phylogenetic tree analysis. In comparable analyses of the genomes of other pathogenic bacteria such as spirochetes or Helicobacter pylori, only three or four genes were linked to eukaryotic origins (L. Aravind, unpublished observation).
50. The chlamydial nucleoid structure differs significantly between the RB and EB developmental stages, wherein it is highly condensed in the EB stage [J. W. Costerton, L. Poffenroth, J. C. Wilt, N. Kordova, Can. J. Bacteriol. 22, 16 (1976)].
51. Nucleoid condensation is associated with EB stage-specific proteins, so-called histone-like proteins [E. A. Wagar and R. S. Stephens, Infect. Immun. 56, 1678 (1988);
52. T. Hackstadt, W. Baehr, Y. Ying, Proc. Natl. Acad. Sci. U.S.A. 88, 3937 (1991) ], that modulate superhelical density in EBs
53. [M. V. Solbrig, M. L. Wong, R. S. Stephens, Mol. Microbiol. 4, 1535 (1990)]
54. and when expressed in E. coli [C. E. d. Barry, S. F. Hayes, T. Hackstadt, Science 256, 377 (1992)].
55. R. Amann et al., Appl. Environ. Microbiol. 63, 115 (1997).
56. M. L Sogin, H. J. Elwood, J. H. Gunderson, Proc. Natl. Acad. Sci. U.S.A. 83, 1383 (1986).
57. J. W. Moulder, in Microbiology of Chlamydiae, A. L. Barren, Ed. (CRC Press, Boca Raton, FL, 1988), pp. 3-19.
58. Single-letter abbreviations for the amino acid residues are as follows: A, Ala; C, Cys; D, Asp; E, Glu; F, Phe; G, Gly; H, His; I, Ile; K, Lys; L, Leu; M, Met; N, Asn; P, Pro; Q, Gln; R, Arg; S, Ser; T, Thr; V, Val; W, Trp; and Y, Tyr. X indicates any residue.
59. E. V. Koonin, L. Aravind, R. L. Tatusov, data not shown.
60. We thank K. Koshiyama, D. R. Walker, E. Chung, C. Komp, S. Mirthipati, and especially, T. Brettin and F. Dietrich for their contributions to this project. S. Kalman led the DNA sequencing phase of this project. Supported by National Institute of Allergy and Infectious Diseases grant AI 39258.