1887

Abstract

Chlamydiae are major human and animal pathogens. Based on alignments of different protein sequences, a number of conserved indels (insertion/deletions) were identified that appear to be unique and distinctive characteristics of the chlamydial species. The identified signatures include one 16 aa and two single aa inserts in the enzyme UDP--acetylglucosamine 1-carboxyvinyltransferase (MurA), a 1 aa insert in protein synthesis elongation factor P (EF-P), a 1 aa insert in the Mg transport protein (MgtE), a 1 aa insert in the carboxy-terminal protease and a 1 aa deletion in the tRNA (guanine- -)-methyltransferase (TrmD) protein. The homologues of these proteins are found in all major groups of bacteria and the observed indels are present in all available chlamydial sequences but not in any other species (except for the large insert in MurA in ). The validity of three of these signatures (MurA, EF-P and MgtE) was tested by PCR amplifying the signature regions from several chlamydial species for which no sequence information was available. All species for which specific fragments could be amplified (, , , ) contained the expected signatures. Additionally, a fragment of the gene from and the gene from , two chlamydia-like species, were also cloned and sequenced. The presence of respective indels in these species provides strong evidence that they are specifically related to the traditional chlamydial species, and that these signatures may be distinctive of the entire order. A 17 aa conserved indel was also identified in the cell wall biosynthesis enzyme UDP--acetylglucosamine pyrophosphorylase (GlmU), which is shared by all archaeal and chlamydial homologues. The gene for this protein is indicated to have been horizontally transferred from an archaeon to a common ancestor of the chlamydiae. The results also support a lateral transfer of the gene between chlamydiae and . The large inserts in these peptidoglycan synthesis related genes in chlamydiae could account for their unusual cell-wall characteristics. These signatures are also potentially useful for screening of the chlamydiae species.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-148-8-2541
2002-08-01
2024-12-01
Loading full text...

Full text loading...

/deliver/fulltext/micro/148/8/1482541a.html?itemId=/content/journal/micro/10.1099/00221287-148-8-2541&mimeType=html&fmt=ahah

References

  1. Brown J. R., Doolittle W. F. 1997; Archaea and the prokaryote-to-eukaryote transition. Microbiol Rev 61:456–502
    [Google Scholar]
  2. Brown E. D., Vivas E. I., Walsh C. T., Kolter R. 1995; MurA (MurZ), the enzyme that catalyzes the first committed step in peptidoglycan biosynthesis, is essential in Escherichia coli . J Bacteriol 177:4194–4197
    [Google Scholar]
  3. Brown K., Pompeo F., Dixon S., Mengin-Lecreulx D., Cambillau C., Bourne Y. 1999; Crystal structure of the bifunctional N -acetylglucosamine 1-phosphate uridyltransferase from Escherichia coli : a paradigm for the related pyrophosphorylase superfamily. EMBO J 18:4096–4107 [CrossRef]
    [Google Scholar]
  4. Bush R. M., Everett K. D. E. 2001; Molecular evolution of the Chlamydiaceae. Int. J Syst Evol Microbiol 51:203–220
    [Google Scholar]
  5. Daian C. M., Wolff A. H., Bielory L. 2000; The role of atypical organisms in asthma. Allergy Asthma Proc 21:107–111 [CrossRef]
    [Google Scholar]
  6. Du W., Brown J. R., Sylvester D. R., Huang J., Chalker A. F., So C. Y., Holmes D. J., Wallis N. G. 2000; Two active forms of UDP- N -acetylglucosamine enolpyruvyltransferase in gram-positive bacteria. J Bacteriol 182:4146–4152 [CrossRef]
    [Google Scholar]
  7. Everett K. D., Bush R. M., Andersen A. A. 1999; Emended description of the order Chlamydiales, proposal of Parachlamydiaceae fam.nov. and Simikaniacae fam. nov.,each containing one monotypic genus, revised taxonomy of the family Chlamydiaceae, including a new genus and five new species, and standards for the identification of organisms. Int J Syst Bacteriol 49:415–440 [CrossRef]
    [Google Scholar]
  8. Felsenstein J. 1994 PHYLIP version 3.5 Seattle, WA: University of Washington;
    [Google Scholar]
  9. Fields P. I., Barnes R. C. others 1992; The genus Chlamydia . In The Prokaryotes pp 3691–3709 Edited by Balows A. New York: Springer;
    [Google Scholar]
  10. Fox A., Rogers J. C., Gilbart J., Morgan S., Davis C. H., Knight S., Wyrick P. B. 1990; Muramic acid is not detectable in Chlamydia psittaci or Chlamydia trachomatis by gas chromatography-mass spectrometry. Infect Immun 58:835–837
    [Google Scholar]
  11. Fukushi H., Hirai K. 1992; Proposal of Chlamydia pecorum sp. nov. for Chlamydia strains derived from ruminants. Int J Syst Bacteriol 42:306–308 [CrossRef]
    [Google Scholar]
  12. Gehring A. M., Lees W. J., Mindiola D. J., Walsh C. T., Brown E. D. 1996; Acetyltransferase precedes uridyl transfer in the formation of UDP- N -acetylglucosamine in separable active sites of the bifunctional GlmU proteins of Escherichia coli . Biochemistry 35:579–585 [CrossRef]
    [Google Scholar]
  13. Ghuysen J.-M., Goffin C. 1999; Lack of cell wall peptidoglycan versus penicillin sensitivity: new insights into the chlamydial anomaly. Antimicrob Agents Chemother 43:2339–2344
    [Google Scholar]
  14. Grayston J. T., Kuo C. C., Campbell A., Wang S. P. 1989; Chlamydia pneumoniae sp. nov. for Chlamydia sp. strain TWAR. Int J Syst Bacteriol 39:88–90 [CrossRef]
    [Google Scholar]
  15. Griffiths E., Gupta R. S. 2001; The use of signature sequences in different proteins to determine the relative branching order of bacterial divisions: evidence that Fibrobacter diverged at a similar time to Chlamydia and the Cytophaga–Flavobacterium–Bacteroides division. Microbiology 147:2611–2622
    [Google Scholar]
  16. Gupta R. S. 1998; Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol Mol Biol Rev 62:1435–1491
    [Google Scholar]
  17. Gupta R. S. 2000a; The natural evolutionary relationships among prokaryotes. CRC Crit Rev Microbiol 26:111–131 [CrossRef]
    [Google Scholar]
  18. Gupta R. S. 2000b; The phylogeny of proteobacteria: relationships to other eubacterial phyla and eukaryotes. FEMS Microbiol Rev 24:367–402 [CrossRef]
    [Google Scholar]
  19. Gupta R. S. 2001; The branching order and phylogenetic placements of species from completed bacterial genomes based on conserved indels found in various proteins. Int Microbiol 4:187–202 [CrossRef]
    [Google Scholar]
  20. Gupta R. S., Johari V. 1998; Signature sequences in diverse proteins provide evidence of a close evolutionary relationship betweeen the Deinococcus/Thermus group and Cyanobacteria. J Mol Evol 46:716–720 [CrossRef]
    [Google Scholar]
  21. Gupta R. S., Singh B. 1994; Phylogenetic analysis of 70 kDa protein sequences suggests a chimeric origin of the eukaryotic cell nucleus. Curr Biol 4:1104–1114 [CrossRef]
    [Google Scholar]
  22. Gupta R. S., Bustard K., Falah M., Singh D. 1997; Sequencing of heat shock protein 70 (DnaK) homologs from Deinococcus proteolyticus and Thermomicrobium roseum and their integration in a protein based phylogeny of prokaryotes. J Bacteriol 179:345–357
    [Google Scholar]
  23. Hatch T. P. 1996; Disulfide cross-linked envelope proteins: the functional equivalent of peptidoglycan in chlamydiae?. J Bacteriol 178:1–5
    [Google Scholar]
  24. Hatch T. P. 1998; Chlamydia: old ideas crushed, new mysteries bared. Science 282:638–639 [CrossRef]
    [Google Scholar]
  25. Herrmann B., Pettersson B., Everett K. D. E., Mikkelsen N. E., Kirsebom L. A. 2000; Characterization of the rnpB gene and RNase P RNA in the order Chlamydiales . Int J Syst Evol Microbiol 50:149–158 [CrossRef]
    [Google Scholar]
  26. Hua S., Youxum Z., Rungte L. 1985; Presence of muramic acid in Chlamydia trachomatis proved by liquid chromatography-mass spectrometry. Kexue Tongbao (Chinese Science Bulletin) 30:695–699
    [Google Scholar]
  27. Kahane S., Everett K. D. E., Kimmel N., Friedman M. G. 1999; Simkania negevensis strain ZT: growth, antigenic and genome characteristics. Int J Syst Bacteriol 49:815–820 [CrossRef]
    [Google Scholar]
  28. Kalman S., Mitchell W., Marathe R. 7 other authors 1999; Comparative genomes of Chlamydia pneumonia and C. trachomatis. Nat Genet 21:385–389 [CrossRef]
    [Google Scholar]
  29. Kandler O., Konig H. 1993; Cell envelopes of archaea: structure and chemistry. In The Biochemistry of Archaea (Archaebacteria) pp 223–259 Edited by Kates M., Kushner D. J., Matheson A. T. New York: Elsevier;
    [Google Scholar]
  30. Kuo C. C., Jackson L. A., Campbell L. A., Grayston J. T. 1995; Chlamydia pneumoniae (TWAR. Clin Microbiol Rev 8:451–461
    [Google Scholar]
  31. Laga M., Nzila N., Goeman J. 1991; The interrelationship of sexually transmitted diseases and HIV infection: implications for the control of both epidemics in Africa. AIDS 5:S55–S63
    [Google Scholar]
  32. Ludwig W., Klenk H.-P. 2001; Overview: a phylogenetic backbone and taxonomic framework for procaryotic systematics. In Bergey’s Manual of Systematic Bacteriology vol. 1The Archaea and the deeply branching and phototrophic Bacteria pp 49–65 Edited by Boone D. R., Castenholz R. W. Berlin: Springer;
    [Google Scholar]
  33. Meijer A., Morre S. A., van den Brule A. J. C., Savelkoul P. H. M., Ossewaarde J. M. 1999; Genomic relatedness of chlamydia isolates determined by amplified fragment length polymorphism analysis. J Bacteriol 181:4469–4475
    [Google Scholar]
  34. Moulder J. W., Hatch T., Kuo C. C., Schachter J., Storz J. 1984; Genus Chlamydia . In Bergey’s Manual of Systematic Bacteriology pp 729–739 Edited by Krieg N. R., Holt J. G. Baltimore, MD: Williams & Wilkins;
    [Google Scholar]
  35. Ossewaarde J. M., Meijer A. 1999; Molecular evidence for the existence of additional members of the order Chlamydiales . Microbiology 145:411–417 [CrossRef]
    [Google Scholar]
  36. Page L. A. 1968; Proposal for the recognition of two species in the genus Chlamydia Jones, Rake and Stearns, 1945. Int J Syst Bacteriol 18:51–66 [CrossRef]
    [Google Scholar]
  37. Pettersson B., Andersson A., Leitner T., Olsvik O., Uhlen M., Storey C., Black C. M. 1997; Evolutionary relationships among members of the genus Chlamydia based on 16S ribosomal DNA analysis. J Bacteriol 179:4195–4205
    [Google Scholar]
  38. Pompeo F., Bourne Y., Heijenoor J. V., Fassy F., Mengin-Lecreulx D. 2001; Dissection of the bifunctional Escherichia coli N -aectylglucosamine-1-phosphate uridyltransferase enzyme into autonomously functional domains and evidence that trimerization is absolutely required for glucosamine-1-phosphate acetyltransferase activity and cell growth. J Biol Chem 276:3883–3889
    [Google Scholar]
  39. Read T. D., Brunham R. C., Shen C. 22 other authors 2000; Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res 28:1397–1406 [CrossRef]
    [Google Scholar]
  40. Rurangirwa F. R., Dilbeck P. M., Crawford T. B., McGuire T. C., McElwain T. F. 1999; Analysis of the 16S rRNA gene of micro-organism WSU 86-1044 from an aborted bovine foetus reveals that it is a member of the order Chlamydiales : proposal of Waddliaceae fam.nov., Waddlia chondrophila gen. nov., sp. nov. Int J Syst Bacteriol 49:577–581 [CrossRef]
    [Google Scholar]
  41. Saikku P. 2000; Chlamydia pneumoniae in atherosclerosis. J Intern Med 247:396
    [Google Scholar]
  42. Schachter J. 1999; Infection and disease epidemiology. In Chlamydia: Intracellular Biology, Pathogenesis, and Immunity pp 139–169 Washington, DC: American Society for Microbiology;
    [Google Scholar]
  43. Schachter J., Stephens R. S., Timms P. 29 other authors 2001; Radical changes to chlamydial taxonomy are not necessary just yet. Int J Syst Evol Microbiol 51:249
    [Google Scholar]
  44. Stephens R. S., Kalman S., Lammel C. 9 other authors 1998; Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis . Science 282:754–759 [CrossRef]
    [Google Scholar]
  45. Sulzenbacher G., Gal L., Peneff C., Fassy F., Bourne Y. 2001; Crystal structure of Streptococcus pneumoniae N -acetylglucosamine-1-phosphate uridyltransferase bound to acetyl-coenzyme A reveals a novel active site architecture. J Biol Chem 276:11844–11851 [CrossRef]
    [Google Scholar]
  46. Woese C. R. 1987; Bacterial evolution. Microbiol Rev 51:221–271
    [Google Scholar]
/content/journal/micro/10.1099/00221287-148-8-2541
Loading
/content/journal/micro/10.1099/00221287-148-8-2541
Loading

Data & Media loading...

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