1887

Abstract

Fourteen conserved indels (i.e. inserts or deletions) have been identified in 10 widely distributed proteins that appear to be characteristic of cyanobacterial species and are not found in any other group of bacteria. These signatures include three inserts of 6, 7 and 28 aa in the DNA helicase II (UvrD) protein, an 18–21 aa insert in DNA polymerase I, a 14 aa insert in the enzyme ADP-glucose pyrophosphorylase, a 3 aa insert in the FtsH protein, an 11–13 aa insert in phytoene synthase, a 5 aa insert in elongation factor-Tu, two deletions of 2 and 7 aa in ribosomal S1 protein, a 2 aa insert in the SecA protein, a 1 aa deletion and a 6 aa insert in the enzyme inosine-5′-monophosphate dehydrogenase and a 1 aa deletion in the major sigma factor. These signatures, which are flanked by conserved regions, provide molecular markers for distinguishing cyanobacterial taxa from all other bacteria and they should prove helpful in the identification of cyanobacterial species, simply on the basis of the presence or absence of these markers in the corresponding proteins. The signatures in six of these proteins (SecA, elongation factor-Tu, ADP-glucose pyrophosphorylase, phytoene synthase, FtsH and ribosomal S1 protein) are also commonly present in plastid homologues from plants and algae (chlorophytes, chromophytes and rhodophytes), indicating their specific relationship to cyanobacteria and supporting their endosymbiotic origin from these bacteria. In phylogenetic trees based on a number of these proteins (SecA, UvrD, DNA polymerase I, elongation factor-Tu) that were investigated, the available cyanobacterial homologues grouped together with high affinity (>95 % bootstrap value), supporting the view that the cyanobacterial phylum is monophyletic and that the identified signatures were introduced in a common ancestor of this group.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.02720-0
2003-11-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/53/6/ijs531833.html?itemId=/content/journal/ijsem/10.1099/ijs.0.02720-0&mimeType=html&fmt=ahah

References

  1. Akiyama Y. 2002; Proton-motive force stimulates the proteolytic activity of FtsH, a membrane-bound ATP-dependent protease in Escherichia coli . Proc Natl Acad Sci U S A 99:8066–8071 [CrossRef]
    [Google Scholar]
  2. Armstrong G. A. 1997; Genetics of eubacterial carotenoid biosynthesis: a colorful tale. Annu Rev Microbiol 51:629–659 [CrossRef]
    [Google Scholar]
  3. Barbrook A. C., Lockhart P. J., Howe C. J. 1998; Phylogenetic analysis of plastid origins based on secA sequences. Curr Genet 34:336–341 [CrossRef]
    [Google Scholar]
  4. Bryant D. A. 1994 The Molecular Biology of Cyanobacteria Dordrecht: Kluwer;
    [Google Scholar]
  5. Castenholz R. W. 2001; Phylum BX. Cyanobacteria. Oxygenic photosynthetic bacteria. In Bergey's Manual of Systematic Bacteriology , 2nd edn. vol 1 pp 474–487Edited by Boone D. R., Castenholz R. W., Garrity G. M. New York: Springer;
    [Google Scholar]
  6. Delwiche C. F., Kuhsel M., Palmer J. D. 1995; Phylogenetic analysis of tufA sequences indicates a cyanobacterial origin of all plastids. Mol Phylogenet Evol 4:110–128 [CrossRef]
    [Google Scholar]
  7. Eisen J. A. 1995; The RecA protein as a model molecule for molecular systematic studies of bacteria: comparison of trees of RecAs and 16S rRNAs from the same species. J Mol Evol 41:1105–1123
    [Google Scholar]
  8. Eisen J. A., Hanawalt P. C. 1999; A phylogenomic study of DNA repair genes, proteins, and processes. Mutat Res 435:171–213 [CrossRef]
    [Google Scholar]
  9. Felsenstein J. 1978; Cases in which parsimony and compatibility methods will be positively misleading. Syst Zool 27:401–410 [CrossRef]
    [Google Scholar]
  10. Felsenstein J. 1994 phylip, version 3.5. Distributed by the author Department of Genetics, University of Washington; Seattle, USA:
    [Google Scholar]
  11. Giovannoni S. J., Turner S., Olsen G. J., Barns S., Lane D. J., Pace N. R. 1988; Evolutionary relationships among cyanobacteria and green chloroplasts. J Bacteriol 170:3584–3592
    [Google Scholar]
  12. Gogarten J. P., Doolittle W. F., Lawrence J. G. 2002; Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19:2226–2238 [CrossRef]
    [Google Scholar]
  13. Gray M. W. 1992; The endosymbiont hypothesis revisited. Int Rev Cytol 141:233–357
    [Google Scholar]
  14. 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]
  15. Griffiths E., Gupta R. S. 2002; Protein signatures distinctive of chlamydial species: horizontal transfer of cell wall biosynthesis genes glmU from archaea to chlamydiae and murA between chlamydiae and Streptomyces . Microbiology 148:2541–2549
    [Google Scholar]
  16. Gruber T. M., Bryant D. A. 1997; Molecular systematic studies of eubacteria, using σ 70-type sigma factors of group 1 and group 2. J Bacteriol 179:1734–1747
    [Google Scholar]
  17. 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]
  18. Gupta R. S. 2000; 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 placement 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. 2002; Phylogeny of bacteria: are we now close to understanding it?. ASM News 68:284–291
    [Google Scholar]
  21. Gupta R. S. 2003; Evolutionary relationships among photosynthetic bacteria. Photosynth Res 76:173–183 [CrossRef]
    [Google Scholar]
  22. Gupta R. S., Griffiths E. 2002; Critical issues in bacterial phylogenies. Theor Popul Biol 61:423–434 [CrossRef]
    [Google Scholar]
  23. Gupta R. S., Johari V. 1998; Signature sequences in diverse proteins provide evidence of a close evolutionary relationship between the Deinococcus Thermus group and cyanobacteria. J Mol Evol 46:716–720 [CrossRef]
    [Google Scholar]
  24. 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]
  25. Honda D., Yokota A., Sugiyama J. 1999; Detection of seven major evolutionary lineages in cyanobacteria based on the 16S rRNA gene sequence analysis with new sequences of five marine Synechococcus strains. J Mol Evol 48:723–739 [CrossRef]
    [Google Scholar]
  26. Isono K., Shimizu M., Yoshimoto K., Niwa Y., Satoh K., Yokota A., Kobayashi H. 1997; Leaf-specifically expressed genes for polypeptides destined for chloroplasts with domains of σ 70 factors of bacterial RNA polymerases in Arabidopsis thaliana . Proc Natl Acad Sci U S A 94:14948–14953 [CrossRef]
    [Google Scholar]
  27. Kimura S., Uchiyama Y., Kasai N. 10 other authors 2002; A novel DNA polymerase homologous to Escherichia coli DNA polymerase I from a higher plant, rice ( Oryza sativa L.). Nucleic Acids Res 30:1585–1592 [CrossRef]
    [Google Scholar]
  28. Kondratieva E. N., Pfennig N., Trüper H. G. 1992; The phototrophic prokaryotes. In The Prokaryotes pp 312–330Edited by Balows A., Trüper H. G., Dworkin M., Harder W., Schleifer K. H. New York: Springer;
    [Google Scholar]
  29. Ludwig W., Klenk H.-P. 2001; Overview: a phylogenetic backbone and taxonomic framework for procaryotic systematics. In Bergey's Manual of Systematic Bacteriology , 2nd edn. vol 1 pp 49–65Edited by Boone D. R., Castenholz R. W., Garrity G. M. Berlin: Springer;
    [Google Scholar]
  30. Margulis L. 1993 Symbiosis in Cell Evolution New York: W. H. Freeman;
    [Google Scholar]
  31. Morden C. W., Delwiche C. F., Kuhsel M., Palmer J. D. 1992; Gene phylogenies and the endosymbiotic origin of plastids. Biosystems 28:75–90 [CrossRef]
    [Google Scholar]
  32. Morse R., O'Hanlon K., Collins M. D. 2002; Phylogenetic, amino acid content and indel analyses of the β subunit of DNA-dependent RNA polymerase of Gram-positive and Gram-negative bacteria. Int J Syst Evol Microbiol 52:1477–1484 [CrossRef]
    [Google Scholar]
  33. Preiss J. 1996; ADPglucose pyrophosphorylase: basic science and applications in biotechnology. Biotechnol Annu Rev 2:259–279
    [Google Scholar]
  34. Raymond J., Zhaxybayeva O., Gogarten J. P., Gerdes S. Y., Blankenship R. E. 2002; Whole-genome analysis of photosynthetic prokaryotes. Science 298:1616–1620 [CrossRef]
    [Google Scholar]
  35. Rippka R., Deruelles J., Waterbury J. B., Herdman M., Stanier R. Y. 1979; Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61 [CrossRef]
    [Google Scholar]
  36. Schmidt M. G., Kiser K. B. 1999; SecA: the ubiquitous component of preprotein translocase in prokaryotes. Microbes Infect 1:993–1004 [CrossRef]
    [Google Scholar]
  37. Stiller J. W., Hall B. D. 1997; The origin of red algae: implications for plastid evolution. Proc Natl Acad Sci U S A 94:4520–4525 [CrossRef]
    [Google Scholar]
  38. Subramanian A. R. 1983; Structure and functions of ribosomal protein S1. Prog Nucleic Acid Res Mol Biol 28:101–142
    [Google Scholar]
  39. Trüper H. G. 1987; Phototrophic bacteria (an incoherent group of prokaryotes). A taxonomic versus phylogenetic survey. Microbiologia 3:71–89
    [Google Scholar]
  40. Turner S., Pryer K. M., Miao V. P., Palmer J. D. 1999; Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46:327–338 [CrossRef]
    [Google Scholar]
  41. Valentin K. 1997; Phylogeny and expression of the secA gene from a chromophytic alga – implications for the evolution of plastids and sec-dependent protein translocation. Curr Genet 32:300–307 [CrossRef]
    [Google Scholar]
  42. Viale A. M., Arakaki A. K., Soncini F. C., Ferreyra R. G. 1994; Evolutionary relationships among eubacterial groups as inferred from GroEL (chaperonin) sequence comparisons. Int J Syst Bacteriol 44:527–533 [CrossRef]
    [Google Scholar]
  43. Whatley J. M. 1993; The endosymbiotic origin of chloroplasts. Int Rev Cytol 144:259–299
    [Google Scholar]
  44. Wilmotte A., Herdman M. 2001; Phylogenetic relationships among the cyanobacteria based on 16S rRNA sequences. In Bergey's Manual of Systematic Bacteriology , 2nd edn. vol 1 pp 487–493Edited by Boone D. R., Castenholz R. W., Garrity G. M. New York: Springer;
    [Google Scholar]
  45. Woese C. R. 1987; Bacterial evolution. Microbiol Rev 51:221–271
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.02720-0
Loading
/content/journal/ijsem/10.1099/ijs.0.02720-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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