1887

Abstract

Abstract

The essential GroEL proteins represent a subset of molecular chaperones ubiquitously distributed among species of the eubacterial lineage, as well as in eukaryote organelles. We employed these highly conserved proteins to infer eubacterial phylogenies. GroEL from the species analyzed clustered in distinct groups in evolutionary trees drawn by either the distance or the parsimony method, which were in general agreement with those found by 16S rRNA comparisons (i.e., proteobacteria, chlamydiae, bacteroids, spirochetes, firmicutes [gram-positive bacteria], and cyanobacteria-chloroplasts). Moreover, the analysis indicated specific relationships between some of the aforementioned groups which appeared not to be clearly defined or controversial in rRNA-based phylogenetic studies. For instance, a monophyletic origin for the low-G+C and high-G+C subgroups among the firmicutes, as well as their specific relationship to the cyanobacteria-chloroplasts, was inferred. The general observations suggest that GroEL proteins provide valuable evolutionary tools for defining evolutionary relationships among the eubacterial lineage of life.

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1994-01-01
2024-04-19
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References

  1. Ahn T. I., Leeu H. K., Kwak I. H., Jeon K. W. 1991; Nucleotide sequence and temperature-dependent expression of XgroEL gene isolated from symbiotic bacteria of Amoeba proteus. Endocyt. Cell Res. 8:33–44
    [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E., Lipman D. J. 1990; Basic local alignment research tool. J. Mol. Biol. 215:403–410
    [Google Scholar]
  3. Ballard S. A., Segers R. P. A. M., Bleumink-Pluym N., Fyfe J., Faine S., Adler B. 1993; Molecular analysis of the hsp (groE) operon of Leptospira interrogans serovar copenhageni. Mol. Microbiol. 8:739–751
    [Google Scholar]
  4. Brenner D. J., O’Connor S. P., Winkler H. H., Steigerwalt A. G. 1993; Proposals to unify the genera Bartonella and Rochalimaea, with descriptions of Bartonella quintana comb, nov., Bartonella vinsonii comb, nov., Bartonella henselae comb, nov., and Bartonella elizabethae comb, nov., and to remove the family Bartonellaceae from the order Rickettsiales. Int. J. Syst. Bacteriol. 43:777–786
    [Google Scholar]
  5. Cavalier-Smith T. 1992; The number of symbiotic origins of organelles. BioSystems 28:91–106
    [Google Scholar]
  6. Dasch G., Swinson K. 1992; The phylogeny of Rickettsia tsutsugamushi as deduced from the sequence of its 16S ribosomal RNA gene, abstr. R-6. 289 Abstr. 92nd Gen. Meet. Am. Soc. Microbiol. 1992 American Society for Microbiology; Washington, D.C.:
    [Google Scholar]
  7. Dasch G. A., Ching W. M., Kim P. Y., Pham H., Stover C. K., Oaks E. V., Dobson M. E., Weiss E. 1990; A structural and immunological comparison of rickettsial HSP60 antigens with those of other species. Ann. N.Y. Acad. Sci. 590:352–369
    [Google Scholar]
  8. Dayhoff M. O., Schwartz R. M., Orcutt B. C. 1978; A model of evolutionary change in proteins. 345–452 Dayhoff M. O. Atlas of protein sequence and structure 5suppl. 3 National Biomedical Research Foundation; Washington, D.C.:
    [Google Scholar]
  9. Felsenstein J. 1988; Phylogenies from molecular sequences: inference and reliability. Annu. Rev. Genet. 22:521–565
    [Google Scholar]
  10. Ferreyra R. G., Soncini F. C., Viale A. M. 1993; Cloning, characterization, and functional expression in Escherichia coli of chaperonin (groESL) genes from the photosynthetic sulfur bacterium Chromatium vinosum. J. Bacteriol. 175:1514–1523
    [Google Scholar]
  11. Fischer H. M., Babst M., Kaspar T., Acuna G., Arigoni F., Hennecke H. 1993; One member of a groESL-like chaperonin multigene family in Bradyrhizobium japonicum is co-regulated with symbiotic nitrogen fixation genes. EMBO J. 12:2901–2912
    [Google Scholar]
  12. Gaydos C. A., Palmer L., Quinn T. C., Falkow S., Eiden J. J. 1993; Phylogenetic relationship of Chlamydia pneumoniae to Chlamydia psittaci and Chlamydia trachomatis as determined by analysis of 16S ribosomal DNA sequences. Int. J. Syst. Bacteriol. 43:610–612
    [Google Scholar]
  13. Georgopoulos C., Welch W. J. 1993; Role of the major heat shock proteins as molecular chaperones. Annu. Rev. Cell Biol. 9:601–634
    [Google Scholar]
  14. Gor D., Mayfield J. E. 1992; Cloning and nucleotide sequence of the Brucella abortus groE operon. Biochim. Biophys. Acta 130:120–122
    [Google Scholar]
  15. Hasegawa M., Hashimoto T. 1993; Ribosomal RNA trees misleading?. Nature (London) 361:23
    [Google Scholar]
  16. Hemmingsen S. M., Woolford C., van der Vies S. M., Tilly K., Dennis D. T., Georgopoulos C. P., Hendrix R. W., Ellis R J. 1988; Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature (London) 333:330–334
    [Google Scholar]
  17. Hindersson P., Knudsen J. D., Axelsen N. H. 1987; Cloning and expression of Treponema pallidum common antigen (Tp-4) in Escherichia coli K-12. J. Gen. Microbiol. 133:587–596
    [Google Scholar]
  18. Hoffman P. S., Houston L., Butler C. A. 1990; Legionella pneumophila htpAB heat shock operon: nucleotide sequence and expression of the 60-kilodalton antigen in L. pneumophila-infected HeLa cells. Infect. Immun. 58:3380–3387
    [Google Scholar]
  19. Hughes A. L. 1993; Contrasting evolutionary rates in the duplicate chaperonin genes of Mycobacterium tuberculosis and M. leprae. Mol. Biol. Evol. 10:1343–1359
    [Google Scholar]
  20. Jukes T. H., Bhushan V. 1986; Silent nucleotide substitutions and G+C content of some mitochondrial and bacterial genes. J. Mol. Evol. 24:39–44
    [Google Scholar]
  21. Kikuta L. C., Puolakkainen M., Kuo C. C., Campbell L. A. 1991; Isolation and sequence analysis of the Chlamydia pneumoniae GroE operon. Infect. Immun. 59:4665–4669
    [Google Scholar]
  22. Lehel C., Los D., Wada H., Györgyei J., Horváth I., Kovács E., Murata N., Vigh L. 1993; A second groEL-like gene, organized in a groESL operon is present in the genome of Synechocystis sp. PCC 6803. J. Biol. Chem. 268:1799–1804
    [Google Scholar]
  23. Macchia G., Massone A., Burroni D., Covacci A., Censini S., Rappuoli R. 1993; The Hsp60 protein of Helicobacter pylori. Structure and immune response in patients with gastroduodenal diseases. Mol. Microbiol. 9:645–652
    [Google Scholar]
  24. Maid U., Steinmüller R., Zetsche K. 1992; Structure and expression of a plastid-encoded groEL homologous heat-shock gene in a thermophilic unicellular red alga. Curr. Genet. 21:521–525
    [Google Scholar]
  25. Mazodier P., Guglielmi G., Davies J., Thompson C. J. 1991; Characterization of the groEL-like genes in Streptomyces albus. J. Bacteriol. 173:7382–7386
    [Google Scholar]
  26. Mehra V., Sweetser D., Young R. A. 1986; Efficient mapping of protein antigenic determinants. Proc. Natl. Acad. Sci. USA 83:7013–7017
    [Google Scholar]
  27. Murray R. G. E. 1984; The higher taxa, or, a place for everything…?. 31–34 Krieg N. R., Holt J. G. Bergey’s manual of systematic bacteriology 1 The Williams & Wilkins Co.; Baltimore:
    [Google Scholar]
  28. Neefs J. M., Van de Peer Y., De Rijk P., Chapelle S., De Wachter R. 1993; Compilation of small ribosomal subunit RNA structures. Nucleic Acids Res. 21:3025–3049
    [Google Scholar]
  29. Ohta T., Honda K., Kuroda M., Saito K., Hayashi H. 1993; Molecular characterization of the gene operon of heat shock proteins HSP60 and HSP10 in methicillin-resistant Staphylococcus aureus. Biochem. Biophys. Res. Commun. 193:730–737
    [Google Scholar]
  30. Olsen G. J., Woese C. R. 1993; Ribosomal RNA: a key to phylogeny. FASEB J. 7:113–123
    [Google Scholar]
  31. Olsen G. J., Woese C. R., Overbeek R. 1994; The winds of evolutionary change: breathing new life into microbiology. J. Bacteriol. 176:1–6
    [Google Scholar]
  32. Parsons L. M., Waring A. L., Shayegani M. 1992; Molecular analysis of the Haemophilus ducreyi groE heat shock operon. Infect. Immun. 60:4111–4118
    [Google Scholar]
  33. Paster B. J., Dewhirst F. E., Olsen I., Fraser G. J. 1994; Phylogeny of Bacteroides, Prevotella, and Porphyromonas spp. and related bacteria. J. Bacteriol. 176:725–732
    [Google Scholar]
  34. Rinke de Wit T. F., Bekelie S., Osland A., Miko T. L., Hermans P. W. M., van Soolingen D., Drijfhout J. W., Schöningh R., Janson A. A. M., Thole J. E. R. 1992; Mycobacteria contain two groEL genes: the second Mycobacterium leprae groEL gene is arranged in an operon with groES. Mol. Microbiol. 6:1995–2007
    [Google Scholar]
  35. Rusanganwa E., Gupta R. S. 1993; Cloning and characterization of multiple groEL chaperonin-encoding genes in Rhizobium meliloti. Gene 126:67–75
    [Google Scholar]
  36. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenic trees. Mol. Biol. Evol. 4:406–425
    [Google Scholar]
  37. Sawada H., Ieki H., Oyaizu H., Matsumoto S. 1993; Proposal for rejection of Agrobacterium tumefaciens and revised descriptions for the genus Agrobacterium and for Agrobacterium radiobacter and Agrobacterium rhizogenes. Int. J. Syst. Bacteriol. 43:694–702
    [Google Scholar]
  38. Schoen U., Schumann W. 1993; Molecular cloning, sequencing, and transcriptional analysis of the groESL operon from Bacillus stearothermophilus. J. Bacteriol. 175:2465–2469
    [Google Scholar]
  39. Segal G., Ron E. Z. 1993; Heat shock transcription of the groESL operon of Agrobacterium tumefaciens may involve a hairpin-loop structure. J. Bacteriol. 175:3083–3088
    [Google Scholar]
  40. Shanafelt M. C., Hindersson P., Soderberg C., Mensi N., Turk C. W., Webb D., Yssel H., Peltz G. 1991; T cell and antibody reactivity with the Borrelia burgdorferi 60-kDa heat shock protein in Lyme arthritis. J. Immunol. 146:3985–3992
    [Google Scholar]
  41. Shinnick T. M. 1987; The 65-kilodalton antigen of Mycobacterium tuberculosis. J. Bacteriol. 169:1080–1088
    [Google Scholar]
  42. Sipos A., Klocke M., Frosch M. 1991; Cloning and sequencing of the genes coding for the 10- and 60-kDa heat shock proteins from Pseudomonas aeruginosa and mapping of a species-specific epitope. Infect. Immun. 59:3219–3226
    [Google Scholar]
  43. Sneath P. H. A. 1989; Analysis and interpretation of sequence data for bacterial systematics: the view of a numerical taxonomist. Syst. Appl. Microbiol. 12:15–31
    [Google Scholar]
  44. Steel M. A., Lockhardt P. J., Penny D. 1993; Confidence in evolutionary trees from biological sequence data. Nature (London) 364:440–442
    [Google Scholar]
  45. Stover C. K., Marana D. P., Dasch G. A., Oaks E. V. 1990; Molecular cloning and sequence analysis of the Sta58 major antigen gene of Rickettsia tsutsugamushi: sequence homology and antigenic comparison of Sta58 to the 60-kilodalton family of stress proteins. Infect. Immun. 58:1360–1368
    [Google Scholar]
  46. Sumner J. W., Sims K. G., Jones D. C., Anderson B. E. 1993; Ehrlichia chaffeensis expresses an immunoreactive protein homologous to the Escherichia coli GroEL protein. Infect. Immun. 61:3536–3539
    [Google Scholar]
  47. Taguchi H., Konishi J., Ishii N., Yoshida M. 1991; A chaperonin from a thermophilic bacterium, Thermus thermophilus, that controls refoldings of several thermophilic enzymes. J. Biol. Chem. 266:22411–22418
    [Google Scholar]
  48. Unterman B. M., Baumann P., McLean D. L. 1989; Pea aphid symbiont relationships established by analysis of 16S rRNAs. J. Bacteriol. 171:2970–2974
    [Google Scholar]
  49. Viale A. M., Arakaki A. K. Unpublished observations
    [Google Scholar]
  50. Viale A. M., Arakaki A. K. 1994; The chaperone connection to the origins of the eukaryotic organelles. FEBS Lett. 341:146–151
    [Google Scholar]
  51. Weisburg W. G., Dobson M. E., Samuel J. E., Dasch G. A., Mallavia L. P., Baca O., Mandelco L., Sechrest J. E., Weiss E., Woese C. R. 1989; Phylogenetic diversity of the rickettsiae. J. Bacteriol. 171:4202–4206
    [Google Scholar]
  52. Willems A., Collins M. D. 1993; Phylogenetic analysis of rhizobia and agrobacteria based on 16S rRNA gene sequences. Int. J. Syst. Bacteriol. 43:305–313
    [Google Scholar]
  53. Woese C. R. 1987; Bacterial evolution. Microbiol. Rev. 51:221–271
    [Google Scholar]
  54. Wong F. Y. K., Stackebrandt E., Ladha J. K., Fleischman D. E., Date R. A., Fuerst J. A. 1994; Phylogenetic analysis of Bradyrhizobium japonicum and photosynthetic stem-nodulating bacteria from Aeschynomene species grown in separated geographical regions. Appl. Environ. Microbiol. 60:940–946
    [Google Scholar]
  55. Zabaleta E., Oropeza A., Jimenez B., Salerno G., Crespi M., Herrera-Estrella L. 1992; Isolation and characterization of genes encoding chaperonin 60b from Arabidopsis thaliana. Gene 111:175–181
    [Google Scholar]
  56. Zavarzin G. A., Stackebrandt E., Murray R. G. E. 1991; A correlation of phylogenetic diversity in the Proteobacteria with the influence of ecological forces. Can. J. Microbiol. 37:1–6
    [Google Scholar]
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