Sequencing of heat shock protein 70 (DnaK) homologs from Deinococcus proteolyticus and Thermomicrobium roseum and their integration in a protein- based phylogeny of prokaryotes

Journal of Bacteriology

Volumn 179, Issue 2, 1997, Pages 345-357

  Gupta, Radhey S ^a   Bustard, Kevin ^a   Falah, Mizied ^a   Singh, Davindra ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; DEINOCOCCUS RADIODURANS; GENETIC ANALYSIS; GENETIC CONSERVATION; NONHUMAN; NUCLEIC ACID ANALYSIS; PHYLOGENY; PRIORITY JOURNAL; PROKARYOTE; PROTEIN DOMAIN; SEQUENCE HOMOLOGY;

EID: 0031022823     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.179.2.345-357.1997     Document Type: Article

References (89)

1. Amann, R., W. Ludwig, and K. H. Schleifer. 1988. β-Subunit of ATP synthase: a useful marker for studying the phylogenetic relationship of eubacteria. J. Gen. Microbiol. 134:2815-2821.
2. Anzola, J., B. J. Luft, G. Gorgone, K. J. Dattwyler, C. Soderberg, R. Lahesmaa, and G. Peltz. 1992. Borrelia bugdorferi HSP70 homolog: characterization of an immunoreactive stress protein. Infect. Immun. 60:3704-3713.
3. Balows, A., H. G. Trüper, D. Martin, W. Harder, and K.-H. Schleifer (ed.), 1992. The prokaryotes, 2nd ed., p. 1-4126. Springer-Verlag, New York, N.Y.
4. Bardwell, J., and E. A. Craig. 1984. Major heat shock gene of Drosophila and the Excherichia coli heat inducible dnaK gene are homologous. Proc. Natl. Acad. Sci. USA 81:848-852.
5. Benachenhou-Lahfa, N., P. Forteerre, and B. Labedan. 1993. Evolution of glutamate dehydrogenase genes: evidence for two paralogous protein families and unusual branching pattern of the archaebacteria in the universal tree of life. J. Mol. Evol. 36:335-346.
6. Birkelund, S., A. G. Lundemose, and G. Christiansen. 1990. The 75-kilodalton cytoplasmic Chlamydia trachomatis L2 polypeptide is a DnaK-like protein. Infect. Immun. 58:2098-2104.
7. Bocchetta, M., E. Ceccarelli, R. Creti, A. M. Sanangielantoni, O. Tiboni, and P. Cammarano. 1995. Arrangement and nucleotide sequence of the gene (fus) encoding elongation factor G (EF-G) from the hyperthermophilic bacterium Aquifex pyrophilus: phylogenetic depth of hyperthermophilic bacteria inferred from analysis of the EF-G/fus sequences. J. Mol. Evol. 41:803-812.
8. Boorstein, W. R., T. Ziegelhoffer, and E. A. Craig. 1994. Molecular evolution of the HSP70 multigene family. J. Mol. Evol. 38:1-17.
9. Breed, R. S., E. G. D. Murray, and N. R. Smith. 1957. Bergey's manual of determinative bacteriology, p. 1-1094. The Williams & Wilkins Company, Baltimore, Md.
10. Brooks, B. W., R. G. E. Murray, J. L. Johnson, E. Stackebrandt, C. R. Woese, and G. E. Fox. 1980. Red-pigmented micrococci: a basis for taxonomy. Int. J. Syst. Bacteriol. 30:627-646.
11. Brown, J. R., Y. Masuchi, F. T. Robb, and W. F. Doolittle. 1994. Evolutionary relationships of bacterial and archaeal glutamine synthetase genes. J. Mol. Evol. 38:566-576.
12. Bucca, G., C. P. Smith, M. Alberti, G. Seidita, R. Passantino, and A. M. Pugila. 1993. Cloning and sequencing of the dnaK region of Streptomyces coelicolor A3. Gene 130:141-144.
13. Cavalier-Smith, T. 1987. The origin of eukaryote and archaebacterial cells. Ann. N. Y. Acad. Sci. 503:17-54.
14. Cellier, M. F., J. Teyssier, M. Nicolas, J. P. Liantard, J. Marti, and J. Sriwidada. 1992. Cloning and characterization of the Brucella ovis heat shock protein DnaK functionally expressed in Escherichia coli. J. Bacteriol. 174:8036-8042.
15. Craig, E. A., J. Karmer, J. Shilling, M. Werner-Washburne, S. Holmes, J. Kosic-Smithers, and C. M. Nicolet. 1989. SSC1, an essential member of the yeast HSP70 multigene family, encodes a mitochondrial protein. Mol. Cell. Biol. 9:3000-3008.
16. De Rijk, P., Y. Van de Peer, I. Van den Broeck, and R. deWachter. 1995. Evolution according to large ribosomal subunit RNA. J. Mol. Evol. 41:366-375.
17. Eisen, J. A. 1995. The RecA protein as a model molecule for molecular systematics studies of bacteria: comparison of trees of RecAs and 16S rRNAs from the same species. J. Mol. Evol. 41:1105-1123.
18. Falah, M., and R. S. Gupta. 1994. Cloning of the hsp70 (dnaK) genes from Rhizobium meliloti and Pseudomonas cepacia: phylogenetic analyses of mitochondrial origin based on a highly conserved protein sequence. J. Bacteriol. 176:7748-7753.
19. Felsenstein, J. 1985. Confidence limits in phylogenies: an approach using the bootstrap. Evolution 39:783-791.
20. Felsenstein, J. 1994. PHYLIP, version 3.5. University of Washington, Seat tie.
21. Fleischmann, R. D., M. D. Adams, O. White, R. A. Clayton, E. F. Kirkness, A. R. Kerlavage, C. J. Bult, J.-F. Tomb, B. A. Dougherty, J. M. Merrick, K. McKenney, G. Sutton, W. Fitzhugh, C. A. Fields, J. D. Scott, R. Shirley, L.-I. Liu, A. Glodek, J. M. Kelley, J. F. Weidman, C. A. Phillips, T. Spriggs, E. Hedblom, M. D. Cotton, T. R. Utterback, M. C. Hanna. D. T. Nyuven, D. M. Saudek, R. C. Brandon, L. D. Fine, J. L. Fritehman, J. L. Fuhrmann, N. S. M. Geoghagen, C. L. Gnehm, L. A. McDonald, K. V. Small, C. M. Fraser, H. O. Smith, and J. C. Venter. 1995, Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496-512.
22. Fox, G. E., E. Staekebrandt, R. B. Hepsell, J. Gibson, J. Maniloff, T. A. Dyer, R. S. Wolfe, W. E. Balch, R. S. Tanner, L. J. Magrum, L. B. Zablen, R. Blakemore, R. Gupta, L. Bonen, B. J. Lewis, D. A. Stahl, K. R. Luehrsen, K. N. Chen, and C. R. Woese. 1980. The phylogeny of prokaryotes. Science 209:457-463.
23. Fraser, C. M., J. D. Gocayne, O. White, M. D. Adams, R. A. Clayton, R. D. Fleischmann, C. J. Bult, A. R. Kerlavage, G. Sutton, J. M. Kelley, J. L. Fritchman, J. F. Weldman, K. V. Small, M. Sandusky, J. L. Fuhrmann, D. T. Nguyen, T. R. Utterback, D. M. Saudek, C. A. Phillips, J. M. Merrick, J.-F. Tomb, B. A. Dougherty, K. F. Bott, P.-C. Hu, T. S. Lucier, S. N. Peterson, H. O. Smith, C. A. Hutchison III, and J. C. Venter. 1995. The minimal gene complement of Mycoplasma genitalium. Science 270:397-403.
24. Galley, K. A., B. Singh, and R. S. Gupta. 1992. Cloning of hsp70 gene from Clostridium perfringens using a general polymerase chain reaction based approach. Biochim. Biophys. Acta 1130:203-208.
25. Golding, G. B., and R. S. Gupta. 1995. Protein based phylogenies support a chimeric origin for the eukaryotic genome. Mol. Biol. Evol. 12:1-6.
26. Gomes, S. L., J. W. Gober, and L. Shapiro. 1990. Expression of the Caulobacter heat shock gene dnaK is developmentally controlled during growth at normal temperatures. J. Bacteriol. 172:3051-3059.
27. Gupta, R. S. 1995. Evolution of the chaperonin families (hsp60, hsp10 and tcp-1) of proteins and the origin of eukaryotic cells. Mol. Microbiol. 15:1-11.
28. Gupta, R. S. 1996. Evolutionary relationships of chaperonins, p. 27-64. In R. J. Ellis (ed.), The chaporonins. Academic Press. New York, N.Y.
29. Gupta, R. S. Protein phylogenies and signature sequences: evolutionary relationships within prokaryotes and between prokaryotes and eukuryotes. Antonie Leeuwenhoek, in press.
30. Gupta, R. S., and G. B. Golding. 1993. Evolution of hsp70 gene and its implications regarding relationships between archaebacteria, eubacteria and eukaryotes. J. Mol. Evol. 37:573-582.
31. Gupta, R. S., and G. B. Golding. 1996. The origin of the eukaryotic cell. Trends Biochem. Sci. 21:166-171.
32. Gupta, R. S., and B. Singh. 1992. Cloning of hsp70 gene from Halobacterium marismortui: relatedness of archaebacterial hsp70 to its eubacterial homolog and a model for the evolution of the hsp70 gene. J. Bacteriol. 174:4504-4604.
33. Gupta, R. S., and B. Singh, 1994. Phylogenetic analysis of 70 kD heat shock protein sequences suggests a chimeric origin for the eukaryotic cell nucleus, Curr. Biol, 4:1104-1114.
34. Gupta, R. S., K. Aitken, M. Falah, and B. Singh. 1994. Cloning of Giardia lamblia heat shock protein hsp70 homologs: implications regarding origin of eukaiyotic cells and of endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 91:2895-2899.
35. Hatada, Y. 1994. Cloning and nucleotide sequence of a hsp70 gene from Streptomyces griseus. J. Ferment. Bioeng. 77:461-477.
36. Hearne, C. M., and D. J. Ellar. 1989. Nucleotide sequence of a Bacillus subtilis gene homologous to the dnaK gene of Escherichia coli. Nucleic Acids Res. 17:8373.
37. Hendric, J. P., and F.-U. Hartl. 1993. Molecular chaperone functions of heat shock proteins. Annu. Rev. Biochem. 62:349-384.
38. Hensel, B., W. Demharter, O. Kandler, R. M. Kroppenstedt, and E. Stackebrandt. 1986. Chemotaxonomic and molecular-genetic studies of the genus Thermus: evidence for a phylogenetic relationship of Thermus aquaticus and Thermus ruber to the genus Deinococcus. Int. J. Syst. Bacteriol. 36:444-453.
39. Hunt, C., and R. I. Morimoto. 1985. Conserved features of ekaryotic hsp70 genes revealed by comparison with the nucleotide sequence of human hsp70. Proc. Natl. Acad. Sci. USA 82:6455-6459.
40. Iwabe, N., K. Kuma, M. Hasegawa, S. Osawa, and T. Miyata. 1989. Evolutionary relationship of archaebacteria, eubacteria and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc. Natl. Acad. Sci. USA 86:9355-9359.
41. Jennifer, M., S. Barril, S. G. Kim, and C. A. Batt. 1994. Cloning and sequencing of the lactocossus lactis subsp, lactis dnaK gene using a PCR-based approach. Gene 142:91-96.
42. Kandler, O., and H. König. 1985. Cell envelopes of archaebacteria, p. 413-457. In C. R. Woese and R. S. Wolfe (ed.), The bacteria: a treatise on structure and function, vol. 8. Archaebacteria. Academic Press, London, United Kingdom.
43. Karlin, S. 1995. Statistical significance of sequence patterns in proteins. Curr. Opin. Struct. Biol. 5:360-371.
44. Karlin, S., G. M. Weinstock, and V. Brendl. 1995. Bacterial classifications derived from RecA protein sequence comparisons. J. Bacteriol. 177:6881-6893.
45. Kornak, J. M., C. C. Kuo, and L. A. Campbell. 1991, Sequence analysis of the gene encoding the Chlamydia pneumoniae DnaK protein homolog. Infect. Immun. 59:721-725.
46. Macario, A. J. L., C. B. Dugan, and E. C. D. Macario. 1991. A dnaK homolog in the archaebacterium Methanosarcino mazei S6. Gene 108:133-137.
47. Marshall, J. S., and K. Keegstra. 1992. Isolation and characterization of a cDNA clone encoding the major HSP70 of the pea chloroplast Stroma. Plant Physiol. (Rockville) 100:1048-1054.
48. McKenzie, K. R., E. Adamas, W. J. Britton, R. J. Garsia,and A. Basten. 1991. Sequence and immunogenicity of the 70-kDa heat shock protein of Mycobacterium leprat. J. Immunol. 147:312-319.
49. Morimoto, R. I., A. Tissieres, and C. Georgopoulos (ed.), 1994. The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
50. Murray, R. G. E. 1992. The family Deinococcaceae, p. 3732-3744. In A. Balows, H. G. Trüper, D. Martin, W. Harder, and K.-H. Schleifer (ed.), The prokaryotes, 2nd ed. Springer-Verlag, New York, N.Y.
51. Naberhaus, F., K. Giebesler, and H. Bahl, 1992. Molecular characterization of the dnaK region of Clostridium acetobutylicum, including grpE, dnaJ, and a new heat shock gene. J. Bacteriol. 174:3290-3299.
52. Nimura, K., H. Yoshikawa, and H. Takahashi. 1994. Identification of dnaK multigene family in Synchecococcus sp. PCC7942. Biochem. Biophys. Res. Commun. 201:466-471.
53. Normington, K., K. Kohno, Y. Kozutsumi, M. J. Gething, and J. Sambrook. 1989. Saccharomyces cerevisiae encodes an essential protein homologous in sequence and function to mammalian BIP. Cell 57:1223-1236.
54. Ohta, T., K. Saito, M. Kuroda, K. Honda, H. Hirata, and H. Hayashi. 1994. Molecular cloning of two new heat shock genes related to the hsp70 genes in Staphylococcus aureus. J. Bacteriol. 176:4779-4783.
55. Olsen, G. J., and C. R. Woese. 1993. Ribosomal RNA: a key to phylogeny. FASEB J. 7:113-123.
56. Olsen, G. J., C. R. Woese, and R. Overbeek. 1994. The winds of (evolutionary) change: breathing new life into microbiology. J. Bacteriol. 176:1-6.
57. Opperman, T., and J. P. Richardson. 1994. Phylogenetic analysis of sequences from diverse bacteria with homology to the Escherichia coli rho gene. J. Bacteriol. 176:5033-5044.
58. Palm, P., C. Schleper, I. Arnold-Ammer, I. Holz, T. Meier, F. Lottspeich, and W. Zillig. 1993. The DNA-dependent RNA polymerase of Thermotoga mairitima: characterization of the enzyme and the DNA sequence of the genes for the large subunits, Nucleic Acids Res. 21:4904-4908.
59. Partridge, J., J. King, J. Krska, D. Rockabrand, and P. Blum. 1993. Cloning, heterologous expression, and characterization of the Drysipelothrix rhusiopathie DnaK protein. Infect. Immun. 61:411-417.
60. Perry, J. J. 1992. The Genus Thermomicrobium, p. 3775-3779. In A. Balows, H. a Trüper, D. Martin, W. Harder, and K.-H. Schleifer (ed.), The prokaryotes, 2nd ed. Springer-Verlag, New York, N.Y.
61. Pesole, G., C. Gissi, C. Lanave, and C. Saccone. 1995. Glutamine synthetase gene evolution in bacteria. Mol. Biol. Evol. 12:189-197.
62. Reith, M., and J. Munholland. 1991. An HSP70 homolog is encoded on the plastid genome of the red alga, Porphyra umbilicalis. FEBS Lett. 294:116-120.
63. Rochester, D. E., J. A. Winer, and D. M. Shah. 1986. The structure and expression of maize genes encoding the major heat shock protein, hsp70. EMBO J. 5:451-458.
64. Rubin, D. M., A. Mehta, J. Zhu, S. Shoham, X. J. Chen, Q. Well, and K. B. Palter. 1993. Genomic structure and sequence analysis of Drosophila melanogaster HSC70 genes. Gene 128:155-163.
65. Saitou, N., and M. Nei. 1987. The neighbor joining method: a new method of reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
66. Seaton, B. L., and L. E. Vickery. 1994. A gene encoding a new Dnak/hsp70 homolog in Escherichia coli. Proc. Natl. Acad. Sci. USA 91:2066-2070.
67. Segal, G., and E. Z. Ron. 1995. The dnaKJ operon of Agrobacterium tumefaciens: transcriptional analysis and evidence for a new heat shock promoter. J. Bacteriol. 177:5952-5958.
68. Slater, M. R., and E. A. Craig. 1989. The SSA1 and SSA2 genes of the yeast Saccaromyces cerevisiae. Nucleic Acids Res. 17:805-806.
69. Smith, M. W., D. F. Feng, and R. F. Doolittle. 1992. Evolution by acquisition: the case for horizontal gene transfer. Trends Biochem. Sci. 17:489-493.
70. Sneath, P. H. A., N. S. Mair, M. E. Sharpe, and J. G. Holt (ed.), 1986. Bergey's manual of systematic bateriology, vol. 2, p. 1035-1043. Williams & Wilkins, Baltimore, Md.
71. Stanier, R. Y., and C. B. Van Niel. 1941. The main outlines of bacterial classification. J. Bacteriol. 42:437-466.
72. Stanier, R. Y., J. L. Ingraham, M. L. Wheelis, and P. R. Painter. 1987. The archaebacteria, p. 330-343. General microbiology, 5th ed. Macmillan Education Ltd., London, United Kingdom.
73. Stevenson, K., N. F. Inglis, B. Rae, W. Donachie, and J. M. Sharp. 1991. Complete nucleotide sequence of a gene encoding the 70 Kd heat shock protein of Mycobacterium paratuberculosis. Nucleic Acids Res. 19:4552.
74. Sussman, M. D., and P. Setlow. 1987. Nucleotide sequence of a Bacillus megaterium gene homologous to the dnaK gene of Escherichia coli. Nucleic Acids Res. 15:3923.
75. Tiboni, O., P. Cammarano, and A. M. Sanangelantoni. 1993. Cloning and sequencing of the gene coding glutamine synthetase I from the archaeum Pyntcoccus woesi: anomalous phylogenies inferred from analysis of archaeal and bacterial glutamine synthetase I sequence. J. Bacteriol. 175:2961-2969.
76. Ting, J., and A. S. Lee. 1988. Human gene encoding the 78,000-dalton glucose-regulated protein and its pseudogene: structure, conservation and regulation. DNA 1:275-286.
77. Van den Hynde, H., Y. Van de Peer, J. Perry, and R. deWachter. 1990. 5S rRNA sequences of representatives of the genera Chlorobium, Prosthecochloris, Thermomicrobium, Cytophaga, Flavobacterium, Flexibacter and Saprospira and a discussion of the evolution of bacteria in general. J. Gen. Microbiol. 136:11-18.
78. Van de Peer, Y., J.-M. Neefs, P. DeRijk, P. DeVos, and R. DeWachter. 1994. About the order of divergence of the major bacterial taxa during evolution. Syst. Appl. Microbiol. 17:32-38.
79. Van Neil, C. B. 1946. The classification and natural relationship of bacteria. Cold Spring Harbor Symp. Quant. Biol. 11:285-301.
80. Viale, A. M., and A. K. Arakaki, 1994. The chaperone connection to the origins of the eukuryotic organelles. FEBS Lett. 341:146-151.
81. Viale, A. M., A. K. Arakaki, F. C. Soncini, and R. G. Ferreyra. 1994. Evolutionary relationships among eubacterial groups as inferred from GroEL (chaperonin) sequence comparisons. Int. J. Syst. Bacteriol. 44:527-533.
82. Wilson, K. 1994. Preparation of genomic DNA from bacteria, p. 2.4.1-2.4.5. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore. J. G. Seidman, J. A. Smith, K. Struhl, L. M. Albright, D. M. Coen, A. Varki, and K. Janssen (ed.), Current protocols in molecular biology, 2nd ed., vol. 1. John Wiley & Sons. Inc., New York, N.Y.
83. Winefield, C. S., K. J. F. Farnden, P. H. S. Reynolds, and C. J. Marshall. 1995. Evolutionary analysis of aspartate aminotransferases. J. Mol. Evol. 40:455-463.
84. Woese, C. R. 1987. Bacterial evolution, Microbiol. Rev. 31:221-271.
85. Woese, C. R. 1991. The use of ribosomal RNA in reconstructing evolutionary relationships among bacteria, p. 1-24. In R. K. Selander, A. G. Clark, and T. S. Whittmay (ed.), Evolution at the molecular level. Sinauer Associates Inc., Publishers, Sunderland, Mass.
86. Woese, C. R. 1994. There must be a prokaryote somewhere: microbiology's search for itself. Microbiol. Rev. 58:1-9.
87. Woese, C. R., O. Kandler, and M. L. Wheelis. 1990. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria and Eucarya. Proc. Natl. Acad. Sci. USA 87:4576-4579.
88. Zuber, M., T. A. Hoover, M. T. Dertzbaugh, and D. L. Court. 1995. Analysis of the DnaK molecular chaperone system of Francisella tulareusis. Gene 164:149-152.
89. Zuckerkandl, E., and L. Pauling. 1965. Molecules as documents of evolutionary history. J. Theor. Biol. 8:357-366.