Molecular characterization and postsplicing fate of three introns within the single rRNA operon of the hyperthermophilic archaeon Aeropyrum pernix K1

Journal of Bacteriology

Volumn 180, Issue 14, 1998, Pages 3635-3643

  Nomura, Norimichi ^a   Sako, Yoshihiko ^a   Uchida, Aritsune ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; ENDONUCLEASE; RNA 16S; RNA 23S;

AEROPYRUM PERNIX; ARCHAEBACTERIUM; ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; INTRON; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OPERON; PRIORITY JOURNAL; RNA SEQUENCE; RNA SPLICING; RNA TRANSLATION; TWO DIMENSIONAL GEL ELECTROPHORESIS;

AEROPYRUM PERNIX; ARCHAEA; AROPYRUM; AROPYRUM PERNIX; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 0032464903     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.180.14.3635-3643.1998     Document Type: Article

References (65)

1. Apirion, D., and A. Miczak. 1993. RNA processing in prokaryotic cells. Bioessays 15:113-120.
2. Belfort, M. 1990. Phage T4 introns: self-splicing and mobility. Annu. Rev. Genet. 24:363-385.
3. Belfort, M., M. E. Reaban, T. Coetzee, and J. Z. Dalgaard. 1995. Prokaryotic introns and inteins: a panoply of form and function. J. Bacteriol. 177:3897-3903.
4. Beserga, S. J., and J. A. Steitz. 1993. The diverse world of small ribonucleoproteins, p. 359-381. In R. F. Gesteland and J. F. Atkins (ed.), The RNA world. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
5. Bulgin, A. B., K. Parodos, D. J. Lane, and N. R. Pace. 1990. The excision of intervening sequences from Salmonella 23S ribosomal RNA. Cell 60:405-414.
6. Burggraf, S., N. Larsen, C. R. Woese, and K. O. Stetter. 1993. An intron within the 16S ribosomal RNA gene of the archaeon Pyrobaculum aerophilum. Proc. Natl. Acad. Sci. USA 90:2547-2550.
7. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-PhOH-chloroform extraction. Anal. Biochem. 162:156-159.
8. Chu, F. K., G. F. Maley, F. Maley, and M. Belfort. 1984. Intervening sequence in the thymidylate synthase gene of bacteriophage T4. Proc. Natl. Acad. Sci. USA 81:3049-3053.
9. Colleaux, L., L. d'Auriol, M. Betermier, G. Cottarel, A. Jacquier, F. Galibert, and B. Dujon. 1986. Universal code equivalent of a yeast mitochondrial intron reading frame is expressed in E. coli as a specific double strand endonuclease. Cell 44:521-533.
10. Colleaux, L., L. d'Auriol, F. Galibert, and B. Dujon. 1988. Recognition and cleavage site of the intron-encoded omega transposase. Proc. Natl. Acad. Sci. USA 85:6022-6026.
11. Dalgaard, J. Z., and R. A. Garrett. 1992. Protein-coding introns from the 23S rRNA-encoding gene form stable circles in the hyperthermophilic archaeon Pyrobaculum organotrophum. Gene 121:103-110.
12. Datta, P. K., L. K. Hawkins, and R. Gupta. 1989. Presence of an intron in elongator methionine-tRNA of Halobacterium volcanii. Can. J. Microbiol. 35:189-194.
13. DiRuggiero, J., L. A. Achenbach, S. H. Brown, R. M. Kelly, and F. T. Robb. 1993. Regulation of ribosomal RNA transcription by growth rate of the hyperthermophilic archaeon, Pyrococcus furiosus. FEMS Microbiol. Lett. 111:159-164.
14. Durovic, P., and P. P. Dennis. 1994. Separate pathways for excision and processing of 16S and 23S rRNA from the primary rRNA operon transcript from the hyperthermophilic archaebacterium Sulfolobus acidocaldarius: similarities to eukaryotic rRNA processing. Mol. Microbiol. 13:229-242.
15. Ferat, J.-F., and F. Michel. 1993. Group II self-splicing introns in bacteria. Nature 364:358-361.
16. Ford, E., and M. Ares, Jr. 1994. Synthesis of circular RNA in bacteria and yeast using RNA cyclase ribozymes derived from a group I intron of phage T4. Proc. Natl. Acad. Sci. USA 91:3117-3121.
17. Garrett, R. A., J. Dalgaard, N. Larsen, J. Kjems, and A. S. Mankin. 1991. Archaeal rRNA operon. Trends Biochem. Sci. 16:22-26.
18. Goldrich-Blair, H., V. Scarlato, J. M. Gott, M.-Q. Xu, and D. A. Shub. 1990. A self-splicing group I intron in the DNA polymerase gene of Bacillus subtilis bacteriophage SPO1. Cell 63:417-424.
19. Gourse, R. L., T. Gaal, M. S. Bartlett, J. A. Appleman, and W. Ross. 1996. rRNA transcription and growth rate-dependent regulation of ribosome synthesis in Escherichia coli. Annu. Rev. Microbiol. 50:645-677.
20. Hain, J., W. D. Reiter, U. Hudepohl, and W. Zillig. 1992. Elements of an archaeal promoter defined by mutational analysis. Nucleic Acids Res. 20: 5423-5428.
21. Henikoff, S. 1984. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28:351-359.
22. Hernandez-Veerdun, D. 1991. The nucleolus today. J. Cell Sci. 99:465-471.
23. Hsu, D., M. Pan, Y. Zee, and R. B. LeFebvre. 1990. Unique ribosomal structure of Leptospira interrogans is composed of four rRNA component. J. Bacteriol. 172:3478-3480.
24. Kaine, B. P. 1987. Intron containing tRNA genes of Sulfolobus solfataricus. J. Mol. Evol. 25:248-254.
25. Kaine, B. P., R. Gupta, C. R. Woese. 1983. Putative introns in tRNA genes of prokaryotes. Proc. Natl. Acad. Sci. USA 80:3309-3312.
26. Kjems, J., and R. A. Garrett. 1985. An intron in the 23S ribosomal RNA gene of the archaebacterium Desulfurococcus mobilis. Nature 318:675-677.
27. Kjems, J., and R. A. Garrett. 1987. Novel expression of the ribosomal RNA genes in the extreme thermophile and archaebacterium Desulfurococcus mobilis. EMBO J. 6:3521-3530.
28. Kjems, J., and R. A. Garrett. 1988. Novel splicing mechanism for the ribosomal RNA intron in the archaebacterium Desulfurococcus mobilis. Cell 54: 693-703.
29. Kjems, J., and R. A. Garrett. 1991. Ribosomal RNA introns in archaea and evidence for RNA conformational changes associated with splicing. Proc. Natl. Acad. Sci. USA 88:439-443.
30. Kleman-Leyer, K., B. W. Armbruster, and C. J. Daniels. 1997. Properties of H. volcanii tRNA intron endonuclease reveal a relationship between the Archaeal and Eucaryal tRNA intron processing systems. Cell 89:839-847.
31. Klenk, H.-P., R. A. Clayton, J.-F. Tomb, O. White, K. E. Nelson, K. A. Ketchum, R. J. Dodson, M. Gwinn, E. K. Hichey, J. D. Pederson, D. L. Richardson, A. R. Kerlavage, D. E. Graham, N. C. Krypides, R. D. Fleischmann, J. Quackenbush, N. H. Lee, G. G. Sutton, S. Gill, E. F. Kirkness, K. A. Dougherty, K. McKenney, M. D. Adams, B. Loftus, S. Peterson, C. I. Reich, L. K. McNeil, J. H. Badger, A. Glodek, L. Zhou, R. Overbeek, J. D. Gocayne, J. F. Weidman, L. McDonald, T. Utterback, M. D. Cotton, T. Spriggs, P. Artiach, B. P. Kaine, S. M. Sykes, P. W. Sadow, K. P. D'Andrea, C. Bowman, C. Fujii, S. A. Garland, T. M. Mason, G. J. Olsen, C. M. Fraser, H. O. Smith, C. R. Woese, and J. C. Venter. 1997. The complete genome sequence of the hyperthermophilic, sulfate-reducing archaeon Archaeoglobus fulgidus. Nature 390:364-370.
32. Konkel, M. E., R. T. Marconi, D. J. Mead, and W. Ceiplak. 1994. Identification and characterization of an intervening sequence within the 23S ribosomal RNA genes of Campylobacter jejuni. Mol. Microbiol. 14:235-241.
33. Kordes, E., S. Jock, J. Fritsch, F. Bosch, and G. Klug. 1994. Cloning of a gene involved in rRNA precursor processing and 23S rRNA cleavage in Rhodobacter capsulatus. J. Bacteriol. 176:1121-1127.
34. Kuhsel, M. G., R. Strickl, and J. D. Palmer. 1990. An ancient group I intron shared by eubacteria and chloroplasts. Science 250:1570-1573.
35. Leffers, H., J. Kjems, L. Ostergaard, N. Larsen, and R. A. Garrett. 1987. Evolutionary relationship amongst archaebacteria. A comparative study of a sulphur-dependent extreme thermophile, an extreme halophile and a thermophilic methanogen. J. Mol. Biol. 195:43-61.
36. Lykke-Andersen, J., and R. A. Garrett. 1994. Structural characteristics of the stable RNA introns of archaeal hyperthermophiles and their splicing junctions. J. Mol. Biol. 243:846-855.
37. Lykke-Andersen, J., C. Aagaard, M. Semionenkov, and R. A. Garrett. 1997. Archaeal introns: splicing, intercellular mobility and evolution. Trends Biochem. Sci. 22:326-331.
38. Moazed, D., and H. F. Noller. 1986. Transfer RNA shields specific nucleotides in 16S ribosomal RNA from attack by chemical probes. Cell 47:985-994.
39. Moazed, D., and H. F. Noller. 1989. Interaction of tRNA with 23S rRNA in the ribosomal A, P, and E sites. Cell 57:585-597.
40. Moazed, D., and H. F. Noller. 1990. Binding of tRNA to the ribosomal A and P site protects two distinct sets of nucleotides in 16S rRNA. J. Mol. Biol. 211: 135-145.
41. Mueller, J. E., M. Bryk, N. Loizos, and M. Belfort. 1993. Homing endonucleases, p. 111-143. In S. M. Linn, R. S. Lloyd, and R. J. Roberts (ed.), Nucleases. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
42. Noller, H. F. 1984. Structure of ribosomal RNA. Annu. Rev. Biochem. 53: 119-162.
43. Nomura, N., Y. Sako, and A. Uchida. Unpublished data.
44. Otsuka, T., H. Nomiyama, H. Yoshida, T. Kukita, S. Kuhara, and Y. Sakaki. 1983. Complete nucleotide sequence of the 26S ribosomal RNA gene of Physarum polycephalum: its significance in gene evolution. Proc. Natl. Acad. Sci. USA 80:3163-3167.
45. Palmer, J. R., and C. J. Daniels. 1995. In vivo definition of an archaeal promoter. J. Bacteriol. 177:1844-1849.
46. Pearson, W. R., and D. J. Lipman. 1988. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 85:2444-2448.
47. Qu, L. H., B. Michot, and J.-P. Bachellerie. 1983. Improved methods for structure probing in large RNAs: a rapid 'heterologous' sequencing approach is coupled to the direct mapping of nuclease accessible sites. Application to the 5′ terminal domain of eukaryotic 28S rRNA. Nucleic Acids Res. 11:5903-5920.
48. Reinhold-Hurek, B., and D. A. Shub. 1992. Self-splicing introns in tRNA genes of widely divergent bacteria. Nature 357:173-176.
49. Reiter, W. D., P. Palm, and W. Zillig. 1988. Analysis of transcription in the archaebacterium Sulfolobus indicates that archaebacterial promoters are homologous to eukaryotic pol II promoters. Nucleic Acids Res. 16:1-19.
50. Sako, Y., N. Nomura, A. Uchida, Y. Ishida, H. Morii, Y. Koga, T. Hoaki, and T. Maruyama. 1996. Aeropyrum pernix gen. nov., sp. nov., a novel aerobic hyperthermophilic archaeon growing at temperatures up to 100°C. Int. J. Syst. Bacteriol. 46:1070-1077.
51. Sambrook, J. E., E. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
52. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
53. Schnare, M. N., and M. N. Gray. 1990. Sixteen discrete RNA components in the cytoplasmic ribosome of Euglena gracilis. J. Mol. Biol. 215:73-83.
54. Skurnik, M., and P. Toivanen. 1991. Intervening sequences (IVSs) in the 23S ribosomal RNA genes of pathogenic Yersinia enterocolitica. The IVSs in Y. enterocolitica and Salmonella typhimurium have a common origin. Mol. Microbiol. 5:585-593.
55. Smith, D. R., L. A. Doucette-Stamm, C. Deloughery, H. Lee, J. Dubois, T. Aldredge, R. Bashirzadeh, D. Blakely, R. Cook, K. Gilbert, D. Harrison, L. Hoang, P. Keagle, W. Lumm, B. Pothier, D. Qiu, R. Spadafora, R. Vicaire, Y. Wang, J. Wierzbowski, R. Gibson, N. Jiwani, A. Caruso, D. Bush, H. Safer, D. Patwell, S. Prabhakar, S. McDougall, G. Shimer, A. Goyal, S. Pietrokovski, G. M. Church, C. J. Daniels, J. Mao, P. Rice, J. Nolling, and J. N. Reeve. 1997. Complete genome sequence of Methanobacterium thermoautotrophicum ΔH: functional analysis and comparative genomics. J. Bacteriol. 179:7135-7155.
56. Spencer, D. F., J. Collings, M. N. Schnare, and M. W. Gray. 1987. Multiple spacer sequences in the nuclear large subunit ribosomal RNA gene of Crithidia fasciculata. EMBO J. 6:1063-1071.
57. Thomm, M., and G. Wich. 1988. An archaebacterial promoter element for stable RNA genes with homology to the TATA box of higher eukaryotes. Nucleic Acids Res. 16:151-163.
58. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
59. Thompson, J., F. Schmidt, and E. Cundliff. 1982. Site of action of a ribosomal RNA methylase conferring resistance to thiostrepton. J. Biol. Chem. 257:7915-7917.
60. Trp intron endonuclease from Halobacterium volcanii. Unique substrate recognition properties. J. Biol. Chem. 263:17951-17959.
61. Turmel, M., J. Boulanger, M. N. Schnare, M. W. Gray, C. Lemieux. 1991. Six group I introns and three internal transcribed spacers in the chloroplast large subunit ribosomal RNA gene of the green alga Chlamydomonas eugametos. J. Mol. Biol. 218:293-311.
62. Wang, H., R. J. DiGate, and N. C. Seaman. 1996. An RNA topoisomerase. Proc. Natl. Acad. Sci. USA 93:9477-9482.
63. Wich, G., W. Leinfelder, and A. Bock. 1987. Genes for stable RNA in the extreme thermophile Thermoproteus tenax introns and transcription signals. EMBO J. 6:523-528.
64. Xu, M-. Q., S. D. Kathe, H. Golgrich-Blair, S. A. Nierzwicki-Bauer, and D. A. Shub. 1990. Bacterial origin of a chloroplast intron: conserved self-splicing group I introns in cyanobacteria. Science 250:1566-1570.
65. Zuker, M., and P. Stieger. 1982. Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res. 9:133-148.