Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1997 Nov;179(21):6798–6806. doi: 10.1128/jb.179.21.6798-6806.1997

Origin and evolution of group I introns in cyanobacterial tRNA genes.

B Paquin 1, S D Kathe 1, S A Nierzwicki-Bauer 1, D A Shub 1
PMCID: PMC179611  PMID: 9352932

Abstract

Many tRNA(Leu)UAA genes from plastids contain a group I intron. An intron is also inserted in the same gene at the same position in cyanobacteria, the bacterial progenitors of plastids, suggesting an ancient bacterial origin for this intron. A group I intron has also been found in the tRNA(fMet) gene of some cyanobacteria but not in plastids, suggesting a more recent origin for this intron. In this study, we investigate the phylogenetic distributions of the two introns among cyanobacteria, from the earliest branching to the more derived species. The phylogenetic distribution of the tRNA(Leu)UAA intron follows the clustering of rRNA sequences, being either absent or present in clades of closely related species, with only one exception in the Pseudanabaena group. Our data support the notion that the tRNA(Leu)UAA intron was inherited by cyanobacteria and plastids through a common ancestor. Conversely, the tRNA(fMet) intron has a sporadic distribution, implying that many gains and losses occurred during cyanobacterial evolution. Interestingly, a phylogenetic tree inferred from intronic sequences clearly separates the different tRNA introns, suggesting that each family has its own evolutionary history.

Full Text

The Full Text of this article is available as a PDF (979.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Bell-Pedersen D., Quirk S., Clyman J., Belfort M. Intron mobility in phage T4 is dependent upon a distinctive class of endonucleases and independent of DNA sequences encoding the intron core: mechanistic and evolutionary implications. Nucleic Acids Res. 1990 Jul 11;18(13):3763–3770. doi: 10.1093/nar/18.13.3763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bhattacharya D., Surek B., Rüsing M., Damberger S., Melkonian M. Group I introns are inherited through common ancestry in the nuclear-encoded rRNA of Zygnematales (Charophyceae). Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):9916–9920. doi: 10.1073/pnas.91.21.9916. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Biniszkiewicz D., Cesnaviciene E., Shub D. A. Self-splicing group I intron in cyanobacterial initiator methionine tRNA: evidence for lateral transfer of introns in bacteria. EMBO J. 1994 Oct 3;13(19):4629–4635. doi: 10.1002/j.1460-2075.1994.tb06785.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cech T. R., Damberger S. H., Gutell R. R. Representation of the secondary and tertiary structure of group I introns. Nat Struct Biol. 1994 May;1(5):273–280. doi: 10.1038/nsb0594-273. [DOI] [PubMed] [Google Scholar]
  6. Chen Z. Y., Moroney J. V. Identification of a Chlamydomonas reinhardtii chloroplast gene with significant homology to bacterial genes involved in cytochrome c biosynthesis. Plant Physiol. 1995 Jun;108(2):843–844. doi: 10.1104/pp.108.2.843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Damberger S. H., Gutell R. R. A comparative database of group I intron structures. Nucleic Acids Res. 1994 Sep;22(17):3508–3510. doi: 10.1093/nar/22.17.3508. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Darnell J. E., Doolittle W. F. Speculations on the early course of evolution. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1271–1275. doi: 10.1073/pnas.83.5.1271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Delwiche C. F., Kuhsel M., Palmer J. D. Phylogenetic analysis of tufA sequences indicates a cyanobacterial origin of all plastids. Mol Phylogenet Evol. 1995 Jun;4(2):110–128. doi: 10.1006/mpev.1995.1012. [DOI] [PubMed] [Google Scholar]
  10. Ferat J. L., Le Gouar M., Michel F. Multiple group II self-splicing introns in mobile DNA from Escherichia coli. C R Acad Sci III. 1994 Feb;317(2):141–148. [PubMed] [Google Scholar]
  11. Ferat J. L., Michel F. Group II self-splicing introns in bacteria. Nature. 1993 Jul 22;364(6435):358–361. doi: 10.1038/364358a0. [DOI] [PubMed] [Google Scholar]
  12. Giovannoni S. J., Turner S., Olsen G. J., Barns S., Lane D. J., Pace N. R. Evolutionary relationships among cyanobacteria and green chloroplasts. J Bacteriol. 1988 Aug;170(8):3584–3592. doi: 10.1128/jb.170.8.3584-3592.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hallick R. B., Hong L., Drager R. G., Favreau M. R., Monfort A., Orsat B., Spielmann A., Stutz E. Complete sequence of Euglena gracilis chloroplast DNA. Nucleic Acids Res. 1993 Jul 25;21(15):3537–3544. doi: 10.1093/nar/21.15.3537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Johnson P. F., Abelson J. The yeast tRNATyr gene intron is essential for correct modification of its tRNA product. Nature. 1983 Apr 21;302(5910):681–687. doi: 10.1038/302681a0. [DOI] [PubMed] [Google Scholar]
  15. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980 Dec;16(2):111–120. doi: 10.1007/BF01731581. [DOI] [PubMed] [Google Scholar]
  16. Kruger K., Grabowski P. J., Zaug A. J., Sands J., Gottschling D. E., Cech T. R. Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell. 1982 Nov;31(1):147–157. doi: 10.1016/0092-8674(82)90414-7. [DOI] [PubMed] [Google Scholar]
  17. Kuhsel M. G., Strickland R., Palmer J. D. An ancient group I intron shared by eubacteria and chloroplasts. Science. 1990 Dec 14;250(4987):1570–1573. doi: 10.1126/science.2125748. [DOI] [PubMed] [Google Scholar]
  18. Lambowitz A. M., Belfort M. Introns as mobile genetic elements. Annu Rev Biochem. 1993;62:587–622. doi: 10.1146/annurev.bi.62.070193.003103. [DOI] [PubMed] [Google Scholar]
  19. Maidak B. L., Olsen G. J., Larsen N., Overbeek R., McCaughey M. J., Woese C. R. The Ribosomal Database Project (RDP). Nucleic Acids Res. 1996 Jan 1;24(1):82–85. doi: 10.1093/nar/24.1.82. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Michel F., Westhof E. Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J Mol Biol. 1990 Dec 5;216(3):585–610. doi: 10.1016/0022-2836(90)90386-Z. [DOI] [PubMed] [Google Scholar]
  21. Oda K., Yamato K., Ohta E., Nakamura Y., Takemura M., Nozato N., Akashi K., Kanegae T., Ogura Y., Kohchi T. Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. A primitive form of plant mitochondrial genome. J Mol Biol. 1992 Jan 5;223(1):1–7. doi: 10.1016/0022-2836(92)90708-r. [DOI] [PubMed] [Google Scholar]
  22. Ohta E., Oda K., Yamato K., Nakamura Y., Takemura M., Nozato N., Akashi K., Ohyama K., Michel F. Group I introns in the liverwort mitochondrial genome: the gene coding for subunit 1 of cytochrome oxidase shares five intron positions with its fungal counterparts. Nucleic Acids Res. 1993 Mar 11;21(5):1297–1305. doi: 10.1093/nar/21.5.1297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Olsen G. J., Matsuda H., Hagstrom R., Overbeek R. fastDNAmL: a tool for construction of phylogenetic trees of DNA sequences using maximum likelihood. Comput Appl Biosci. 1994 Feb;10(1):41–48. doi: 10.1093/bioinformatics/10.1.41. [DOI] [PubMed] [Google Scholar]
  24. Palmer J. D., Logsdon J. M., Jr The recent origins of introns. Curr Opin Genet Dev. 1991 Dec;1(4):470–477. doi: 10.1016/s0959-437x(05)80194-7. [DOI] [PubMed] [Google Scholar]
  25. Peebles C. L., Perlman P. S., Mecklenburg K. L., Petrillo M. L., Tabor J. H., Jarrell K. A., Cheng H. L. A self-splicing RNA excises an intron lariat. Cell. 1986 Jan 31;44(2):213–223. doi: 10.1016/0092-8674(86)90755-5. [DOI] [PubMed] [Google Scholar]
  26. RajBhandary U. L. Initiator transfer RNAs. J Bacteriol. 1994 Feb;176(3):547–552. doi: 10.1128/jb.176.3.547-552.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Reinhold-Hurek B., Shub D. A. Self-splicing introns in tRNA genes of widely divergent bacteria. Nature. 1992 May 14;357(6374):173–176. doi: 10.1038/357173a0. [DOI] [PubMed] [Google Scholar]
  28. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  29. Shub D. A. The antiquity of group I introns. Curr Opin Genet Dev. 1991 Dec;1(4):478–484. doi: 10.1016/s0959-437x(05)80195-9. [DOI] [PubMed] [Google Scholar]
  30. Sprinzl M., Steegborn C., Hübel F., Steinberg S. Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 1996 Jan 1;24(1):68–72. doi: 10.1093/nar/24.1.68. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Szweykowska-Kulinska Z., Senger B., Keith G., Fasiolo F., Grosjean H. Intron-dependent formation of pseudouridines in the anticodon of Saccharomyces cerevisiae minor tRNA(Ile). EMBO J. 1994 Oct 3;13(19):4636–4644. doi: 10.1002/j.1460-2075.1994.tb06786.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wilmotte A., Neefs J. M., De Wachter R. Evolutionary affiliation of the marine nitrogen-fixing cyanobacterium Trichodesmium sp. strain NIBB 1067, derived by 16S ribosomal RNA sequence analysis. Microbiology. 1994 Aug;140(Pt 8):2159–2164. doi: 10.1099/13500872-140-8-2159. [DOI] [PubMed] [Google Scholar]
  33. Woodson S. A., Cech T. R. Reverse self-splicing of the tetrahymena group I intron: implication for the directionality of splicing and for intron transposition. Cell. 1989 Apr 21;57(2):335–345. doi: 10.1016/0092-8674(89)90971-9. [DOI] [PubMed] [Google Scholar]
  34. Xu M. Q., Kathe S. D., Goodrich-Blair H., Nierzwicki-Bauer S. A., Shub D. A. Bacterial origin of a chloroplast intron: conserved self-splicing group I introns in cyanobacteria. Science. 1990 Dec 14;250(4987):1566–1570. doi: 10.1126/science.2125747. [DOI] [PubMed] [Google Scholar]
  35. Zaug A. J., McEvoy M. M., Cech T. R. Self-splicing of the group I intron from Anabaena pre-tRNA: requirement for base-pairing of the exons in the anticodon stem. Biochemistry. 1993 Aug 10;32(31):7946–7953. doi: 10.1021/bi00082a016. [DOI] [PubMed] [Google Scholar]
  36. van der Veen R., Arnberg A. C., van der Horst G., Bonen L., Tabak H. F., Grivell L. A. Excised group II introns in yeast mitochondria are lariats and can be formed by self-splicing in vitro. Cell. 1986 Jan 31;44(2):225–234. doi: 10.1016/0092-8674(86)90756-7. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES