MBE Advance Access published online on October 1, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn216
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Research Article |
Comprehensive analysis of archaeal tRNA genes reveals rapid increase of tRNA introns in the order Thermoproteales
1 Institute for Advanced Biosciences, Keio University, Tsuruoka, 997-0017, Japan
2 Systems Biology Program, Graduate School of Media and Governance, Keio University, Fujisawa, 252-8520, Japan
3 Department of Environmental Information, Keio University, Fujisawa, 252-8520, Japan
To whom correspondence should be addressed: Akio Kanai, 403-1 Nihonkoku, Tsuruoka 997-0017, Yamagata, Japan, Phone: +81-235-29-0524, Fax: + 81-235-29-0525, E-mail: akio{at}sfc.keio.ac.jp.
Received for publication May 23, 2008. Revision received September 12, 2008. Accepted for publication September 24, 2008.
The analysis of archaeal tRNA genes is becoming more important to evaluate origin and evolution of tRNA molecule. Even with the recent accumulation of complete genomes of numerous archaeal species, several tRNA genes are still required for a full complement of the codon table. We conducted comprehensive screening of tRNA genes from 47 archaeal genomes by using a combination of different types of tRNA prediction programs, and extracted a total of 2143 reliable tRNA gene candidates including 437 intron-containing tRNA genes, which covered more than 99.9% of the codon tables in Archaea. Previously, the content of intron-containing tRNA genes in Archaea was estimated to be approximately 15% of the whole tRNA genes, and most of the introns were known to be located at canonical positions (nucleotide position between 37 and 38) of precursor tRNA (pre-tRNA). Surprisingly, we observed marked enrichment of tRNA introns in five species of the archaeal order Thermoproteales; about 70% of tRNA gene candidates were found to be intron-containing tRNA genes, half of which contained multiple introns, and the introns were located at various non-canonical positions. Sequence similarity analysis revealed that approximately half of the tRNA introns found at Thermoproteales-specific intron locations were highly conserved among several tRNA genes. Intriguingly, identical tRNA intron sequences were found within different types of tRNA genes that completely lacked exon sequence similarity, suggesting that the tRNA introns in Thermoproteales could have been gained via intron insertion events at a later stage of tRNA evolution. Moreover, although the CCA sequence at the 3'-terminal of pre-tRNA is added by a CCA-adding enzyme after gene transcription in Archaea, most of the tRNA genes containing highly conserved introns already encode the CCA sequence at their 3'-terminal. Based on these results, we propose possible models explaining the rapid increase of tRNA introns as a result of intron insertion events via retrotransposition of pre-tRNAs. The sequences and secondary structures of the tRNA genes and their BHB motifs were registered in SPLITSdb (http://splits.iab.keio.ac.jp/splitsdb/), a novel and comprehensive database for archaeal tRNA genes.
Key Words: tRNA • Archaea • intron • Bulge-Helix-Bulge (BHB) motif • Thermoproteales • Bioinformatics
* These authors contributed equally to this work.
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