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Sequence evidence in the archaeal genomes that tRNAs emerged through the combination of ancestral genes as 5' and 3' tRNA halves.

Fujishima K, Sugahara J, Tomita M, Kanai A - PLoS ONE (2008)

Bottom Line: Furthermore, the combinations of 5' and 3' halves corresponded with the variation of amino acids in the codon table.We found not only universally conserved combinations of 5'-3' tRNA halves in tRNA(iMet), tRNA(Thr), tRNA(Ile), tRNA(Gly), tRNA(Gln), tRNA(Glu), tRNA(Asp), tRNA(Lys), tRNA(Arg) and tRNA(Leu) but also phylum-specific combinations in tRNA(Pro), tRNA(Ala), and tRNA(Trp).Our results support the idea that tRNA emerged through the combination of separate genes and explain the sequence diversity that arose during archaeal tRNA evolution.

View Article: PubMed Central - PubMed

Affiliation: Institute for Advanced Biosciences, Keio University, Tsuruoka, Yamagata, Japan.

ABSTRACT
The discovery of separate 5' and 3' halves of transfer RNA (tRNA) molecules-so-called split tRNA-in the archaeal parasite Nanoarchaeum equitans made us wonder whether ancestral tRNA was encoded on 1 or 2 genes. We performed a comprehensive phylogenetic analysis of tRNAs in 45 archaeal species to explore the relationship between the three types of tRNAs (nonintronic, intronic and split). We classified 1953 mature tRNA sequences into 22 clusters. All split tRNAs have shown phylogenetic relationships with other tRNAs possessing the same anticodon. We also mimicked split tRNA by artificially separating the tRNA sequences of 7 primitive archaeal species at the anticodon and analyzed the sequence similarity and diversity of the 5' and 3' tRNA halves. Network analysis revealed specific characteristics of and topological differences between the 5' and 3' tRNA halves: the 5' half sequences were categorized into 6 distinct groups with a sequence similarity of >80%, while the 3' half sequences were categorized into 9 groups with a higher sequence similarity of >88%, suggesting different evolutionary backgrounds of the 2 halves. Furthermore, the combinations of 5' and 3' halves corresponded with the variation of amino acids in the codon table. We found not only universally conserved combinations of 5'-3' tRNA halves in tRNA(iMet), tRNA(Thr), tRNA(Ile), tRNA(Gly), tRNA(Gln), tRNA(Glu), tRNA(Asp), tRNA(Lys), tRNA(Arg) and tRNA(Leu) but also phylum-specific combinations in tRNA(Pro), tRNA(Ala), and tRNA(Trp). Our results support the idea that tRNA emerged through the combination of separate genes and explain the sequence diversity that arose during archaeal tRNA evolution.

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Comparison of the 3 types of tRNA sequences.(A) Full nucleotide sequences of pre-tRNAs (1 split tRNALys [Neq] and 2 intronic tRNAArgs [Pae]) and 2 nonintronic tRNALys (Pfu and Afu) were aligned. Black bar marks the intron of the intronic tRNAs and the leader sequences of the split tRNAs, which are inserted at tRNA nucleotide position 32/33. Red bar marks the anticodon. (B) Comparison of the secondary structures and nucleotide sequences around the exon–intron boundary of the 3 types of tRNAs. Nucleotides that are identical between leader sequence and intron are shown in red. Red bar marks the anticodon.
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pone-0001622-g002: Comparison of the 3 types of tRNA sequences.(A) Full nucleotide sequences of pre-tRNAs (1 split tRNALys [Neq] and 2 intronic tRNAArgs [Pae]) and 2 nonintronic tRNALys (Pfu and Afu) were aligned. Black bar marks the intron of the intronic tRNAs and the leader sequences of the split tRNAs, which are inserted at tRNA nucleotide position 32/33. Red bar marks the anticodon. (B) Comparison of the secondary structures and nucleotide sequences around the exon–intron boundary of the 3 types of tRNAs. Nucleotides that are identical between leader sequence and intron are shown in red. Red bar marks the anticodon.

Mentions: Since 4 out of the 6 split tRNAs possessed clear sequence similarity with other tRNAs with the same anticodons, we focused on the precise phylogeny of the 6 split tRNAs from N. equitans in relation to other archaeal tRNAs. We performed detailed phylogenetic analysis for each of the 6 split tRNAs based on the Bayesian method (Supplemental Fig. S2). Mature sequences of 3 split tRNAs (tRNAiMet, tRNALys and tRNAGln) branched with other tRNAs with same anticodon from Crenarchaeota and Euryarchaeota lineages. Split tRNAHis clustered with tRNAHis from the Crenarchaeota lineage and M. kandleri. The most notable was split tRNAGlu, which located at the root of tRNAGlu cluster. The phylogenetic position of split tRNAGlu in NJ tree was adjacent to tRNAGln and tRNATrp cluster, although this contradiction exemplifies the sequence ambiguity of split tRNAGlu. Thus, split tRNAs reveal various characteristics in the phylogeny of archaeal tRNAs—universal (tRNAiMet, tRNALys and tRNAGln), crenarchaeal-specific (tRNAHis), and unique (tRNAGlu) phylogenetic positions—suggesting that split tRNA could be the ancestral form of tRNAs. Besides, intronic tRNAs were scattered throughout tRNA phylogeny in almost every tRNA clusters with introns positioned at the same location as the 5′–3′ boundary of the split tRNAs. We found an intronic tRNAArg with an intron sequence possessing 58% identity to that of the split tRNALys leader sequence located at the same position as that of the intron position (Fig. 2). Both tRNA belongs to the same cluster (cluster 22 in Fig. 1) suggesting that some intronic tRNAs may have emerged from integrated split tRNA in the archaeal genome.


Sequence evidence in the archaeal genomes that tRNAs emerged through the combination of ancestral genes as 5' and 3' tRNA halves.

Fujishima K, Sugahara J, Tomita M, Kanai A - PLoS ONE (2008)

Comparison of the 3 types of tRNA sequences.(A) Full nucleotide sequences of pre-tRNAs (1 split tRNALys [Neq] and 2 intronic tRNAArgs [Pae]) and 2 nonintronic tRNALys (Pfu and Afu) were aligned. Black bar marks the intron of the intronic tRNAs and the leader sequences of the split tRNAs, which are inserted at tRNA nucleotide position 32/33. Red bar marks the anticodon. (B) Comparison of the secondary structures and nucleotide sequences around the exon–intron boundary of the 3 types of tRNAs. Nucleotides that are identical between leader sequence and intron are shown in red. Red bar marks the anticodon.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2237900&req=5

pone-0001622-g002: Comparison of the 3 types of tRNA sequences.(A) Full nucleotide sequences of pre-tRNAs (1 split tRNALys [Neq] and 2 intronic tRNAArgs [Pae]) and 2 nonintronic tRNALys (Pfu and Afu) were aligned. Black bar marks the intron of the intronic tRNAs and the leader sequences of the split tRNAs, which are inserted at tRNA nucleotide position 32/33. Red bar marks the anticodon. (B) Comparison of the secondary structures and nucleotide sequences around the exon–intron boundary of the 3 types of tRNAs. Nucleotides that are identical between leader sequence and intron are shown in red. Red bar marks the anticodon.
Mentions: Since 4 out of the 6 split tRNAs possessed clear sequence similarity with other tRNAs with the same anticodons, we focused on the precise phylogeny of the 6 split tRNAs from N. equitans in relation to other archaeal tRNAs. We performed detailed phylogenetic analysis for each of the 6 split tRNAs based on the Bayesian method (Supplemental Fig. S2). Mature sequences of 3 split tRNAs (tRNAiMet, tRNALys and tRNAGln) branched with other tRNAs with same anticodon from Crenarchaeota and Euryarchaeota lineages. Split tRNAHis clustered with tRNAHis from the Crenarchaeota lineage and M. kandleri. The most notable was split tRNAGlu, which located at the root of tRNAGlu cluster. The phylogenetic position of split tRNAGlu in NJ tree was adjacent to tRNAGln and tRNATrp cluster, although this contradiction exemplifies the sequence ambiguity of split tRNAGlu. Thus, split tRNAs reveal various characteristics in the phylogeny of archaeal tRNAs—universal (tRNAiMet, tRNALys and tRNAGln), crenarchaeal-specific (tRNAHis), and unique (tRNAGlu) phylogenetic positions—suggesting that split tRNA could be the ancestral form of tRNAs. Besides, intronic tRNAs were scattered throughout tRNA phylogeny in almost every tRNA clusters with introns positioned at the same location as the 5′–3′ boundary of the split tRNAs. We found an intronic tRNAArg with an intron sequence possessing 58% identity to that of the split tRNALys leader sequence located at the same position as that of the intron position (Fig. 2). Both tRNA belongs to the same cluster (cluster 22 in Fig. 1) suggesting that some intronic tRNAs may have emerged from integrated split tRNA in the archaeal genome.

Bottom Line: Furthermore, the combinations of 5' and 3' halves corresponded with the variation of amino acids in the codon table.We found not only universally conserved combinations of 5'-3' tRNA halves in tRNA(iMet), tRNA(Thr), tRNA(Ile), tRNA(Gly), tRNA(Gln), tRNA(Glu), tRNA(Asp), tRNA(Lys), tRNA(Arg) and tRNA(Leu) but also phylum-specific combinations in tRNA(Pro), tRNA(Ala), and tRNA(Trp).Our results support the idea that tRNA emerged through the combination of separate genes and explain the sequence diversity that arose during archaeal tRNA evolution.

View Article: PubMed Central - PubMed

Affiliation: Institute for Advanced Biosciences, Keio University, Tsuruoka, Yamagata, Japan.

ABSTRACT
The discovery of separate 5' and 3' halves of transfer RNA (tRNA) molecules-so-called split tRNA-in the archaeal parasite Nanoarchaeum equitans made us wonder whether ancestral tRNA was encoded on 1 or 2 genes. We performed a comprehensive phylogenetic analysis of tRNAs in 45 archaeal species to explore the relationship between the three types of tRNAs (nonintronic, intronic and split). We classified 1953 mature tRNA sequences into 22 clusters. All split tRNAs have shown phylogenetic relationships with other tRNAs possessing the same anticodon. We also mimicked split tRNA by artificially separating the tRNA sequences of 7 primitive archaeal species at the anticodon and analyzed the sequence similarity and diversity of the 5' and 3' tRNA halves. Network analysis revealed specific characteristics of and topological differences between the 5' and 3' tRNA halves: the 5' half sequences were categorized into 6 distinct groups with a sequence similarity of >80%, while the 3' half sequences were categorized into 9 groups with a higher sequence similarity of >88%, suggesting different evolutionary backgrounds of the 2 halves. Furthermore, the combinations of 5' and 3' halves corresponded with the variation of amino acids in the codon table. We found not only universally conserved combinations of 5'-3' tRNA halves in tRNA(iMet), tRNA(Thr), tRNA(Ile), tRNA(Gly), tRNA(Gln), tRNA(Glu), tRNA(Asp), tRNA(Lys), tRNA(Arg) and tRNA(Leu) but also phylum-specific combinations in tRNA(Pro), tRNA(Ala), and tRNA(Trp). Our results support the idea that tRNA emerged through the combination of separate genes and explain the sequence diversity that arose during archaeal tRNA evolution.

Show MeSH