Limits...
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.

Show MeSH
Phylogenetic tree of mature tRNA sequences in 45 archaeal species.The phylogenetic neighbor-joining tree was constructed by using mature sequences of 1953 predicted tRNAs from the complete genomes of 45 archaeal species. Clusters are numbered from 1 to 22, and tRNAs within each cluster are denoted by amino acids corresponding to the anticodon. Clusters including tRNAs from all 3 archaeal phyla (Euryarchaeota, Crenarchaeota, and Nanoarchaeota) are shaded in blue. The amino acids corresponding to the split tRNAs are boxed.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2237900&req=5

pone-0001622-g001: Phylogenetic tree of mature tRNA sequences in 45 archaeal species.The phylogenetic neighbor-joining tree was constructed by using mature sequences of 1953 predicted tRNAs from the complete genomes of 45 archaeal species. Clusters are numbered from 1 to 22, and tRNAs within each cluster are denoted by amino acids corresponding to the anticodon. Clusters including tRNAs from all 3 archaeal phyla (Euryarchaeota, Crenarchaeota, and Nanoarchaeota) are shaded in blue. The amino acids corresponding to the split tRNAs are boxed.

Mentions: We predicted 1977 putative tRNA candidates from the genome sequences of 45 archaeal species with 2 tRNA predicting programs, SPLITS [7], [8] and tRNAscan-SE [25]. All tRNA sequences were manually checked, and 24 false candidates (tRNA-like sequences used for viral integration, and pseudogenes) were eliminated from the dataset. The resulting 1953 archaeal tRNAs, including 6 known split tRNAs and 423 intronic tRNAs, were used as a dataset for phylogenetic analysis. We performed structural alignment based on their mature tRNA sequences (from which introns and leader sequences were deleted) by manually improving the multiple alignment data through complete matching of the consensus nucleotides conserved among archaeal tRNAs (see Methods for detail). An unrooted neighbor-joining (NJ) tree was then produced. As a result, 1953 tRNAs were separated into 22 clusters: 12 dominated by tRNAs with its anticodon corresponding to a single type of amino acid (e.g., a tRNA for Ala), and 10 consisting of tRNAs with anticodons corresponding to 2 to 4 amino acids (e.g., a tRNA for Arg-Lys-Trp [i.e., 3 amino acids]) (Fig. 1). For example, 89 out of 90 archaeal tRNAGln were clustered in the same branch (cluster 16); and all tRNAAsp and tRNAGlu except the split tRNAGlu were clustered indistinguishably in the same branch (cluster 17). Like as Asp-Glu cluster, there are several indistinguishable pairs of amino acids clustered in the same branch that are in precursor-product relationship or in biosynthetic relationship (ex: Ala-Val, Arg-Lys, Phe-Tyr, Cys-Ser) supporting the coevolution theory of the origin of the genetic code [26].


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)

Phylogenetic tree of mature tRNA sequences in 45 archaeal species.The phylogenetic neighbor-joining tree was constructed by using mature sequences of 1953 predicted tRNAs from the complete genomes of 45 archaeal species. Clusters are numbered from 1 to 22, and tRNAs within each cluster are denoted by amino acids corresponding to the anticodon. Clusters including tRNAs from all 3 archaeal phyla (Euryarchaeota, Crenarchaeota, and Nanoarchaeota) are shaded in blue. The amino acids corresponding to the split tRNAs are boxed.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2237900&req=5

pone-0001622-g001: Phylogenetic tree of mature tRNA sequences in 45 archaeal species.The phylogenetic neighbor-joining tree was constructed by using mature sequences of 1953 predicted tRNAs from the complete genomes of 45 archaeal species. Clusters are numbered from 1 to 22, and tRNAs within each cluster are denoted by amino acids corresponding to the anticodon. Clusters including tRNAs from all 3 archaeal phyla (Euryarchaeota, Crenarchaeota, and Nanoarchaeota) are shaded in blue. The amino acids corresponding to the split tRNAs are boxed.
Mentions: We predicted 1977 putative tRNA candidates from the genome sequences of 45 archaeal species with 2 tRNA predicting programs, SPLITS [7], [8] and tRNAscan-SE [25]. All tRNA sequences were manually checked, and 24 false candidates (tRNA-like sequences used for viral integration, and pseudogenes) were eliminated from the dataset. The resulting 1953 archaeal tRNAs, including 6 known split tRNAs and 423 intronic tRNAs, were used as a dataset for phylogenetic analysis. We performed structural alignment based on their mature tRNA sequences (from which introns and leader sequences were deleted) by manually improving the multiple alignment data through complete matching of the consensus nucleotides conserved among archaeal tRNAs (see Methods for detail). An unrooted neighbor-joining (NJ) tree was then produced. As a result, 1953 tRNAs were separated into 22 clusters: 12 dominated by tRNAs with its anticodon corresponding to a single type of amino acid (e.g., a tRNA for Ala), and 10 consisting of tRNAs with anticodons corresponding to 2 to 4 amino acids (e.g., a tRNA for Arg-Lys-Trp [i.e., 3 amino acids]) (Fig. 1). For example, 89 out of 90 archaeal tRNAGln were clustered in the same branch (cluster 16); and all tRNAAsp and tRNAGlu except the split tRNAGlu were clustered indistinguishably in the same branch (cluster 17). Like as Asp-Glu cluster, there are several indistinguishable pairs of amino acids clustered in the same branch that are in precursor-product relationship or in biosynthetic relationship (ex: Ala-Val, Arg-Lys, Phe-Tyr, Cys-Ser) supporting the coevolution theory of the origin of the genetic code [26].

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