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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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Examples of tRNA sequences explained by specific combinations of 5′ and 3′ tRNA halves.(A) Examples of tRNA sequences with different 5′ half sequences but a common 3′ half sequence. (B) Example of tRNA sequences with different 3′ half sequences but a common 5′ half sequence. Asterisk denotes matching nucleotides in the aligned tRNA sequences. Boxes delineate sequences belonging to the same group in the sequence similarity network (Fig. 3). The corresponding group ID is labeled in a black box.
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pone-0001622-g006: Examples of tRNA sequences explained by specific combinations of 5′ and 3′ tRNA halves.(A) Examples of tRNA sequences with different 5′ half sequences but a common 3′ half sequence. (B) Example of tRNA sequences with different 3′ half sequences but a common 5′ half sequence. Asterisk denotes matching nucleotides in the aligned tRNA sequences. Boxes delineate sequences belonging to the same group in the sequence similarity network (Fig. 3). The corresponding group ID is labeled in a black box.

Mentions: Since the 5′ and 3′ halves are suggested to have had different evolutionary backgrounds, we hypothesized that the sequence variety of tRNAs was derived directly from different combinations of 5′ and 3′ tRNA sequences in the early stage of archaeal evolution. To examine the correlation between specific combinations of 5′ and 3′ halves and the corresponding amino acids in the codon table, we filled the codon table of 7 archaeal species by annotating each of the anticodons with the 5′ and 3′ group IDs denoted in Figure. 3. We have selected different sequence similarity thresholds (80% for 5′ half and 88% for 3′ half) for grouping the tRNA sequences, since the two networks possessed similar clustering coefficient of c = 0.08 and 0.05. Figure. 5 shows a codon table filled by the 5′ and 3′ group IDs of N. equitans tRNA sequences. Codon tables of the other 6 species are shown in Supplemental Figure S3. Group A is the largest group in the 3′ half network, accounting for 104/296 (35%) sequences of tRNAs corresponding to various amino acids. In N. equitans, 3′ half sequences of tRNAArg, tRNAIle, tRNAVal, tRNAAla, tRNAPro, tRNATrp, and tRNAPhe were all categorized as group A. Adding the 5′ sequence information further classified these tRNAs into small groups possessing the same 5′–3′ combination. For example, in all 7 species, the same 4–A combination was observed for tRNAArg and tRNALys; this, together with the fact that split tRNALys is clustered among the Arg-Lys cluster (Fig. 1), suggests that these tRNAs originated from a combination of ancestral minigenes of the 2 sequence groups. The same features are apparent in the 5–A combination of tRNAVal. Exceptionally, however, 2 tRNAVals in M. kandleri both have the 4–A combination located in unique cluster (cluster 11 in Fig. 1). M. kandleri is an intriguing species which possesses many unique tRNAs clustered at different phylogenetic positions from other tRNAs with the same anticodon (Supplemental Fig. 1). The N. equitans genome also encodes unique tRNAIle, which displays the only UAU (TAT) anticodon found in the Archaea. tRNAIle (Neq) is considered to be evolutionarily unique, as no homologous sequence has been found in any other archaeal species and therefore it is located within an isolated branch with various tRNAs from M. kandleri (cluster 11 in Fig. 1). However, by splitting the sequence of tRNAIle (Neq), we found tRNAGly(GCC) in N. equitans genome which possessed identical 3′ half but different 5′half (Fig. 6A). This sequence evidence supports our idea of the ancient integration of split tRNA genes.


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)

Examples of tRNA sequences explained by specific combinations of 5′ and 3′ tRNA halves.(A) Examples of tRNA sequences with different 5′ half sequences but a common 3′ half sequence. (B) Example of tRNA sequences with different 3′ half sequences but a common 5′ half sequence. Asterisk denotes matching nucleotides in the aligned tRNA sequences. Boxes delineate sequences belonging to the same group in the sequence similarity network (Fig. 3). The corresponding group ID is labeled in a black box.
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Related In: Results  -  Collection

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pone-0001622-g006: Examples of tRNA sequences explained by specific combinations of 5′ and 3′ tRNA halves.(A) Examples of tRNA sequences with different 5′ half sequences but a common 3′ half sequence. (B) Example of tRNA sequences with different 3′ half sequences but a common 5′ half sequence. Asterisk denotes matching nucleotides in the aligned tRNA sequences. Boxes delineate sequences belonging to the same group in the sequence similarity network (Fig. 3). The corresponding group ID is labeled in a black box.
Mentions: Since the 5′ and 3′ halves are suggested to have had different evolutionary backgrounds, we hypothesized that the sequence variety of tRNAs was derived directly from different combinations of 5′ and 3′ tRNA sequences in the early stage of archaeal evolution. To examine the correlation between specific combinations of 5′ and 3′ halves and the corresponding amino acids in the codon table, we filled the codon table of 7 archaeal species by annotating each of the anticodons with the 5′ and 3′ group IDs denoted in Figure. 3. We have selected different sequence similarity thresholds (80% for 5′ half and 88% for 3′ half) for grouping the tRNA sequences, since the two networks possessed similar clustering coefficient of c = 0.08 and 0.05. Figure. 5 shows a codon table filled by the 5′ and 3′ group IDs of N. equitans tRNA sequences. Codon tables of the other 6 species are shown in Supplemental Figure S3. Group A is the largest group in the 3′ half network, accounting for 104/296 (35%) sequences of tRNAs corresponding to various amino acids. In N. equitans, 3′ half sequences of tRNAArg, tRNAIle, tRNAVal, tRNAAla, tRNAPro, tRNATrp, and tRNAPhe were all categorized as group A. Adding the 5′ sequence information further classified these tRNAs into small groups possessing the same 5′–3′ combination. For example, in all 7 species, the same 4–A combination was observed for tRNAArg and tRNALys; this, together with the fact that split tRNALys is clustered among the Arg-Lys cluster (Fig. 1), suggests that these tRNAs originated from a combination of ancestral minigenes of the 2 sequence groups. The same features are apparent in the 5–A combination of tRNAVal. Exceptionally, however, 2 tRNAVals in M. kandleri both have the 4–A combination located in unique cluster (cluster 11 in Fig. 1). M. kandleri is an intriguing species which possesses many unique tRNAs clustered at different phylogenetic positions from other tRNAs with the same anticodon (Supplemental Fig. 1). The N. equitans genome also encodes unique tRNAIle, which displays the only UAU (TAT) anticodon found in the Archaea. tRNAIle (Neq) is considered to be evolutionarily unique, as no homologous sequence has been found in any other archaeal species and therefore it is located within an isolated branch with various tRNAs from M. kandleri (cluster 11 in Fig. 1). However, by splitting the sequence of tRNAIle (Neq), we found tRNAGly(GCC) in N. equitans genome which possessed identical 3′ half but different 5′half (Fig. 6A). This sequence evidence supports our idea of the ancient integration of split tRNA genes.

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