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
Distribution of networks based on the 5′ and 3′ tRNA sequences.Relation between the number of tRNA sequences and the number of links is represented at 4 sequence similarity thresholds (A–D). Clustering coefficient c is denoted for each tRNA halves.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2237900&req=5

pone-0001622-g004: Distribution of networks based on the 5′ and 3′ tRNA sequences.Relation between the number of tRNA sequences and the number of links is represented at 4 sequence similarity thresholds (A–D). Clustering coefficient c is denoted for each tRNA halves.

Mentions: To characterize the overall network topology of the 5′ and 3′ halves, we compared the 2 networks by measuring the distribution of the number of connections per node (connectivity distribution). Network topology can be classified into 2 distinct types: ‘scale-free networks’, in which a few nodes have many links but most have only a few links, and which follow a power-law distribution [28]; and ‘small-world networks’, which consist of nodes linked randomly and follow a Poisson or exponential distribution [29]. We found obvious difference in degree distribution between the 2 networks at all similarity thresholds (Fig. 4). At a similarity threshold of >75%, the clustering coefficient c (degree of linkage between nodes) of 5′ half was only 0.17 while 3′ half was 0.47, which means that 47% of all possible connection are used. The power-law-like distribution of the 5′ half network was enhanced as the similarity threshold increased, while the distribution of 3′ half network changed from Poisson-like (>75%) to irregular (>80–85%) then finally a power-law-like distribution at a sequence similarity of >88%. Meanwhile, the ratio of the cluster coefficient between 5′ and 3′ halves were constantly 1∶2.5–1∶4 showing that characteristics of the 2 tRNA domains significantly differ at all level of sequence threshold (75%–88%). We suggest that high commonality of the 3′ half sequences is one of the evidence of which 3′ half could have had a single origin. On the other hand, the scale-free distribution of the 5′ half represents a specific sequence characteristic within each sequence group, suggesting a non-monophyletic origin of the 5′ half sequences. These different sequence characteristics of the 5′ and 3′ tRNA halves further support the idea that ancient archaeal tRNA emerged from a specific combination of 5′ and 3′ halves.


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)

Distribution of networks based on the 5′ and 3′ tRNA sequences.Relation between the number of tRNA sequences and the number of links is represented at 4 sequence similarity thresholds (A–D). Clustering coefficient c is denoted for each tRNA halves.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0001622-g004: Distribution of networks based on the 5′ and 3′ tRNA sequences.Relation between the number of tRNA sequences and the number of links is represented at 4 sequence similarity thresholds (A–D). Clustering coefficient c is denoted for each tRNA halves.
Mentions: To characterize the overall network topology of the 5′ and 3′ halves, we compared the 2 networks by measuring the distribution of the number of connections per node (connectivity distribution). Network topology can be classified into 2 distinct types: ‘scale-free networks’, in which a few nodes have many links but most have only a few links, and which follow a power-law distribution [28]; and ‘small-world networks’, which consist of nodes linked randomly and follow a Poisson or exponential distribution [29]. We found obvious difference in degree distribution between the 2 networks at all similarity thresholds (Fig. 4). At a similarity threshold of >75%, the clustering coefficient c (degree of linkage between nodes) of 5′ half was only 0.17 while 3′ half was 0.47, which means that 47% of all possible connection are used. The power-law-like distribution of the 5′ half network was enhanced as the similarity threshold increased, while the distribution of 3′ half network changed from Poisson-like (>75%) to irregular (>80–85%) then finally a power-law-like distribution at a sequence similarity of >88%. Meanwhile, the ratio of the cluster coefficient between 5′ and 3′ halves were constantly 1∶2.5–1∶4 showing that characteristics of the 2 tRNA domains significantly differ at all level of sequence threshold (75%–88%). We suggest that high commonality of the 3′ half sequences is one of the evidence of which 3′ half could have had a single origin. On the other hand, the scale-free distribution of the 5′ half represents a specific sequence characteristic within each sequence group, suggesting a non-monophyletic origin of the 5′ half sequences. These different sequence characteristics of the 5′ and 3′ tRNA halves further support the idea that ancient archaeal tRNA emerged from a specific combination of 5′ and 3′ halves.

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