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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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Network analysis based on the sequence similarities of 5′ and 3′ tRNA halves.A total of 296 mature tRNA sequences from 7 archaeal species (Neq, Sso, Ape, Pae, Mka, Pfu, Mja) were artificially split into 5′ and 3′ halves at the anti-codon region. Each node (colored dot) represents a tRNA half, and its color indicates the charged amino acid's chemical properties (DE, mid-green; MNQ, light green; RKH, blue; FWY, purple; AGP, red; ILV, orange; CST, yellow; iMet, gray). Nodes are linked by a white line (edge) when the sequence similarity is above the threshold. (A) Network created by set of 5′ half sequences with thresholds of >70%, >75%, and >80%. The sequences are classified into 6 clusters (1–6) at a threshold of >80%. (B) Network created by set of 3′ half sequences with thresholds of >80%, >85%, and >88%. The sequences are classified into 9 clusters (A–I) at a threshold of >88%.
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pone-0001622-g003: Network analysis based on the sequence similarities of 5′ and 3′ tRNA halves.A total of 296 mature tRNA sequences from 7 archaeal species (Neq, Sso, Ape, Pae, Mka, Pfu, Mja) were artificially split into 5′ and 3′ halves at the anti-codon region. Each node (colored dot) represents a tRNA half, and its color indicates the charged amino acid's chemical properties (DE, mid-green; MNQ, light green; RKH, blue; FWY, purple; AGP, red; ILV, orange; CST, yellow; iMet, gray). Nodes are linked by a white line (edge) when the sequence similarity is above the threshold. (A) Network created by set of 5′ half sequences with thresholds of >70%, >75%, and >80%. The sequences are classified into 6 clusters (1–6) at a threshold of >80%. (B) Network created by set of 3′ half sequences with thresholds of >80%, >85%, and >88%. The sequences are classified into 9 clusters (A–I) at a threshold of >88%.

Mentions: As described in the previous section, comprehensive phylogenetic analysis of 1953 mature archaeal tRNA sequences revealed an evolutionary relationship between the three types of tRNAs. If split genes were the ancestral form of tRNA, can we explain the origin and evolution of modern tRNA sequences by the combination patterns of 5′ and 3′ tRNA halves? We attempted to corroborate this hypothesis by analyzing the evolutionary backgrounds of 5′ and 3′ halves. We selected 7 archaeal species, each from the closest taxon to the last archaeal common ancestor: 1 Nanoarchaeota (N. equitans, Neq), 3 Crenarchaeota (P. aerophilum, Pae; A. pernix, Ape; and S. solfataricus; Sso), and 3 Euryarchaeota (P. furiosus, Pfu; M. kandleri, Mka; and M. jannaschii, Mja). In total, 296 tRNA sequences were extracted and separated into the 5′ half (positions 1–33) and the 3′ half (positions 37–73) at the anticodon region (positions 34–36) to mimic split tRNA. We considered each tRNA half as a network node, and nodes were linked when sequence identity between the 2 tRNA halves was above certain threshold. Accordingly, we have constructed 2 different networks (5′ half network and 3′ half network) based on their sequence similarities. Previously, a network-based approach was used to explain 2 mechanisms of tRNA evolution: point mutation and complementary mutation [27]. Thus, concept of representing the sequence similarities among tRNA halves as a network provides comprehensive understanding of sequence characteristics and its diversity based on the global statistics. Figure. 3 shows the sequence similarity networks of 5′ and 3′ tRNA halves with thresholds of >70%, >75%, and >80% for 5′ tRNA halves (Fig. 3A), and >80%, >85%, and >88% for 3′ tRNA halves (Fig. 3B). A noticeable topological difference is apparent between the sequence similarity networks of the 5′ and 3′ halves. Sequence diversity of the 5′ half sequences appeared between sequence similarities of >70% and >75%, where the single large network started to localize into small clusters corresponding to specific amino acids. This feature was more prominent at a similarity of >80%, where 5′ halves clearly separated into 6 groups (1–6 in Fig. 3A). In contrast, all 3′ half sequences except tRNASer and tRNALeu (possessing long variable stem loops shown as yellow and orange nodes in Fig. 3B) gathered into 1 large group even at a sequence similarity of >80%. The 3′ half sequences were finally differentiated at a sequence similarity of >88% into 9 groups (A–I in Fig. 3B).


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)

Network analysis based on the sequence similarities of 5′ and 3′ tRNA halves.A total of 296 mature tRNA sequences from 7 archaeal species (Neq, Sso, Ape, Pae, Mka, Pfu, Mja) were artificially split into 5′ and 3′ halves at the anti-codon region. Each node (colored dot) represents a tRNA half, and its color indicates the charged amino acid's chemical properties (DE, mid-green; MNQ, light green; RKH, blue; FWY, purple; AGP, red; ILV, orange; CST, yellow; iMet, gray). Nodes are linked by a white line (edge) when the sequence similarity is above the threshold. (A) Network created by set of 5′ half sequences with thresholds of >70%, >75%, and >80%. The sequences are classified into 6 clusters (1–6) at a threshold of >80%. (B) Network created by set of 3′ half sequences with thresholds of >80%, >85%, and >88%. The sequences are classified into 9 clusters (A–I) at a threshold of >88%.
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Related In: Results  -  Collection

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pone-0001622-g003: Network analysis based on the sequence similarities of 5′ and 3′ tRNA halves.A total of 296 mature tRNA sequences from 7 archaeal species (Neq, Sso, Ape, Pae, Mka, Pfu, Mja) were artificially split into 5′ and 3′ halves at the anti-codon region. Each node (colored dot) represents a tRNA half, and its color indicates the charged amino acid's chemical properties (DE, mid-green; MNQ, light green; RKH, blue; FWY, purple; AGP, red; ILV, orange; CST, yellow; iMet, gray). Nodes are linked by a white line (edge) when the sequence similarity is above the threshold. (A) Network created by set of 5′ half sequences with thresholds of >70%, >75%, and >80%. The sequences are classified into 6 clusters (1–6) at a threshold of >80%. (B) Network created by set of 3′ half sequences with thresholds of >80%, >85%, and >88%. The sequences are classified into 9 clusters (A–I) at a threshold of >88%.
Mentions: As described in the previous section, comprehensive phylogenetic analysis of 1953 mature archaeal tRNA sequences revealed an evolutionary relationship between the three types of tRNAs. If split genes were the ancestral form of tRNA, can we explain the origin and evolution of modern tRNA sequences by the combination patterns of 5′ and 3′ tRNA halves? We attempted to corroborate this hypothesis by analyzing the evolutionary backgrounds of 5′ and 3′ halves. We selected 7 archaeal species, each from the closest taxon to the last archaeal common ancestor: 1 Nanoarchaeota (N. equitans, Neq), 3 Crenarchaeota (P. aerophilum, Pae; A. pernix, Ape; and S. solfataricus; Sso), and 3 Euryarchaeota (P. furiosus, Pfu; M. kandleri, Mka; and M. jannaschii, Mja). In total, 296 tRNA sequences were extracted and separated into the 5′ half (positions 1–33) and the 3′ half (positions 37–73) at the anticodon region (positions 34–36) to mimic split tRNA. We considered each tRNA half as a network node, and nodes were linked when sequence identity between the 2 tRNA halves was above certain threshold. Accordingly, we have constructed 2 different networks (5′ half network and 3′ half network) based on their sequence similarities. Previously, a network-based approach was used to explain 2 mechanisms of tRNA evolution: point mutation and complementary mutation [27]. Thus, concept of representing the sequence similarities among tRNA halves as a network provides comprehensive understanding of sequence characteristics and its diversity based on the global statistics. Figure. 3 shows the sequence similarity networks of 5′ and 3′ tRNA halves with thresholds of >70%, >75%, and >80% for 5′ tRNA halves (Fig. 3A), and >80%, >85%, and >88% for 3′ tRNA halves (Fig. 3B). A noticeable topological difference is apparent between the sequence similarity networks of the 5′ and 3′ halves. Sequence diversity of the 5′ half sequences appeared between sequence similarities of >70% and >75%, where the single large network started to localize into small clusters corresponding to specific amino acids. This feature was more prominent at a similarity of >80%, where 5′ halves clearly separated into 6 groups (1–6 in Fig. 3A). In contrast, all 3′ half sequences except tRNASer and tRNALeu (possessing long variable stem loops shown as yellow and orange nodes in Fig. 3B) gathered into 1 large group even at a sequence similarity of >80%. The 3′ half sequences were finally differentiated at a sequence similarity of >88% into 9 groups (A–I in Fig. 3B).

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