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Structure and variation of the mitochondrial genome of fishes

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ABSTRACT

Background: The mitochondrial (mt) genome has been used as an effective tool for phylogenetic and population genetic analyses in vertebrates. However, the structure and variability of the vertebrate mt genome are not well understood. A potential strategy for improving our understanding is to conduct a comprehensive comparative study of large mt genome data. The aim of this study was to characterize the structure and variability of the fish mt genome through comparative analysis of large datasets.

Results: An analysis of the secondary structure of proteins for 250 fish species (248 ray-finned and 2 cartilaginous fishes) illustrated that cytochrome c oxidase subunits (COI, COII, and COIII) and a cytochrome bc1 complex subunit (Cyt b) had substantial amino acid conservation. Among the four proteins, COI was the most conserved, as more than half of all amino acid sites were invariable among the 250 species. Our models identified 43 and 58 stems within 12S rRNA and 16S rRNA, respectively, with larger numbers than proposed previously for vertebrates. The models also identified 149 and 319 invariable sites in 12S rRNA and 16S rRNA, respectively, in all fishes. In particular, the present result verified that a region corresponding to the peptidyl transferase center in prokaryotic 23S rRNA, which is homologous to mt 16S rRNA, is also conserved in fish mt 16S rRNA. Concerning the gene order, we found 35 variations (in 32 families) that deviated from the common gene order in vertebrates. These gene rearrangements were mostly observed in the area spanning the ND5 gene to the control region as well as two tRNA gene cluster regions (IQM and WANCY regions). Although many of such gene rearrangements were unique to a specific taxon, some were shared polyphyletically between distantly related species.

Conclusions: Through a large-scale comparative analysis of 250 fish species mt genomes, we elucidated various structural aspects of the fish mt genome and the encoded genes. The present results will be important for understanding functions of the mt genome and developing programs for nucleotide sequence analysis. This study demonstrated the significance of extensive comparisons for understanding the structure of the mt genome.

Electronic supplementary material: The online version of this article (doi:10.1186/s12864-016-3054-y) contains supplementary material, which is available to authorized users.

No MeSH data available.


Base frequencies (%) of the mitochondrial transcription termination factor binding site in the tRNA-Leu (UUR) gene in the mt genomes of 250 fishes (see Additional file 8 for detailed information)
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Fig5: Base frequencies (%) of the mitochondrial transcription termination factor binding site in the tRNA-Leu (UUR) gene in the mt genomes of 250 fishes (see Additional file 8 for detailed information)

Mentions: To examine the presence or absence of the mt transcription termination factor (mTERF) binding site reported for the mammalian mt genome, we compared the fish mt tRNA-Leu (UUR), which contains the target binding site for mTERF [58–60]. This site is involved in the regulation of the level of transcription from the two rRNA genes and the remaining downstream genes coded on the H-strand [61]. Christianson and Clayton [58] and Kruse et al. [59] reported a tridecamer sequence (5’-TGGCAGAGCCCGG-3’) in the tRNA-Leu (UUR) gene as a key sequence of the mTERF binding site in the human mt genome [58, 59]. As a result of the present comparative analysis, the fish tRNA-Leu (UUR) gene also had this tridecamer motif in the same region corresponding to a part of the D arm as found in the human mt genome (Fig. 5 and Additional file 8: Table S7). The sequence of the motif in fishes was nearly identical to the human tridecamer sequence. The predominant base in all 13 nucleotide sites was completely identical to that in humans, and in particular, four bases were completely invariable in all 250 fishes and in humans (Fig. 5: positions 3–5 and 7). This conservation implies that this region also functions as the mTERF binding site in the fish mt genome.Fig. 5


Structure and variation of the mitochondrial genome of fishes
Base frequencies (%) of the mitochondrial transcription termination factor binding site in the tRNA-Leu (UUR) gene in the mt genomes of 250 fishes (see Additional file 8 for detailed information)
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC5015259&req=5

Fig5: Base frequencies (%) of the mitochondrial transcription termination factor binding site in the tRNA-Leu (UUR) gene in the mt genomes of 250 fishes (see Additional file 8 for detailed information)
Mentions: To examine the presence or absence of the mt transcription termination factor (mTERF) binding site reported for the mammalian mt genome, we compared the fish mt tRNA-Leu (UUR), which contains the target binding site for mTERF [58–60]. This site is involved in the regulation of the level of transcription from the two rRNA genes and the remaining downstream genes coded on the H-strand [61]. Christianson and Clayton [58] and Kruse et al. [59] reported a tridecamer sequence (5’-TGGCAGAGCCCGG-3’) in the tRNA-Leu (UUR) gene as a key sequence of the mTERF binding site in the human mt genome [58, 59]. As a result of the present comparative analysis, the fish tRNA-Leu (UUR) gene also had this tridecamer motif in the same region corresponding to a part of the D arm as found in the human mt genome (Fig. 5 and Additional file 8: Table S7). The sequence of the motif in fishes was nearly identical to the human tridecamer sequence. The predominant base in all 13 nucleotide sites was completely identical to that in humans, and in particular, four bases were completely invariable in all 250 fishes and in humans (Fig. 5: positions 3–5 and 7). This conservation implies that this region also functions as the mTERF binding site in the fish mt genome.Fig. 5

View Article: PubMed Central - PubMed

ABSTRACT

Background: The mitochondrial (mt) genome has been used as an effective tool for phylogenetic and population genetic analyses in vertebrates. However, the structure and variability of the vertebrate mt genome are not well understood. A potential strategy for improving our understanding is to conduct a comprehensive comparative study of large mt genome data. The aim of this study was to characterize the structure and variability of the fish mt genome through comparative analysis of large datasets.

Results: An analysis of the secondary structure of proteins for 250 fish species (248 ray-finned and 2 cartilaginous fishes) illustrated that cytochrome c oxidase subunits (COI, COII, and COIII) and a cytochrome bc1 complex subunit (Cyt b) had substantial amino acid conservation. Among the four proteins, COI was the most conserved, as more than half of all amino acid sites were invariable among the 250 species. Our models identified 43 and 58 stems within 12S rRNA and 16S rRNA, respectively, with larger numbers than proposed previously for vertebrates. The models also identified 149 and 319 invariable sites in 12S rRNA and 16S rRNA, respectively, in all fishes. In particular, the present result verified that a region corresponding to the peptidyl transferase center in prokaryotic 23S rRNA, which is homologous to mt 16S rRNA, is also conserved in fish mt 16S rRNA. Concerning the gene order, we found 35 variations (in 32 families) that deviated from the common gene order in vertebrates. These gene rearrangements were mostly observed in the area spanning the ND5 gene to the control region as well as two tRNA gene cluster regions (IQM and WANCY regions). Although many of such gene rearrangements were unique to a specific taxon, some were shared polyphyletically between distantly related species.

Conclusions: Through a large-scale comparative analysis of 250 fish species mt genomes, we elucidated various structural aspects of the fish mt genome and the encoded genes. The present results will be important for understanding functions of the mt genome and developing programs for nucleotide sequence analysis. This study demonstrated the significance of extensive comparisons for understanding the structure of the mt genome.

Electronic supplementary material: The online version of this article (doi:10.1186/s12864-016-3054-y) contains supplementary material, which is available to authorized users.

No MeSH data available.