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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.


Representative stem-loop structures of the origin of L-strand replication in the fish mt genome. Red box represents a conserved sequence motif, which is necessary for in vitro replication of the L-strand in mammals. Numerals in front of the species name are the same as those in Additional file 1
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Fig9: Representative stem-loop structures of the origin of L-strand replication in the fish mt genome. Red box represents a conserved sequence motif, which is necessary for in vitro replication of the L-strand in mammals. Numerals in front of the species name are the same as those in Additional file 1

Mentions: OL was identified in 245 fishes, whereas it was not found in the remaining five fishes (Additional file 16: Figure S5). The obtained 245 OL sequences displayed considerable length variation, ranging from 22 to 87 nucleotides, but they exclusively had the potential to form a stable stem-loop structure (Table 6; Fig. 9). Stem and loop lengths ranged from 8 to 39 bp and from 3 to 23 nucleotides, respectively. The stem was moderately GC rich similarly as the RNA stems, whereas the loop was A rich similarly as the RNA loops (Table 2). The 5’-end (tRNA-Cys side) of the loop was T rich (Additional file 16: Figure S5). A conserved sequence motif (5’-GCCGG-3’) that was reported as necessary for in vitro replication of the L-strand in mammals [74, 75] was observed in nearly 70 % of species (Table 6).Table 6


Structure and variation of the mitochondrial genome of fishes
Representative stem-loop structures of the origin of L-strand replication in the fish mt genome. Red box represents a conserved sequence motif, which is necessary for in vitro replication of the L-strand in mammals. Numerals in front of the species name are the same as those in Additional file 1
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig9: Representative stem-loop structures of the origin of L-strand replication in the fish mt genome. Red box represents a conserved sequence motif, which is necessary for in vitro replication of the L-strand in mammals. Numerals in front of the species name are the same as those in Additional file 1
Mentions: OL was identified in 245 fishes, whereas it was not found in the remaining five fishes (Additional file 16: Figure S5). The obtained 245 OL sequences displayed considerable length variation, ranging from 22 to 87 nucleotides, but they exclusively had the potential to form a stable stem-loop structure (Table 6; Fig. 9). Stem and loop lengths ranged from 8 to 39 bp and from 3 to 23 nucleotides, respectively. The stem was moderately GC rich similarly as the RNA stems, whereas the loop was A rich similarly as the RNA loops (Table 2). The 5’-end (tRNA-Cys side) of the loop was T rich (Additional file 16: Figure S5). A conserved sequence motif (5’-GCCGG-3’) that was reported as necessary for in vitro replication of the L-strand in mammals [74, 75] was observed in nearly 70 % of species (Table 6).Table 6

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.