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The Mitochondrial Genomes of a Myxozoan Genus Kudoa Are Extremely Divergent in Metazoa.

Takeuchi F, Sekizuka T, Ogasawara Y, Yokoyama H, Kamikawa R, Inagaki Y, Nozaki T, Sugita-Konishi Y, Ohnishi T, Kuroda M - PLoS ONE (2015)

Bottom Line: To further elucidate the evolution of Myxozoa, we sequenced the mitochondrial genomes of the myxozoan species Kudoa septempunctata, K. hexapunctata and K. iwatai and compared them with those of other metazoans.As possible causes, we attributed the divergence to the population genetic characteristics shared between the two most divergent clades, Ctenophora and Myxozoa, and to the parasitic lifestyle of Myxozoa.The fast-evolving, functional mitochondria of the genus Kudoa expanded our understanding of metazoan mitochondrial evolution.

View Article: PubMed Central - PubMed

Affiliation: Pathogen Genomics Center, National Institute of Infectious Diseases, Shinjuku-ku, Tokyo, Japan.

ABSTRACT
The Myxozoa are oligo-cellular parasites with alternate hosts--fish and annelid worms--and some myxozoan species harm farmed fish. The phylum Myxozoa, comprising 2,100 species, was difficult to position in the tree of life, due to its fast evolutionary rate. Recent phylogenomic studies utilizing an extensive number of nuclear-encoded genes have confirmed that Myxozoans belong to Cnidaria. Nevertheless, the evolution of parasitism and extreme body simplification in Myxozoa is not well understood, and no myxozoan mitochondrial DNA sequence has been reported to date. To further elucidate the evolution of Myxozoa, we sequenced the mitochondrial genomes of the myxozoan species Kudoa septempunctata, K. hexapunctata and K. iwatai and compared them with those of other metazoans. The Kudoa mitochondrial genomes code for ribosomal RNAs, transfer RNAs, eight proteins for oxidative phosphorylation and three proteins of unknown function, and they are among the metazoan mitochondrial genomes coding the fewest proteins. The mitochondrial-encoded proteins were extremely divergent, exhibiting the fastest evolutionary rate in Metazoa. Nevertheless, the dN/dS ratios of the protein genes in genus Kudoa were approximately 0.1 and similar to other cnidarians, indicating that the genes are under negative selection. Despite the divergent genetic content, active oxidative phosphorylation was indicated by the transcriptome, metabolism and structure of mitochondria in K. septempunctata. As possible causes, we attributed the divergence to the population genetic characteristics shared between the two most divergent clades, Ctenophora and Myxozoa, and to the parasitic lifestyle of Myxozoa. The fast-evolving, functional mitochondria of the genus Kudoa expanded our understanding of metazoan mitochondrial evolution.

No MeSH data available.


Related in: MedlinePlus

Mitochondrial genome maps of Kudoa species.Outer circle: protein-coding genes are represented by blue arrows, rRNAs by gray arrows and tRNAs by green arrowheads. Middle circle: plot of AT skew with the positive value towards the outside. Inner circle: plot of GC-content with higher %GC towards the outside.
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pone.0132030.g001: Mitochondrial genome maps of Kudoa species.Outer circle: protein-coding genes are represented by blue arrows, rRNAs by gray arrows and tRNAs by green arrowheads. Middle circle: plot of AT skew with the positive value towards the outside. Inner circle: plot of GC-content with higher %GC towards the outside.

Mentions: We sequenced the mitochondrial DNA of Kudoa species using Illumina next-generation sequencers and confirmed the sequences with PCR experiments and PacBio long reads. The mitochondrial genomes were circular and contained approximately 15 to 19 kilobase pairs with GC-content 31% for K. iwatai and 42–44% for the others (Fig 1). By Southern blotting, we verified that the DNA sequence was not derived from nuclear chromosomes or from fish mitochondria (S1 Fig). The circular nature of mitochondrial DNA was confirmed by PCR experiments and by mapping PacBio long reads (S2 Fig). We also performed RNA-seq using total RNA and mapped the reads to the mitochondrial genome. The large- and small-subunit mitochondrial rRNA genes were clearly distinguishable by their abundant expression (S3 Fig). A few candidate transfer RNA (tRNA) genes were detected. Eight typical mitochondrial-encoded protein genes existed: cytochrome c oxidase subunits I, II (cox1–2), cytochrome b (cob), NADH dehydrogenase subunits 1, 3, 4L, 5–6 (nad1, nad3, nad4L, nad5–6). The genes were common in the Kudoa species, except for nad4L, which was undetected in K. iwatai. In addition, there were three genes with unknown function conserved in Kudoa species (orf1–3) and one unique to K. septempunctata isolate 201204 (orf4). The largest one, orf3, coded a membrane protein with around seven transmembrane regions. As is visible in the AT skew plot, adenine was less abundant than thymine on the strand coding the proteins. In all genomes, the genes were condensed in one half, and the remaining half (6–10 kb) coded almost no genes (only a few candidate tRNA genes in some isolates) and was not conserved among the Kudoa species.


The Mitochondrial Genomes of a Myxozoan Genus Kudoa Are Extremely Divergent in Metazoa.

Takeuchi F, Sekizuka T, Ogasawara Y, Yokoyama H, Kamikawa R, Inagaki Y, Nozaki T, Sugita-Konishi Y, Ohnishi T, Kuroda M - PLoS ONE (2015)

Mitochondrial genome maps of Kudoa species.Outer circle: protein-coding genes are represented by blue arrows, rRNAs by gray arrows and tRNAs by green arrowheads. Middle circle: plot of AT skew with the positive value towards the outside. Inner circle: plot of GC-content with higher %GC towards the outside.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4492933&req=5

pone.0132030.g001: Mitochondrial genome maps of Kudoa species.Outer circle: protein-coding genes are represented by blue arrows, rRNAs by gray arrows and tRNAs by green arrowheads. Middle circle: plot of AT skew with the positive value towards the outside. Inner circle: plot of GC-content with higher %GC towards the outside.
Mentions: We sequenced the mitochondrial DNA of Kudoa species using Illumina next-generation sequencers and confirmed the sequences with PCR experiments and PacBio long reads. The mitochondrial genomes were circular and contained approximately 15 to 19 kilobase pairs with GC-content 31% for K. iwatai and 42–44% for the others (Fig 1). By Southern blotting, we verified that the DNA sequence was not derived from nuclear chromosomes or from fish mitochondria (S1 Fig). The circular nature of mitochondrial DNA was confirmed by PCR experiments and by mapping PacBio long reads (S2 Fig). We also performed RNA-seq using total RNA and mapped the reads to the mitochondrial genome. The large- and small-subunit mitochondrial rRNA genes were clearly distinguishable by their abundant expression (S3 Fig). A few candidate transfer RNA (tRNA) genes were detected. Eight typical mitochondrial-encoded protein genes existed: cytochrome c oxidase subunits I, II (cox1–2), cytochrome b (cob), NADH dehydrogenase subunits 1, 3, 4L, 5–6 (nad1, nad3, nad4L, nad5–6). The genes were common in the Kudoa species, except for nad4L, which was undetected in K. iwatai. In addition, there were three genes with unknown function conserved in Kudoa species (orf1–3) and one unique to K. septempunctata isolate 201204 (orf4). The largest one, orf3, coded a membrane protein with around seven transmembrane regions. As is visible in the AT skew plot, adenine was less abundant than thymine on the strand coding the proteins. In all genomes, the genes were condensed in one half, and the remaining half (6–10 kb) coded almost no genes (only a few candidate tRNA genes in some isolates) and was not conserved among the Kudoa species.

Bottom Line: To further elucidate the evolution of Myxozoa, we sequenced the mitochondrial genomes of the myxozoan species Kudoa septempunctata, K. hexapunctata and K. iwatai and compared them with those of other metazoans.As possible causes, we attributed the divergence to the population genetic characteristics shared between the two most divergent clades, Ctenophora and Myxozoa, and to the parasitic lifestyle of Myxozoa.The fast-evolving, functional mitochondria of the genus Kudoa expanded our understanding of metazoan mitochondrial evolution.

View Article: PubMed Central - PubMed

Affiliation: Pathogen Genomics Center, National Institute of Infectious Diseases, Shinjuku-ku, Tokyo, Japan.

ABSTRACT
The Myxozoa are oligo-cellular parasites with alternate hosts--fish and annelid worms--and some myxozoan species harm farmed fish. The phylum Myxozoa, comprising 2,100 species, was difficult to position in the tree of life, due to its fast evolutionary rate. Recent phylogenomic studies utilizing an extensive number of nuclear-encoded genes have confirmed that Myxozoans belong to Cnidaria. Nevertheless, the evolution of parasitism and extreme body simplification in Myxozoa is not well understood, and no myxozoan mitochondrial DNA sequence has been reported to date. To further elucidate the evolution of Myxozoa, we sequenced the mitochondrial genomes of the myxozoan species Kudoa septempunctata, K. hexapunctata and K. iwatai and compared them with those of other metazoans. The Kudoa mitochondrial genomes code for ribosomal RNAs, transfer RNAs, eight proteins for oxidative phosphorylation and three proteins of unknown function, and they are among the metazoan mitochondrial genomes coding the fewest proteins. The mitochondrial-encoded proteins were extremely divergent, exhibiting the fastest evolutionary rate in Metazoa. Nevertheless, the dN/dS ratios of the protein genes in genus Kudoa were approximately 0.1 and similar to other cnidarians, indicating that the genes are under negative selection. Despite the divergent genetic content, active oxidative phosphorylation was indicated by the transcriptome, metabolism and structure of mitochondria in K. septempunctata. As possible causes, we attributed the divergence to the population genetic characteristics shared between the two most divergent clades, Ctenophora and Myxozoa, and to the parasitic lifestyle of Myxozoa. The fast-evolving, functional mitochondria of the genus Kudoa expanded our understanding of metazoan mitochondrial evolution.

No MeSH data available.


Related in: MedlinePlus