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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.


The phylogenetic tree of mitochondrial-encoded proteins.The trees were inferred using the maximum-likelihood method and bootstrapped 100 times. Branches with bootstrap support ≥80% are colored black, and those with support <80% are colored gray with the support value denoted.
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pone.0132030.g003: The phylogenetic tree of mitochondrial-encoded proteins.The trees were inferred using the maximum-likelihood method and bootstrapped 100 times. Branches with bootstrap support ≥80% are colored black, and those with support <80% are colored gray with the support value denoted.

Mentions: We next studied the phylogeny of mitochondrial-encoded and nuclear-encoded proteins. The phylogenetic tree of nuclear-encoded proteins (Fig 2) supported the previous phylogenomic studies [6,9,10] by suggesting the monophyly of the myxozoans, Kudoa and Buddenbrockia, and the position of myxozoans within Cnidaria with 100% bootstrap support. The evolutionary rate of myxozoans was faster than other metazoans, as visible from the longer branch. In the phylogenetic tree of mitochondrial-encoded proteins (Fig 3), the evolutionary rate was even faster for Kudoa and was faster than the previously known extreme case of ctenophores [13,14]. Because both Kudoa and Ctenophora have long branches, their branches were very likely falsely joined together with the long branches of Platyhelminthes (such as Schistosoma mansoni) due to long-branch attraction. In long-branch attraction, divergent species are known to be falsely grouped within a phylogenetic tree, while their branch lengths are unchanged [17]. There was no conclusive support on the deeper branches of the mitochondrial phylogenetic tree. To investigate if the fast mitochondrial evolutionary rate of Kudoa species could be due to positive selection or a lack of selective pressure (as in pseudogenes), we measured the relative rates of nonsynonymous and synonymous substitutions. The dN/dS ratios of mitochondrial-encoded protein genes in the genus Kudoa were approximately 0.1 and not remarkably higher than other cnidarians, suggesting that the genes are under negative selection to a similar degree in Kudoa and other cnidarian classes (Fig 4).


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)

The phylogenetic tree of mitochondrial-encoded proteins.The trees were inferred using the maximum-likelihood method and bootstrapped 100 times. Branches with bootstrap support ≥80% are colored black, and those with support <80% are colored gray with the support value denoted.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0132030.g003: The phylogenetic tree of mitochondrial-encoded proteins.The trees were inferred using the maximum-likelihood method and bootstrapped 100 times. Branches with bootstrap support ≥80% are colored black, and those with support <80% are colored gray with the support value denoted.
Mentions: We next studied the phylogeny of mitochondrial-encoded and nuclear-encoded proteins. The phylogenetic tree of nuclear-encoded proteins (Fig 2) supported the previous phylogenomic studies [6,9,10] by suggesting the monophyly of the myxozoans, Kudoa and Buddenbrockia, and the position of myxozoans within Cnidaria with 100% bootstrap support. The evolutionary rate of myxozoans was faster than other metazoans, as visible from the longer branch. In the phylogenetic tree of mitochondrial-encoded proteins (Fig 3), the evolutionary rate was even faster for Kudoa and was faster than the previously known extreme case of ctenophores [13,14]. Because both Kudoa and Ctenophora have long branches, their branches were very likely falsely joined together with the long branches of Platyhelminthes (such as Schistosoma mansoni) due to long-branch attraction. In long-branch attraction, divergent species are known to be falsely grouped within a phylogenetic tree, while their branch lengths are unchanged [17]. There was no conclusive support on the deeper branches of the mitochondrial phylogenetic tree. To investigate if the fast mitochondrial evolutionary rate of Kudoa species could be due to positive selection or a lack of selective pressure (as in pseudogenes), we measured the relative rates of nonsynonymous and synonymous substitutions. The dN/dS ratios of mitochondrial-encoded protein genes in the genus Kudoa were approximately 0.1 and not remarkably higher than other cnidarians, suggesting that the genes are under negative selection to a similar degree in Kudoa and other cnidarian classes (Fig 4).

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.