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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.


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Transmission electron microscopy of mitochondria in sporoplasm released from K. septempunctata myxospores.
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pone.0132030.g006: Transmission electron microscopy of mitochondria in sporoplasm released from K. septempunctata myxospores.

Mentions: To examine if oxidative phosphorylation is maintained under the extremely divergent mitochondrial genome, we analyzed the transcriptome, metabolism and structure of mitochondria in K. septempunctata. We used K. septempunctata myxospores, which could be purified fresh from an aquaculture-raised flounder [3]. In the transcriptome, all genes of the citrate cycle and around half of the genes of each complex for oxidative phosphorylation were expressed (S1 Table). Additionally, we observed in vivo the aerobic respiration in K. septempunctata. In typical mitochondria, the first four complexes of oxidative phosphorylation pump protons out of the mitochondrial inner membrane, and the last complex uses the proton gradient to synthesize ATP. We stained K. septempunctata myxospores with Rhodamine 123, which detects proton gradients in the mitochondria. Rhodamine 123 accumulated next to the polar capsules of the myxospores, suggesting that the mitochondria therein were performing aerobic respiration (Fig 5, S4 Fig). Furthermore, by using transmission electron microscopy (Fig 6), we observed the tubular cristae structure in the mitochondria, as in other myxozoans [4]. The diameter of a mitochondrion was 1 μm in both the confocal and electron microscopy images. The transcriptome and microscopy data suggest active aerobic respiration in K. septempunctata mitochondria.


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)

Transmission electron microscopy of mitochondria in sporoplasm released from K. septempunctata myxospores.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0132030.g006: Transmission electron microscopy of mitochondria in sporoplasm released from K. septempunctata myxospores.
Mentions: To examine if oxidative phosphorylation is maintained under the extremely divergent mitochondrial genome, we analyzed the transcriptome, metabolism and structure of mitochondria in K. septempunctata. We used K. septempunctata myxospores, which could be purified fresh from an aquaculture-raised flounder [3]. In the transcriptome, all genes of the citrate cycle and around half of the genes of each complex for oxidative phosphorylation were expressed (S1 Table). Additionally, we observed in vivo the aerobic respiration in K. septempunctata. In typical mitochondria, the first four complexes of oxidative phosphorylation pump protons out of the mitochondrial inner membrane, and the last complex uses the proton gradient to synthesize ATP. We stained K. septempunctata myxospores with Rhodamine 123, which detects proton gradients in the mitochondria. Rhodamine 123 accumulated next to the polar capsules of the myxospores, suggesting that the mitochondria therein were performing aerobic respiration (Fig 5, S4 Fig). Furthermore, by using transmission electron microscopy (Fig 6), we observed the tubular cristae structure in the mitochondria, as in other myxozoans [4]. The diameter of a mitochondrion was 1 μm in both the confocal and electron microscopy images. The transcriptome and microscopy data suggest active aerobic respiration in K. septempunctata mitochondria.

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