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

  • ️Thu Jan 01 2015

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

Fumihiko Takeuchi et al. PLoS One. 2015.

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.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. 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.

Fig 2
Fig 2. The phylogenetic tree of nuclear-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. Support values are denoted also for the cnidarian clade. Image of T. adhaerens taken from [18], and others from the public domain.

Fig 3
Fig 3. 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.

Fig 4
Fig 4. The relative rates of nonsynonymous and synonymous substitutions in mitochondrial-encoded protein genes, compared among the genus Kudoa and other cnidarian classes.
Fig 5
Fig 5. Mitochondrial aerobic respiration observed in K. septempunctata myxospores.

(A) Confocal microscope images. Mitochondria are stained with Rhodamine 123 (red), and nuclei are stained with Hoechst 33258 (blue). (B) Bright field images. (C) Schematic representation of the myxospores. Polar capsules (PC) are arranged in a garlic shape within a myxospore. Within the sporoplasm, Rhodamine 123 accumulated beside the PCs, which indicates the negative electric potential in the mitochondrial membrane and suggests aerobic respiration. The myxospore in the top panel appears in transverse section, and the myxospore in the lower half of the bottom panel appears in radial section. Images of other sections are shown in S4 Fig.

Fig 6
Fig 6. Transmission electron microscopy of mitochondria in sporoplasm released from K. septempunctata myxospores.

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This work was supported by the Ministry of Health, Labor, and Welfare (H23-Shokuhin-Ippan-007) and the Ministry of Education, Culture, Sports, Science and Technology of Japan (KAKENHI 23117005, 15H05606, 15H14591). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.