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

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.

The joint evolution of the Myxozoa and their alternate hosts: A cnidarian recipe for success and vast biodiversity

“…Parasitic taxa are likely to have a faster rate of molecular evolution in order to win the “arms race” against their hosts (e.g., Bromham, Cowman, & Lanfear, ; Paterson et al., ). The rate heterogeneity across genes within the Myxozoa can be as high as that between myxozoans and other organisms (Hartigan et al., ; this study), and mitochondrial gene order and organization is highly variable (Takeuchi et al., ; Yahalomi et al., ), indicating a considerably accelerated rate of molecular evolution, possibly the fastest known among eukaryotes. This may well be explained by the extraordinary level of radiation that occurred within this group (Castro, Austin, & Dowton, ; Eo & DeWoody, ).…”

Linear Mitochondrial genome in Anthozoa (Cnidaria): A case study in Ceriantharia

“…The linear mitochondrial genome characteristic among members of Medusozoa appears to be quite variable in Myxozoa. The mitochondrion of species in the myxozoan genus Kudoa are small, and the genes in them are organized into a single circular genome that is evolving more quickly than those in other Medusozoa (Takeuchi et al 2015). The order of genes reported for the mitochondrial genome of Kudoa does not correspond to those published for other Medusozoans (cf.…”

“…The order of genes reported for the mitochondrial genome of Kudoa does not correspond to those published for other Medusozoans (cf. Kayal et al 2015;Takeuchi et al 2015). In contrast, in the myxozoan Enteromyxum leei, the mitogenome is organized into eight circular chromosomes (Yahalomi et al 2017).…”

Animal Mitochondrial DNA as We Do Not Know It: mt-Genome Organization and Evolution in Nonbilaterian Lineages

“…In addition, Myxozoa, a large (∼1,300 species) group of oligo-cellular parasites of fish and annelids with previously unknown phylogenetic affinity, is now placed inside Cnidaria (Nesnidal et al 2013; Feng et al 2014; Foox and Siddall 2015; Takeuchi et al 2015). The relationships among nonbilaterian phyla and bilaterian animals remain contentious (Pisani et al 2015; Whelan et al 2015), but are largely irrelevant to the present study.…”