Comparative Genomics of Large Mitochondria in Placozoans

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Abstract
The first sequenced mitochondrial genome of a placozoan, Trichoplax adhaerens, challenged the conventional wisdom that a compact mitochondrial genome is a common feature among all animals. Three additional placozoan mitochondrial genomes representing highly divergent clades have been sequenced to determine whether the large Trichoplax mtDNA is a shared feature among members of the phylum Placozoa or a uniquely derived condition. All three mitochondrial genomes were found to be very large, 32- to 37-kb, circular molecules, having the typical 12 respiratory chain genes, 24 tRNAs, rnS, and rnL. They share with the Trichoplax mitochondrial genome the absence of atp8, atp9, and all ribosomal protein genes, the presence of several cox1 introns, and a large open reading frame containing an intron group I LAGLIDADG endonuclease domain. The differences in mtDNA size within Placozoa are due to variation in intergenic spacer regions and the presence or absence of long open reading frames of unknown function. Phylogenetic analyses of the 12 respiratory chain genes support the monophyly of Placozoa. The similarities in composition and structure between the three mitochondrial genomes reported here and that of Trichoplax's mtDNA suggest that their uncompacted state is a shared ancestral feature to other nonmetazoans while their gene content is a derived feature shared only among the Metazoa. Animals typically have much smaller mitochondrial genomes than do nonanimal single-celled organisms and fungi. Whereas animal mitochondrial genomes are characterized by a tightly packed collection of conserved genes and other functional elements, the larger nonanimal mitochondrial genomes generally contain noncoding regions, such as introns and additional genes not present among animals. It has thus been argued that drastic mitochondrial size reduction occurred deep in evolutionary history, before the emergence of animals. In this study, however, we show that the phylum Placozoa, arguably one of the most ancient animal groups, possesses mitochondrial genomes of intermediate size, smaller than the typical nonanimal genome yet much larger than the mitochondrial genome found in typical animals. As in nonanimals, the increased size of the placozoan mitochondrial genome is due to the presence of additional genes, introns, and long noncoding regions. Although other large animal mitochondrial genomes have been discovered, they have been isolated findings in particular species and none encompassed as large a taxonomic group as the level of phylum. Because large mitochondrial genomes are a shared feature among all placozoans and given this phylum's phylogenetic position in the animal tree, we conclude that, contrary to conventional wisdom, the ancestral animal mitochondria was likely a large, noncompacted molecule.