Comparative genomics of large mitochondria in placozoans

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.

Figure 1. Linearized Scaled Maps of the Four Placozoan Mitochondrial Genomes

Each of the four heavy black lines represents the nucleotide sequence of a genome. Genes and RNAs are indicated by their names and color-coded rectangles. Genes transcribed in opposing directions are positioned to the right or left of the sequence line. Introns of cox1 and nad5 are denoted by thin black lines connecting each exon. The four mitochondrial genomes were divided into two groups based on their structural and phylogenetic similarity: BZ10101 and BZ49 (A) and Trichoplax and BZ2423 (B). Within each group, red and gray lines over the sequence indicate segmental translocations and insertions, respectively. The gray dashed lines across groups (A) and (B) indicate an inversion of the delineated region.

Figure 2. Phylogeny of the Metazoa

This phylogenetic tree is based on 2,553 amino acids from 12 concatenated respiratory chain genes (atp6, cob, cox1–3, nad1–6, and nad4L). Values above internal nodes represent Bayesian posterior probabilities, and those below represent bootstrap percentages under ML. The tree was rooted with the chytrid fungus Monoblepharella.