Comparative genomics of large mitochondria in placozoans.

Ana Y Signorovitch,Stephen L Dellaporta,Leo W Buss

doi:10.1371/journal.pgen.0030013

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.

Highlights

Comparative mitochondrial genomics is becoming a powerful approach to resolving phylogenetic relationships among distantly related taxa (e.g., [1,2,3,4,5,6,7], and reviewed in [8,9])
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
The increased size of the placozoan mitochondrial genome is due to the presence of additional genes, introns, and long noncoding regions

Summary

Introduction

Comparative mitochondrial genomics is becoming a powerful approach to resolving phylogenetic relationships among distantly related taxa (e.g., [1,2,3,4,5,6,7], and reviewed in [8,9]). Sequencing of the entire Trichoplax adhaerens (phylum Placozoa) mitochondrial genome [6] made possible phylogenetic comparisons using all shared mitochondrial coding sequences (12 respiratory chain genes in all) across three lower metazoan phyla—Cnidaria, Placozoa, and Porifera—and two outgroup species, the choanoflagellate Monosiga brevicollis and the chytrid fungus Monoblepharella. This revised phylogeny provides support for the placement of the lineage leading to the placozoan Trichoplax as a basal animal phylum and raises the possibility that the ancestral animal mitochondrial genome could have been a large molecule akin to that of Trichoplax, instead of a compact molecule similar to that of all other animals. Most animal mitochondrial genomes are small, 15- to 20-kb, circular molecules encoding the typical respiratory chain genes (ATP synthase: atp and atp, apocytochrome b: cob, cytochrome oxidase: cox, cox, and cox, and reduced nicotinamide adenine dinucleotide ubiquinone oxireductase: nad, and nad4L), 22 tRNA genes, and two rRNA genes

Methods

Results

Discussion

Conclusion