Mitochondrial Genome Evolution of Placozoans: Gene Rearrangements and Repeat Expansions

Author:

Miyazawa Hideyuki12,Osigus Hans-Jürgen3,Rolfes Sarah3,Kamm Kai3,Schierwater Bernd3,Nakano Hiroaki2

Affiliation:

1. Center for Genome Informatics, Joint Support-Center for Data Science Research, Research Organization of Information and Systems, Mishima, Shizuoka, Japan

2. Shimoda Marine Research Center, University of Tsukuba, Shimoda, Shizuoka, Japan

3. Division of Molecular Evolution, Institute of Animal Ecology, University of Veterinary Medicine Hannover, Foundation, Germany

Abstract

Abstract Placozoans, nonbilaterian animals with the simplest known metazoan bauplan, are currently classified into 20 haplotypes belonging to three genera, Polyplacotoma, Trichoplax, and Hoilungia. The latter two comprise two and five clades, respectively. In Trichoplax and Hoilungia, previous studies on six haplotypes belonging to four different clades have shown that their mtDNAs are circular chromosomes of 32–43 kb in size, which encode 12 protein-coding genes, 24 tRNAs, and two rRNAs. These mitochondrial genomes (mitogenomes) also show unique features rarely seen in other metazoans, including open reading frames (ORFs) of unknown function, and group I and II introns. Here, we report seven new mitogenomes, covering the five previously described haplotypes H2, H17, H19, H9, and H11, as well as two new haplotypes, H23 (clade III) and H24 (clade VII). The overall gene content is shared between all placozoan mitochondrial genomes, but genome sizes, gene orders, and several exon–intron boundaries vary among clades. Phylogenomic analyses strongly support a tree topology different from previous 16S rRNA analyses, with clade VI as the sister group to all other Hoilungia clades. We found small inverted repeats in all 13 mitochondrial genomes of the Trichoplax and Hoilungia genera and evaluated their distribution patterns among haplotypes. Because Polyplacotoma mediterranea (H0), the sister to the remaining haplotypes, has a small mitochondrial genome with few small inverted repeats and ORFs, we hypothesized that the proliferation of inverted repeats and ORFs substantially contributed to the observed increase in the size and GC content of the Trichoplax and Hoilungia mitochondrial genomes.

Publisher

Oxford University Press (OUP)

Subject

Genetics,Ecology, Evolution, Behavior and Systematics

Reference51 articles.

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