The mitochondrial genomes of the acoelomorph worms Paratomella rubra, Isodiametra pulchra and Archaphanostoma ylvae

Helen E Robertson,Bernhard Egger,Maximilian J Telford,Philipp H Schiffer,François Lapraz

doi:10.1038/s41598-017-01608-4

Abstract

Acoels are small, ubiquitous - but understudied - marine worms with a very simple body plan. Their internal phylogeny is still not fully resolved, and the position of their proposed phylum Xenacoelomorpha remains debated. Here we describe mitochondrial genome sequences from the acoels Paratomella rubra and Isodiametra pulchra, and the complete mitochondrial genome of the acoel Archaphanostoma ylvae. The P. rubra and A. ylvae sequences are typical for metazoans in size and gene content. The larger I. pulchra mitochondrial genome contains both ribosomal genes, 21 tRNAs, but only 11 protein-coding genes. We find evidence suggesting a duplicated sequence in the I. pulchra mitochondrial genome. The P. rubra, I. pulchra and A. ylvae mitochondria have a unique genome organisation in comparison to other metazoan mitochondrial genomes. We found a large degree of protein-coding gene and tRNA overlap with little non-coding sequence in the compact P. rubra genome. Conversely, the A. ylvae and I. pulchra genomes have many long non-coding sequences between genes, likely driving genome size expansion in the latter. Phylogenetic trees inferred from mitochondrial genes retrieve Xenacoelomorpha as an early branching taxon in the deuterostomes. Sequence divergence analysis between P. rubra sampled in England and Spain indicates cryptic diversity.

Highlights

We describe the mitochondrial genomes from three species of acoel: Paratomella rubra, Isodiametra pulchra and Archaphanostoma ylvae
The 14.9 kb sequence of the P. rubra mitochondrial genome determined in our analysis contains the full complement of 37 genes typical of metazoan mitochondrial DNA
Numerous lab-based and computational efforts to close the circular mitochondrial genome were unsuccessful, but the complete gene complement and length of our final sequence indicates that this fragment covers the majority of the P. rubra complete mitochondrial genome

Summary

Introduction

Soft-bodied, unsegmented, marine animals lacking a gut epithelium, coelomic cavity, and anus Instead, they typically possess a ventral mouth opening, and a simple syncytial digestive system[1]. The first molecular systematic studies on these animals using small subunit (SSU) ribosomal RNA gene sequences revealed that the Acoelomorpha are a distinct lineage, quite separate from the main clade of the Platyhelminthes (Rhabditophora and Catenulida)[2,3,4] Instead, these initial molecular studies supported a position of the Acoelomorpha diverging prior to the protostome/deuterostome common ancestor. Metazoan mitochondrial DNA (mtDNA) is a closed-circular molecule typically comprising 37 genes which are, for the most part, invariant across the Metazoa[10] These include the two rRNAs of the mitochondrial ribosome, 22 tRNAs necessary for translation, and 13 protein-coding genes for the enzymes of oxidative phosphorylation. These include the two rRNAs of the mitochondrial ribosome, 22 tRNAs necessary for translation, and 13 protein-coding genes for the enzymes of oxidative phosphorylation. atp[8] is the only gene known to have been commonly lost from this complement, and this has been observed

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Conclusion