Mitochondrial Genomes of Kinorhyncha: trnM Duplication and New Gene Orders within Animals.

Olga V Popova,Vladimir V Aleoshin,Olga S Kedrova,Kirill V Mikhailov,Maria S Muntyan,Aleksey A Penin,Yuri V Panchin,Mikhail A Nikitin,Nikolai B Petrov,Maria D Logacheva,Bi-Song Yue

doi:10.1371/journal.pone.0165072

Abstract

Many features of mitochondrial genomes of animals, such as patterns of gene arrangement, nucleotide content and substitution rate variation are extensively used in evolutionary and phylogenetic studies. Nearly 6,000 mitochondrial genomes of animals have already been sequenced, covering the majority of animal phyla. One of the groups that escaped mitogenome sequencing is phylum Kinorhyncha—an isolated taxon of microscopic worm-like ecdysozoans. The kinorhynchs are thought to be one of the early-branching lineages of Ecdysozoa, and their mitochondrial genomes may be important for resolving evolutionary relations between major animal taxa. Here we present the results of sequencing and analysis of mitochondrial genomes from two members of Kinorhyncha, Echinoderes svetlanae (Cyclorhagida) and Pycnophyes kielensis (Allomalorhagida). Their mitochondrial genomes are circular molecules approximately 15 Kbp in size. The kinorhynch mitochondrial gene sequences are highly divergent, which precludes accurate phylogenetic inference. The mitogenomes of both species encode a typical metazoan complement of 37 genes, which are all positioned on the major strand, but the gene order is distinct and unique among Ecdysozoa or animals as a whole. We predict four types of start codons for protein-coding genes in E. svetlanae and five in P. kielensis with a consensus DTD in single letter code. The mitochondrial genomes of E. svetlanae and P. kielensis encode duplicated methionine tRNA genes that display compensatory nucleotide substitutions. Two distant species of Kinorhyncha demonstrate similar patterns of gene arrangements in their mitogenomes. Both genomes have duplicated methionine tRNA genes; the duplication predates the divergence of two species. The kinorhynchs share a few features pertaining to gene order that align them with Priapulida. Gene order analysis reveals that gene arrangement specific of Priapulida may be ancestral for Scalidophora, Ecdysozoa, and even Protostomia.

Highlights

Mitochondrial genomes provide a set of important tools for evolutionary studies of animals owing to their accessibility and higher evolutionary rate in comparison with the nuclear genomes
In addition to the gene sequence data, the mitochondrial genome displays other features that are applicable for evolutionary studies
The GC and AT skews characterize the asymmetry of nucleotide content between the two strands of mitochondrial DNA [40, 61]

Summary

Introduction

Mitochondrial genomes provide a set of important tools for evolutionary studies of animals owing to their accessibility and higher evolutionary rate in comparison with the nuclear genomes. It was suggested that changes in the mitochondrial gene order can be used as cladistic characters for studying relationships among higher-level taxa [3]. The gene order within blocks remains uniform in most species, while the blocks themselves experience transpositions The arrangements of these blocks allow to deduce putative ground patterns for some bilaterian taxa, including Ecdysozoa [15], Lophotrochozoa [16], and Deuterostomia [17]. The ground patterns for taxa with highly variable gene order (such as Nematoda or Chaetognatha) or for higher-level taxa (such as Bilateria or Metazoa) remains intractable. Within Ecdysozoa the mitochondrial gene order is generally more variable than in other taxa of the same rank, and it is potentially a valuable resource for phylogenetic information in the group [18,19,20]

Methods

Results

Conclusion