The mitochondrial genome structure of Xenoturbella bocki(phylum Xenoturbellida) is ancestral within the deuterostomes

Sarah J Bourlat,Omar Rota-Stabelli,Maximilian J Telford,Robert Lanfear

doi:10.1186/1471-2148-9-107

Sarah J Bourlat, Omar Rota-Stabelli + Show 2 more

Open Access

https://doi.org/10.1186/1471-2148-9-107

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Abstract

BackgroundMitochondrial genome comparisons contribute in multiple ways when inferring animal relationships. As well as primary sequence data, rare genomic changes such as gene order, shared gene boundaries and genetic code changes, which are unlikely to have arisen through convergent evolution, are useful tools in resolving deep phylogenies. Xenoturbella bocki is a morphologically simple benthic marine worm recently found to belong among the deuterostomes. Here we present analyses comparing the Xenoturbella bocki mitochondrial gene order, genetic code and control region to those of other metazoan groups.ResultsThe complete mitochondrial genome sequence of Xenoturbella bocki was determined. The gene order is most similar to that of the chordates and the hemichordates, indicating that this conserved mitochondrial gene order might be ancestral to the deuterostome clade. Using data from all phyla of deuterostomes, we infer the ancestral mitochondrial gene order for this clade. Using inversion and breakpoint analyses of metazoan mitochondrial genomes, we test conflicting hypotheses for the phylogenetic placement of Xenoturbella and find a closer affinity to the hemichordates than to other metazoan groups. Comparative analyses of the control region reveal similarities in the transcription initiation and termination sites and origin of replication of Xenoturbella with those of the vertebrates. Phylogenetic analyses of the mitochondrial sequence indicate a weakly supported placement as a basal deuterostome, a result that may be the effect of compositional bias.ConclusionThe mitochondrial genome of Xenoturbella bocki has a very conserved gene arrangement in the deuterostome group, strikingly similar to that of the hemichordates and the chordates, and thus to the ancestral deuterostome gene order. Similarity to the hemichordates in particular is suggested by inversion and breakpoint analysis. Finally, while phylogenetic analyses of the mitochondrial sequences support a basal deuterostome placement, support for this decreases with the use of more sophisticated models of sequence evolution.

Highlights

Mitochondrial genome comparisons contribute in multiple ways when inferring animal relationships
ATG is used as a start codon for all of the protein coding genes, except cox2, which starts with GTG. atp6, cox3, nd3 and nd4 end on TA and cox2 on T, while all other genes end on the usual TAA
Comparative analyses of the mitochondrial genome structure of Xenoturbella bocki with those of other deuterostomes and bilaterians have revealed a number of characteristics linking it to the deuterostome clade

Summary

Introduction

Mitochondrial genome comparisons contribute in multiple ways when inferring animal relationships. The primitive state for the mitochondrial genome probably resembled that found in the protozoan Reclinomonas americana, which has a 69,034 bp genome which still retains eubacterial features of genome organisation such as operons [2] During their evolutionary history, many mitochondrial genomes have been reduced in size, having lost many genes, some of which have been transferred to the nucleus. Within the Metazoa, mitochondrial genomes show surprising conservation of size and composition [3], almost invariably containing 13 protein coding genes, 2 ribosomal genes and 22 tRNAs, necessary for the transcription of the mitochondrially encoded genes The order of those genes on the mitochondrial genome differs widely among the metazoan phyla, but can show surprising conservation in organisation within specific metazoan clades, such as the Vertebrata [4] and the Ecdysozoa [5]. Breakpoint and maximum parsimony analyses have revealed phylogenetic signal derived from the mitochondrial gene order allowing inference of evolutionary relationships among the metazoan phyla, and support aspects of the new animal phylogeny (Lophotrochozoa/Ecdysozoa) [6]

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