A close phylogenetic relationship between Sipuncula and Annelida evidenced from the complete mitochondrial genome sequence of Phascolosoma esculenta

Xin Shen,Fangqing Zhao,Xiaoyin Ma,Jianfeng Ren

doi:10.1186/1471-2164-10-136

Abstract

BackgroundThere are many advantages to the application of complete mitochondrial (mt) genomes in the accurate reconstruction of phylogenetic relationships in Metazoa. Although over one thousand metazoan genomes have been sequenced, the taxonomic sampling is highly biased, left with many phyla without a single representative of complete mitochondrial genome. Sipuncula (peanut worms or star worms) is a small taxon of worm-like marine organisms with an uncertain phylogenetic position. In this report, we present the mitochondrial genome sequence of Phascolosoma esculenta, the first complete mitochondrial genome of the phylum.ResultsThe mitochondrial genome of P.esculenta is 15,494 bp in length. The coding strand consists of 32.1% A, 21.5% C, 13.0% G, and 33.4% T bases (AT = 65.5%; AT skew = -0.019; GC skew = -0.248). It contains thirteen protein-coding genes (PCGs) with 3,709 codons in total, twenty-two transfer RNA genes, two ribosomal RNA genes and a non-coding AT-rich region (AT = 74.2%). All of the 37 identified genes are transcribed from the same DNA strand. Compared with the typical set of metazoan mt genomes, sipunculid lacks trnR but has an additional trnM. Maximum Likelihood and Bayesian analyses of the protein sequences show that Myzostomida, Sipuncula and Annelida (including echiurans and pogonophorans) form a monophyletic group, which supports a closer relationship between Sipuncula and Annelida than with Mollusca, Brachiopoda, and some other lophotrochozoan groups.ConclusionThis is the first report of a complete mitochondrial genome as a representative within the phylum Sipuncula. It shares many more similar features with the four known annelid and one echiuran mtDNAs. Firstly, sipunculans and annelids share quite similar gene order in the mitochondrial genome, with all 37 genes located on the same strand; secondly, phylogenetic analyses based on the concatenated protein sequences also strongly support the sipunculan + annelid clade (including echiurans and pogonophorans). Hence annelid "key-characters" including segmentation may be more labile than previously assumed.

Highlights

There are many advantages to the application of complete mitochondrial genomes in the accurate reconstruction of phylogenetic relationships in Metazoa
We described the gene content, organization and codon usage of the first complete mitochondrial genome in the phylum Sipuncula, Phascolosoma esculenta
Gene order All the mitochondrial genes of P.esculenta are transcribed from the same strand (Figure 1), as is the case for the four studied annelids (Orbinia latreillii [27], C.torquata [28], Platynereis dumerilii [29], and Lumbricus terrestris [20]), one echiuran Urechis caupo [30], and many other lophotrochozoan mitochondrial DNA (mtDNA) [31]

Summary

Introduction

There are many advantages to the application of complete mitochondrial (mt) genomes in the accurate reconstruction of phylogenetic relationships in Metazoa. In 1767 Linnaeus described Sipunculus nudus, placing it within the Vermes Intestina, a group containing truly "internal worms" and other bilateral invertebrates lacking lateral appendages [6]. These were later considered to be a derived group of annelids [7]. Hyman (1959) suggested the disposal of Gephyre on the grounds that it was an easy way of grouping organisms of uncertain phylogenetic affinities. She suggested the elevation of sipunculans to phylum status (under the name Sipunculida) [5]. Stephen (1965) proposed the name Sipuncula for the phylum [9], a term which has been widely adopted

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Conclusion