Sipunculans (peanut worms or star worms) form a minor phylum of nonsegmented coelomate worms with bilaterally symmetrical bodies that are divisible into a trunk and a retractable introvert. In spite of low species diversity (about 150 species), sipunculans are found from tropical to Antarctic oceans [1
]. The fossil records for sipunculans are generally rare but three species from the Lower Cambrian Maotianshan Shale were reported by Huang et al
. (2004), suggesting that the most typical features of extant sipunculans have undergone only minor changes over the past 520 million years [3
]. Although the group was first documented in 1555, their phylogenetic relations are controversial [1
]. 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
]. Quatrefages (1847) proposed the name Gephyrea or "bridge group" for sipunculans, echiurans and priapulids, assuming that they represented a connection between annelids and echinoderms [8
]. Hyman (1959) suggested the disposal of Gephyre on the grounds that it was simply an easy way of grouping organisms of uncertain phylogenetic affinities. Furthermore, she suggested the elevation of sipunculans to phylum status (under the name Sipunculida) [5
]. Later on, Stephen (1965) proposed the name Sipuncula for the phylum [9
], a term which has been widely adopted.
Scheltema (1993) maintained the presence of a molluscan-cross during cleavage as an indication to place Sipuncula as the sister taxon to the Mollusca [10
]. However, cell lineage studies have shown that the concept of the molluscan-cross vs. the annelidan-cross is oversimplified and of limited phylogenetic significance [11
]. Due to superficial body plan similarity, sipunculans and echiurans are often grouped together [12
]. But prominent differences including anal position and proboscis form suggest that the similar body plans are a result of convergence due to parallel burrowing lifestyles, rather than common ancestry. Recently, the Echiura has been considered a derived polychaete group that may have lost segmentation [13
], leading to a more confused placement of sipunculans.
Previous cladistic analyses based on morphological and limited molecular data have rendered a great variety of hypotheses relating Sipuncula, including sister group to Echiura [15
], sister group to Annelida [16
], sister group to Mollusca [10
], sister group to Echiura + Annelida [17
], sister group to Mollusca + Annelida [18
], and sister group to an unresolved clade containing Mollusca, Annelida and the Panarthropoda [19
], or within Annelida [4
]. In summary, little agreement is reached with regards to the exact position of Sipuncula within the protostomes.
With a few remarkable exceptions, animal mitochondrial DNAs (mtDNAs) are circular molecules, 14–20 kb in size, containing 37 genes: 13 for proteins of electron transport (cox1
), 2 for ribosomal RNAs (srRNA
), and 22 for transfer RNAs. Over the past decades, inference of a deeper phylogenetic relationship of Metazoa with complete mitochondrial genome sequences has gained popularity [20
]. This resulted from many advantages offered over other molecular markers for phylogenetic analysis, such as (a) ease of isolation and assaying; (b) simple genetic structure lacking complicated features such as repetitive DNA, transposable elements, pseudogenes, and introns; and (c) effectively single copy, comparison of paralogous genes is generally not a concern [21
]. In addition, mitochondrial genome provides a systematic view and measurement of evolutionary history of an organism which is synchronized with the nuclear genome of the host [23
]. More importantly, compared to individual genes, mitochondrial genomes can provide sets of genome-level characteristics, such as the relative rearrangements of gene orders, which can be powerful for phylogenetic analysis [24
More than one thousand complete mitochondrial genome sequences http://www.ncbi.nlm.nih.gov/genomes/ORGANELLES/mztax_short.html
have been reported to date. The taxonomic sampling, however, is highly biased toward vertebrates and arthropods (both groups account for ~86% of sequenced mt genomes), with no complete mt genome in many minor phyla. Minor phyla are generally considered to be of little consequence usually with uncertain affinity in mainstream animal evolution theories because they are not well represented in present macrofauna. However, if we use the questionable definition of a phylum as a taxon with a distinctly unique body plan and leave aside the requirement of monophyly, then minor phyla represent the majority of nature's experimentation with animal body plans [26
In this paper, we described the gene content, organization and codon usage of the first complete mitochondrial genome in the phylum Sipuncula, Phascolosoma esculenta. We analyzed the phylogentic relationship of Sipuncula with mitochondrial genomes from Annelida, Echiura, Pogonophora, Myzostomida, Mollusca and some other protostomes. The result provides further evidence on phylogenomic scale to a close relationship of Myzostomida, Sipuncula and Annelida (including echiurans and pogonophorans).