The phylogenetic position of Acoela as revealed by the complete mitochondrial genome of Symsagittifera roscoffensis

Abstract

Background: Acoels are simply organized unsegmented worms, lacking hindgut and anus. Several publications over recent years challenge the long-held view that acoels are early offshoots of the flatworms. Instead a basal position as sister group to all other bilaterian animals was suggested, mainly based on molecular evidence. This led to the view that features of acoels might reflect those of the last common ancestor of Bilateria, and resulted in several evo-devo studies trying to interpret bilaterian evolution using acoels as a proxy model for the "Urbilateria".

Results: We describe the first complete mitochondrial genome sequence of a member of the Acoela, Symsagittifera roscoffensis. Gene content and circular organization of the mitochondrial genome does not significantly differ from other bilaterian animals. However, gene order shows no similarity to any other mitochondrial genome within the Metazoa. Phylogenetic analyses of concatenated alignments of amino acid sequences from protein coding genes support a position of Acoela and Nemertodermatida as the sister group to all other Bilateria. Our data provided no support for a sister group relationship between Xenoturbellida and Acoela or Acoelomorpha. The phylogenetic position of Xenoturbella bocki as sister group to or part of the deuterostomes was also unstable.

Conclusions: Our phylogenetic analysis supports the view that acoels and nemertodermatids are the earliest divergent extant lineage of Bilateria. As such they remain a valid source for seeking primitive characters present in the last common ancestor of Bilateria. Gene order of mitochondrial genomes seems to be very variable among Acoela and Nemertodermatida and the groundplan for the metazoan mitochondrial genome remains elusive. More data are needed to interpret mitochondrial genome evolution at the base of Bilateria.

Figure 1

Mitochondrial DNA map of S. roscoffensis [GenBank: HM237350]. Gene abbreviations are explained in the text. Numbers show the size of non-coding regions between genes. Protein-coding genes on plus-strand are coloured in green, on minus-strand in blue and ribosomal RNA genes are in red. tRNA genes are black arrows, specified by the three letter abbreviation of the corresponding amino acid.

Figure 2

Presumed secondary structures of the putative tRNA genes in S. roscoffensis. Sequences are illustrated from 5' to 3' end. trnL1 and trnL2 are nested in other genes (nad5, rrnL), therefore their existence is highly speculative. But there were no alternatives found in other parts of the mitochondrial genome.

Figure 3

Gene order comparison. Gene order of S. roscoffensis compared to the partial sequences of Paratomella rubra (Acoela), Nemertoderma westbladi (Nemertodermatida) and Microstomum lineare (Rhabditophora), as well as to the complete sequence of Fasciola hepatica (Trematoda), Xenoturbella bocki (Xenoturbellida) and the putative bilaterian ground pattern.

Figure 4

Phylogenetic analysis of mitochondrial sequences - first alternative. Best tree from two of four independent chains of Bayesian inference analysis (NH-PhyloBayes, CAT-BP, concatenated amino acid alignments of 11 mitochondrial protein-coding genes). Numbers close to nodes are Bayesian posterior probabilities. Branch lengths reflect substitutions per site (see scale bar). Asterisks indicate taxa with incomplete mt genome data.

Figure 5

Phylogenetic analysis of mitochondrial sequences - second alternative. Alternative tree topology from one of four independent chains of Bayesian inference analysis (NH-PhyloBayes, CAT-BP, concatenated amino acid alignments of 11 mitochondrial protein-coding genes). Numbers close to nodes are Bayesian posterior probabilities. Branch lengths reflect substitutions per site (see scale bar). Asterisks indicate taxa with incomplete mt genome data.