The enigmatic mitochondrial genome of Rhabdopleura compacta (Pterobranchia) reveals insights into selection of an efficient tRNA system and supports monophyly of Ambulacraria

Molecular Evolution and Animal Systematics, University of Leipzig, Talstr 33, 04103 Leipzig, Germany.
BMC Evolutionary Biology (Impact Factor: 3.37). 05/2011; 11(1):134. DOI: 10.1186/1471-2148-11-134
Source: PubMed


The Hemichordata comprises solitary-living Enteropneusta and colonial-living Pterobranchia, sharing morphological features with both Chordata and Echinodermata. Despite their key role for understanding deuterostome evolution, hemichordate phylogeny is controversial and only few molecular data are available for phylogenetic analysis. Furthermore, mitochondrial sequences are completely lacking for pterobranchs. Therefore, we determined and analyzed the complete mitochondrial genome of the pterobranch Rhabdopleura compacta to elucidate deuterostome evolution. Thereby, we also gained important insights in mitochondrial tRNA evolution.
The mitochondrial DNA of Rhabdopleura compacta corresponds in size and gene content to typical mitochondrial genomes of metazoans, but shows the strongest known strand-specific mutational bias in the nucleotide composition among deuterostomes with a very GT-rich main-coding strand. The order of the protein-coding genes in R. compacta is similar to that of the deuterostome ground pattern. However, the protein-coding genes have been highly affected by a strand-specific mutational pressure showing unusual codon frequency and amino acid composition. This composition caused extremely long branches in phylogenetic analyses. The unusual codon frequency points to a selection pressure on the tRNA translation system to codon-anticodon sequences of highest versatility instead of showing adaptations in anticodon sequences to the most frequent codons. Furthermore, an assignment of the codon AGG to Lysine has been detected in the mitochondrial genome of R. compacta, which is otherwise observed only in the mitogenomes of some arthropods. The genomes of these arthropods do not have such a strong strand-specific bias as found in R. compacta but possess an identical mutation in the anticodon sequence of the tRNALys.
A strong reversed asymmetrical mutational constraint in the mitochondrial genome of Rhabdopleura compacta may have arisen by an inversion of the replication direction and adaptation to this bias in the protein sequences leading to an enigmatic mitochondrial genome. Although, phylogenetic analyses of protein coding sequences are hampered, features of the tRNA system of R. compacta support the monophyly of Ambulacraria. The identical reassignment of AGG to Lysine in two distinct groups may have occurred by convergent evolution in the anticodon sequence of the tRNALys.

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    • "et al., 2002; Gerhart et al., 2005; Swalla and Smith, 2008; Kaul-Strehlow, 2011; Perseke et al., 2011; Stach and Kaul, 2011), but their exact origins remain a mystery. It is sufficiently well established from molecular data that the hemichordates are a sister group to the echinoderms, with which they form the Ambulacraria (Halanych, 1996; Bromham and Degnan, 1999; Cameron et al., 2000; Halanych, 2004; Peterson, 2004; Cameron, 2005; Bourlat et al., 2006; Sato et al., 2008b; Perseke et al., 2011). The Xenoturbellida are regarded as a sister group of the Ambulacraria, but the latter phylogenetic interpretation is not yet settled and the Xenoturbellida may alternatively represent an out-group to the deuterostomes (Swalla and Smith, 2008). "
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    ABSTRACT: The Hemichordata are generally interpreted as early deuterostomes, closely related to the chordates, a notion important for modern analyses of the origin of the deuterostomes. Because their fossil record is quite scanty, modern phylogenetic interpretations largely rely on analysis of DNA of the available extant taxa. The tripartite body plan of the group of worm-like hemichordates, the Enteropneusta, may be traced back in deep time to a few poorly known Middle Cambrian (Series 3, Stage 5) taxa from the Burgess Shale biota. The derived small, colonial or pseudocolonial Pterobranchia (Cephalodiscida and Graptolithina) have a more complete fossil record due to their preservable housing construction, the tubarium. The relationships of fossil taxa, putatively identified as early deuterostomes and possible hemichordates or even as pterobranchs of Lower to Middle Cambrian age (e.g. Galeaplumosus, Herpetogaster), cannot be substantiated. The Pterobranchia and their housing construction is first seen in the Middle Cambrian Series 3, Stage 5 but a clonal, colonial organization of the tubaria can only be recognized in the basal Drumian. The fossil enteropneust Mazoglossus ramsdelli Bardack, 1997 from the Carboniferous Mazon Creek Biota is re-described, its lectotype designated and illustrated for the first time.
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    • "However, in most of these highly cited molecular phylogenies, Hemichordata is represented by enteropneust species only. The position of Pterobranchia is not clear, neither in molecular studies (Cannon et al. 2009; Perseke et al. 2011) nor in morphological (Ax 2001; Cameron 2005; Nielsen 2001, 2012). The morphology of pterobranchs has traditionally been important in phylogenetic considerations of deuterostome evolution, because the sessile organization with tentacles and trimeric coelom organization was thought to link sessile echinoderms and sessile ascidians with tadpole larvae (Garstang 1928). "
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