The enigmatic mitochondrial genome of Rhabdopleura compacta (Pterobranchia) reveals insights into selection of an efficient tRNA system and supports monophyly of Ambulacraria
1 Molecular Evolution and Animal Systematics, University of Leipzig, Talstr. 33, 04103 Leipzig, Germany
2 Laboratory of Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Science, 164 West Xingang Road, 510301 Guangzhou, PR China
3 Parallel Computing and Complex Systems Group, University of Leipzig, Johannisgasse, 26, 04103 Leipzig, Germany
4 Bioinformatics Group, Dept. of Computer Science, University of Leipzig, Härtelstr, 16-18, 04107 Leipzig, Germany
5 Interdisciplinary Center for Bioinformatics, University of Leipzig, Härtelstr, 16-18, 04107 Leipzig, Germany
6 Max Planck Institute for Mathematics in the Sciences, Inselstrasse 22, 04103 Leipzig, Germany
7 Fraunhofer Institut für Zelltherapie und Immunologie, IZI, Perlickstrasse 1, 04103 Leipzig, Germany
8 Center for non-coding RNA in Technology and Health, University of Copenhagen, Grønnegårdsvej 3, 1870 Frederiksberg C, Denmark
9 Department of Theoretical Chemistry, University of Vienna, Währingerstrasse 17, 1090 Wien, Austria
10 Santa Fe Institute, 1399 Hyde Park Rd, Santa Fe, NM 87501, USA
BMC Evolutionary Biology 2011, 11:134 doi:10.1186/1471-2148-11-134Published: 20 May 2011
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.