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BMC Evol Biol
2011 May 20;11:134. doi: 10.1186/1471-2148-11-134.
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The enigmatic mitochondrial genome of Rhabdopleura compacta (Pterobranchia) reveals insights into selection of an efficient tRNA system and supports monophyly of Ambulacraria.
Perseke M
,
Hetmank J
,
Bernt M
,
Stadler PF
,
Schlegel M
,
Bernhard D
.
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BACKGROUND: 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.
RESULTS: 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.
CONCLUSION: 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.
Figure 1. Nucleotide skews for the main-coding strand of the pterobranch Rhabdopleura compacta compared to other bilaterian mitochondrial genomes. Values of the nucleotide skews of R. compacta are marked by filled black circles (3rd: values for the 3rd codon position of all protein-coding genes; np: values for non- protein coding regions). The nucleotide skew values for other bilaterian mitochondrial genomes are marked by different symbols as indicated in each figure. The values of different phylogenetic groups are visualized by a cross giving the minimum and maximum of the nucleotide skews, and an ellipse with major axis in the direction of the eigenvector of the covariance matrix. Note the strong deviation of the nucleotide skews in R. compacta, similar to the mitochondrial genomes of the parasitic flatworms (Cestoda, Trematoda) and certain nematodes (Chromadorea).
Figure 2. Linear map of the mitochondrial genome of the pterobranch Rhabdopleura compacta with the (G + T)/(A + C) ratios at each nucleotide position computed for windows of size 300 (see Methods). The nucleotides were counted starting with COX1 and are shown on the bottom scale. Genes located above the middle line are transcribed from the heavy strand whereas those located below the middle line are transcribed from the light strand. UAS regions > 16 bp are indicated by arrows with the number showing their length. The values of a (G + T)/(A + C) ratio larger than slope (m = 2.824) of a fitted linear model are shaded.
Figure 3. Amino acid composition of the 13 protein-coding genes in Rhabdopleura compacta compared to closely related deuterostome species: the enteropneusts Balanoglossus carnosus and Saccoglossus kowalevskii, the sea urchin Paracentrotus lividus and the brittle star Ophiocomina nigra. Amino acids solely encoded by GT or AC rich codons are indicated by white letters. These codons are listed on the left and are identical for all mtDNAs of Deuterostomia.
Figure 4. Maximum likelihood tree of the major deuterostome groups excluding tunicates using the amino acid sequences of all thirteen mitochondrial protein-coding genes. The numbers on the nodes show the bootstrap percentages (BP) for ML and the posterior probabilities (PP) of the Bayesian analyses in this order. Asterisks indicate highest support values. The numbers in parenthesis behind the deuterostome groups show the number of analyzed species. The length of the triangles for each group indicates the variability within the group. The extreme long branch leading to the pterobranch R. compacta is based on its highly different protein-composition compared to other deuterostome sequences (for details see text).
Figure 5. Protein-coding gene order comparison of the mtDNAs from the pterobranch Rhabdopleura compacta to the enteropneusts, Xenoturbella bocki, the ground pattern of echinoderms and the consensus arrangement of vertebrates. Genes located above the middle line are transcribed from the heavy strand whereas those located below the middle line are transcribed from the light strand. The question marks indicate the unknown ancestral strand affiliation of the fragment containing the ND1 and ND2 genes in echinoderm genomes (see [11]). Rearrangement steps between the gene orders are marked by grey straight lines (transpositions) and grey crossed lines (inversions).
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