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The complete mitochondrial genome of Flustra foliacea (Ectoprocta, Cheilostomata) - compositional bias affects phylogenetic analyses of lophotrochozoan relationships.

Nesnidal MP, Helmkampf M, Bruchhaus I, Hausdorf B - BMC Genomics (2011)

Bottom Line: Different approaches for reducing heterogeneity in nucleotide and amino acid data sets and saturation did not result in a more robust resolution of lophotrochozoan relationships.The mitochondrial gene order is also not useful for inferring their phylogenetic relationships, because it is highly variable in ectoprocts, brachiopods and some other lophotrochozoan phyla.However, our study revealed several rare genomic changes like the evolution of long intergenic sequences and changes in the structure of tRNAs, which may be helpful for reconstructing ectoproct phylogeny.

View Article: PubMed Central - HTML - PubMed

Affiliation: Zoological Museum of the University of Hamburg, Martin-Luther-King-Platz 3, 20146 Hamburg, Germany.

ABSTRACT

Background: The phylogenetic relationships of the lophophorate lineages, ectoprocts, brachiopods and phoronids, within Lophotrochozoa are still controversial. We sequenced an additional mitochondrial genome of the most species-rich lophophorate lineage, the ectoprocts. Although it is known that there are large differences in the nucleotide composition of mitochondrial sequences of different lineages as well as in the amino acid composition of the encoded proteins, this bias is often not considered in phylogenetic analyses. We applied several approaches for reducing compositional bias and saturation in the phylogenetic analyses of the mitochondrial sequences.

Results: The complete mitochondrial genome (16,089 bp) of Flustra foliacea (Ectoprocta, Gymnolaemata, Cheilostomata) was sequenced. All protein-encoding, rRNA and tRNA genes are transcribed from the same strand. Flustra shares long intergenic sequences with the cheilostomate ectoproct Bugula, which might be a synapomorphy of these taxa. Further synapomorphies might be the loss of the DHU arm of the tRNA L(UUR), the loss of the DHU arm of the tRNA S(UCN) and the unique anticodon sequence GAG of the tRNA L(CUN). The gene order of the mitochondrial genome of Flustra differs strongly from that of the other known ectoprocts. Phylogenetic analyses of mitochondrial nucleotide and amino acid data sets show that the lophophorate lineages are more closely related to trochozoan phyla than to deuterostomes or ecdysozoans confirming the Lophotrochozoa hypothesis. Furthermore, they support the monophyly of Cheilostomata and Ectoprocta. However, the relationships of the lophophorate lineages within Lophotrochozoa differ strongly depending on the data set and the used method. Different approaches for reducing heterogeneity in nucleotide and amino acid data sets and saturation did not result in a more robust resolution of lophotrochozoan relationships.

Conclusion: The contradictory and usually weakly supported phylogenetic reconstructions of the relationships among lophotrochozoan phyla based on mitochondrial sequences indicate that these alone do not contain enough information for a robust resolution of the relations of the lophotrochozoan phyla. The mitochondrial gene order is also not useful for inferring their phylogenetic relationships, because it is highly variable in ectoprocts, brachiopods and some other lophotrochozoan phyla. However, our study revealed several rare genomic changes like the evolution of long intergenic sequences and changes in the structure of tRNAs, which may be helpful for reconstructing ectoproct phylogeny.

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Metazoan phylogeny based on mitochondrial sequences of 49 taxa. (A) Bayesian inference reconstructions calculated with the CAT model based on 2,729 amino acid positions. Bayesian posterior probabilities are shown to the right of the nodes; posterior probabilities equal to 1.0 are indicated by black circles. (B) Maximum likelihood tree calculated with the GTR model based on 7,537 nucleotides from first and second codon positions. Bootstrap support values larger than 50% are shown to the right of the nodes; 100% bootstrap values are indicated by black circles.
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Figure 5: Metazoan phylogeny based on mitochondrial sequences of 49 taxa. (A) Bayesian inference reconstructions calculated with the CAT model based on 2,729 amino acid positions. Bayesian posterior probabilities are shown to the right of the nodes; posterior probabilities equal to 1.0 are indicated by black circles. (B) Maximum likelihood tree calculated with the GTR model based on 7,537 nucleotides from first and second codon positions. Bootstrap support values larger than 50% are shown to the right of the nodes; 100% bootstrap values are indicated by black circles.

Mentions: In the Bayesian inference tree based on the mitochondrial amino acid data set edited with ALISCORE [53,54] comprising 2,729 positions of 49 taxa calculated with the CAT model implemented in PhyloBayes (Figure 5A), the long-branch group is broken up and Lophotrochozoa including Platyhelminthes form a well-supported monophylum (posterior probability 0.96). The maximum likelihood analysis of this data set with the MtZoa+F model (Additional file 6) resulted again in a long-branch attraction of platyhelminths, nematodes and chaetognaths. The monophyly of most of the lophotrochozoan phyla with the exception of the molluscs is strongly supported in both analyses, but the relationships between these phyla remains unresolved. The maximum likelihood tree based on the amino acid sequences edited with Gblocks [56] (Additional file 7) does not differ from that edited with ALISCORE in any strongly supported nodes. In the Bayesian inference tree ectoprocts are sister group of annelids (posterior probability 0.84), and brachiopods are sister group of this monophylum (0.75). Phoronida is sister group of a clade consisting of Nemertea and Polyplacophora (0.76). In contrast, according to the maximum likelihood tree ectoprocts are sister group to the long-branch group consisting of nematodes, platyhelminths and chaetognaths. Brachiopods are sister group of annelids (52% bootstrap probability) and phoronids are sister group of entoprocts (52%).


The complete mitochondrial genome of Flustra foliacea (Ectoprocta, Cheilostomata) - compositional bias affects phylogenetic analyses of lophotrochozoan relationships.

Nesnidal MP, Helmkampf M, Bruchhaus I, Hausdorf B - BMC Genomics (2011)

Metazoan phylogeny based on mitochondrial sequences of 49 taxa. (A) Bayesian inference reconstructions calculated with the CAT model based on 2,729 amino acid positions. Bayesian posterior probabilities are shown to the right of the nodes; posterior probabilities equal to 1.0 are indicated by black circles. (B) Maximum likelihood tree calculated with the GTR model based on 7,537 nucleotides from first and second codon positions. Bootstrap support values larger than 50% are shown to the right of the nodes; 100% bootstrap values are indicated by black circles.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3285623&req=5

Figure 5: Metazoan phylogeny based on mitochondrial sequences of 49 taxa. (A) Bayesian inference reconstructions calculated with the CAT model based on 2,729 amino acid positions. Bayesian posterior probabilities are shown to the right of the nodes; posterior probabilities equal to 1.0 are indicated by black circles. (B) Maximum likelihood tree calculated with the GTR model based on 7,537 nucleotides from first and second codon positions. Bootstrap support values larger than 50% are shown to the right of the nodes; 100% bootstrap values are indicated by black circles.
Mentions: In the Bayesian inference tree based on the mitochondrial amino acid data set edited with ALISCORE [53,54] comprising 2,729 positions of 49 taxa calculated with the CAT model implemented in PhyloBayes (Figure 5A), the long-branch group is broken up and Lophotrochozoa including Platyhelminthes form a well-supported monophylum (posterior probability 0.96). The maximum likelihood analysis of this data set with the MtZoa+F model (Additional file 6) resulted again in a long-branch attraction of platyhelminths, nematodes and chaetognaths. The monophyly of most of the lophotrochozoan phyla with the exception of the molluscs is strongly supported in both analyses, but the relationships between these phyla remains unresolved. The maximum likelihood tree based on the amino acid sequences edited with Gblocks [56] (Additional file 7) does not differ from that edited with ALISCORE in any strongly supported nodes. In the Bayesian inference tree ectoprocts are sister group of annelids (posterior probability 0.84), and brachiopods are sister group of this monophylum (0.75). Phoronida is sister group of a clade consisting of Nemertea and Polyplacophora (0.76). In contrast, according to the maximum likelihood tree ectoprocts are sister group to the long-branch group consisting of nematodes, platyhelminths and chaetognaths. Brachiopods are sister group of annelids (52% bootstrap probability) and phoronids are sister group of entoprocts (52%).

Bottom Line: Different approaches for reducing heterogeneity in nucleotide and amino acid data sets and saturation did not result in a more robust resolution of lophotrochozoan relationships.The mitochondrial gene order is also not useful for inferring their phylogenetic relationships, because it is highly variable in ectoprocts, brachiopods and some other lophotrochozoan phyla.However, our study revealed several rare genomic changes like the evolution of long intergenic sequences and changes in the structure of tRNAs, which may be helpful for reconstructing ectoproct phylogeny.

View Article: PubMed Central - HTML - PubMed

Affiliation: Zoological Museum of the University of Hamburg, Martin-Luther-King-Platz 3, 20146 Hamburg, Germany.

ABSTRACT

Background: The phylogenetic relationships of the lophophorate lineages, ectoprocts, brachiopods and phoronids, within Lophotrochozoa are still controversial. We sequenced an additional mitochondrial genome of the most species-rich lophophorate lineage, the ectoprocts. Although it is known that there are large differences in the nucleotide composition of mitochondrial sequences of different lineages as well as in the amino acid composition of the encoded proteins, this bias is often not considered in phylogenetic analyses. We applied several approaches for reducing compositional bias and saturation in the phylogenetic analyses of the mitochondrial sequences.

Results: The complete mitochondrial genome (16,089 bp) of Flustra foliacea (Ectoprocta, Gymnolaemata, Cheilostomata) was sequenced. All protein-encoding, rRNA and tRNA genes are transcribed from the same strand. Flustra shares long intergenic sequences with the cheilostomate ectoproct Bugula, which might be a synapomorphy of these taxa. Further synapomorphies might be the loss of the DHU arm of the tRNA L(UUR), the loss of the DHU arm of the tRNA S(UCN) and the unique anticodon sequence GAG of the tRNA L(CUN). The gene order of the mitochondrial genome of Flustra differs strongly from that of the other known ectoprocts. Phylogenetic analyses of mitochondrial nucleotide and amino acid data sets show that the lophophorate lineages are more closely related to trochozoan phyla than to deuterostomes or ecdysozoans confirming the Lophotrochozoa hypothesis. Furthermore, they support the monophyly of Cheilostomata and Ectoprocta. However, the relationships of the lophophorate lineages within Lophotrochozoa differ strongly depending on the data set and the used method. Different approaches for reducing heterogeneity in nucleotide and amino acid data sets and saturation did not result in a more robust resolution of lophotrochozoan relationships.

Conclusion: The contradictory and usually weakly supported phylogenetic reconstructions of the relationships among lophotrochozoan phyla based on mitochondrial sequences indicate that these alone do not contain enough information for a robust resolution of the relations of the lophotrochozoan phyla. The mitochondrial gene order is also not useful for inferring their phylogenetic relationships, because it is highly variable in ectoprocts, brachiopods and some other lophotrochozoan phyla. However, our study revealed several rare genomic changes like the evolution of long intergenic sequences and changes in the structure of tRNAs, which may be helpful for reconstructing ectoproct phylogeny.

Show MeSH
Related in: MedlinePlus