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The mitochondrial genome structure of Xenoturbella bocki (phylum Xenoturbellida) is ancestral within the deuterostomes.

Bourlat SJ, Rota-Stabelli O, Lanfear R, Telford MJ - BMC Evol. Biol. (2009)

Bottom Line: Xenoturbella bocki is a morphologically simple benthic marine worm recently found to belong among the deuterostomes.Phylogenetic analyses of the mitochondrial sequence indicate a weakly supported placement as a basal deuterostome, a result that may be the effect of compositional bias.Finally, while phylogenetic analyses of the mitochondrial sequences support a basal deuterostome placement, support for this decreases with the use of more sophisticated models of sequence evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Invertebrate Zoology, Swedish Museum of Natural History, Stockholm, Sweden. sarah.bourlat@nrm.se

ABSTRACT

Background: Mitochondrial genome comparisons contribute in multiple ways when inferring animal relationships. As well as primary sequence data, rare genomic changes such as gene order, shared gene boundaries and genetic code changes, which are unlikely to have arisen through convergent evolution, are useful tools in resolving deep phylogenies. Xenoturbella bocki is a morphologically simple benthic marine worm recently found to belong among the deuterostomes. Here we present analyses comparing the Xenoturbella bocki mitochondrial gene order, genetic code and control region to those of other metazoan groups.

Results: The complete mitochondrial genome sequence of Xenoturbella bocki was determined. The gene order is most similar to that of the chordates and the hemichordates, indicating that this conserved mitochondrial gene order might be ancestral to the deuterostome clade. Using data from all phyla of deuterostomes, we infer the ancestral mitochondrial gene order for this clade. Using inversion and breakpoint analyses of metazoan mitochondrial genomes, we test conflicting hypotheses for the phylogenetic placement of Xenoturbella and find a closer affinity to the hemichordates than to other metazoan groups. Comparative analyses of the control region reveal similarities in the transcription initiation and termination sites and origin of replication of Xenoturbella with those of the vertebrates. Phylogenetic analyses of the mitochondrial sequence indicate a weakly supported placement as a basal deuterostome, a result that may be the effect of compositional bias.

Conclusion: The mitochondrial genome of Xenoturbella bocki has a very conserved gene arrangement in the deuterostome group, strikingly similar to that of the hemichordates and the chordates, and thus to the ancestral deuterostome gene order. Similarity to the hemichordates in particular is suggested by inversion and breakpoint analysis. Finally, while phylogenetic analyses of the mitochondrial sequences support a basal deuterostome placement, support for this decreases with the use of more sophisticated models of sequence evolution.

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Gene map of the Xenoturbella bocki mitochondrial genome compared to other deuterostome mitochondrial genomes. Xenoturbella bocki gene order is compared to Balanoglossus carnosus and Saccoglossus kowalevskii (two hemichordates), Homo sapiens, Branchiostoma floridae (a cephalochordate) and Gymnocrinus richeri (a crinoid echinoderm). Below: Mitochondrial gene order reconstruction for the deuterostome common ancestor. *Position of the control region is uncertain. The most parsimonious scenario for the ancestral deuterostome was reconstructed using gene order information from species in the echinoderm, hemichordate, Xenoturbella, vertebrate and cephalochordate lineages. The urochordate lineage was too derived.
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Figure 1: Gene map of the Xenoturbella bocki mitochondrial genome compared to other deuterostome mitochondrial genomes. Xenoturbella bocki gene order is compared to Balanoglossus carnosus and Saccoglossus kowalevskii (two hemichordates), Homo sapiens, Branchiostoma floridae (a cephalochordate) and Gymnocrinus richeri (a crinoid echinoderm). Below: Mitochondrial gene order reconstruction for the deuterostome common ancestor. *Position of the control region is uncertain. The most parsimonious scenario for the ancestral deuterostome was reconstructed using gene order information from species in the echinoderm, hemichordate, Xenoturbella, vertebrate and cephalochordate lineages. The urochordate lineage was too derived.

Mentions: The gene order of the Xenoturbella bocki mitochondrial genome is shown in figure 1. Within the deuterostome group, the gene order of Xenoturbella bocki is most similar to that of the conserved vertebrate gene order as well as the hemichordate Balanoglossus carnosus, which has virtually the same gene order as the vertebrates [21]. In Xenoturbella, Balanoglossus and the vertebrates all protein coding genes follow the same order on the plus strand except for the control region and -nd6, the only protein coding gene on the minus strand. In the remaining deuterostome phyla, the echinoderms and the urochordates, the gene orders are very different, and vary extensively even amongst the echinoderm classes [20] (figure 1). Given that the echinoderm lineage is very derived, and considering the phylogenetic position of Xenoturbella as a separate phylum at the base of Ambulacraria [7,8], it is likely that the vertebrate/hemichordate/Xenoturbella arrangement represents the ancestral gene order for the deuterostome clade.


The mitochondrial genome structure of Xenoturbella bocki (phylum Xenoturbellida) is ancestral within the deuterostomes.

Bourlat SJ, Rota-Stabelli O, Lanfear R, Telford MJ - BMC Evol. Biol. (2009)

Gene map of the Xenoturbella bocki mitochondrial genome compared to other deuterostome mitochondrial genomes. Xenoturbella bocki gene order is compared to Balanoglossus carnosus and Saccoglossus kowalevskii (two hemichordates), Homo sapiens, Branchiostoma floridae (a cephalochordate) and Gymnocrinus richeri (a crinoid echinoderm). Below: Mitochondrial gene order reconstruction for the deuterostome common ancestor. *Position of the control region is uncertain. The most parsimonious scenario for the ancestral deuterostome was reconstructed using gene order information from species in the echinoderm, hemichordate, Xenoturbella, vertebrate and cephalochordate lineages. The urochordate lineage was too derived.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2697986&req=5

Figure 1: Gene map of the Xenoturbella bocki mitochondrial genome compared to other deuterostome mitochondrial genomes. Xenoturbella bocki gene order is compared to Balanoglossus carnosus and Saccoglossus kowalevskii (two hemichordates), Homo sapiens, Branchiostoma floridae (a cephalochordate) and Gymnocrinus richeri (a crinoid echinoderm). Below: Mitochondrial gene order reconstruction for the deuterostome common ancestor. *Position of the control region is uncertain. The most parsimonious scenario for the ancestral deuterostome was reconstructed using gene order information from species in the echinoderm, hemichordate, Xenoturbella, vertebrate and cephalochordate lineages. The urochordate lineage was too derived.
Mentions: The gene order of the Xenoturbella bocki mitochondrial genome is shown in figure 1. Within the deuterostome group, the gene order of Xenoturbella bocki is most similar to that of the conserved vertebrate gene order as well as the hemichordate Balanoglossus carnosus, which has virtually the same gene order as the vertebrates [21]. In Xenoturbella, Balanoglossus and the vertebrates all protein coding genes follow the same order on the plus strand except for the control region and -nd6, the only protein coding gene on the minus strand. In the remaining deuterostome phyla, the echinoderms and the urochordates, the gene orders are very different, and vary extensively even amongst the echinoderm classes [20] (figure 1). Given that the echinoderm lineage is very derived, and considering the phylogenetic position of Xenoturbella as a separate phylum at the base of Ambulacraria [7,8], it is likely that the vertebrate/hemichordate/Xenoturbella arrangement represents the ancestral gene order for the deuterostome clade.

Bottom Line: Xenoturbella bocki is a morphologically simple benthic marine worm recently found to belong among the deuterostomes.Phylogenetic analyses of the mitochondrial sequence indicate a weakly supported placement as a basal deuterostome, a result that may be the effect of compositional bias.Finally, while phylogenetic analyses of the mitochondrial sequences support a basal deuterostome placement, support for this decreases with the use of more sophisticated models of sequence evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Invertebrate Zoology, Swedish Museum of Natural History, Stockholm, Sweden. sarah.bourlat@nrm.se

ABSTRACT

Background: Mitochondrial genome comparisons contribute in multiple ways when inferring animal relationships. As well as primary sequence data, rare genomic changes such as gene order, shared gene boundaries and genetic code changes, which are unlikely to have arisen through convergent evolution, are useful tools in resolving deep phylogenies. Xenoturbella bocki is a morphologically simple benthic marine worm recently found to belong among the deuterostomes. Here we present analyses comparing the Xenoturbella bocki mitochondrial gene order, genetic code and control region to those of other metazoan groups.

Results: The complete mitochondrial genome sequence of Xenoturbella bocki was determined. The gene order is most similar to that of the chordates and the hemichordates, indicating that this conserved mitochondrial gene order might be ancestral to the deuterostome clade. Using data from all phyla of deuterostomes, we infer the ancestral mitochondrial gene order for this clade. Using inversion and breakpoint analyses of metazoan mitochondrial genomes, we test conflicting hypotheses for the phylogenetic placement of Xenoturbella and find a closer affinity to the hemichordates than to other metazoan groups. Comparative analyses of the control region reveal similarities in the transcription initiation and termination sites and origin of replication of Xenoturbella with those of the vertebrates. Phylogenetic analyses of the mitochondrial sequence indicate a weakly supported placement as a basal deuterostome, a result that may be the effect of compositional bias.

Conclusion: The mitochondrial genome of Xenoturbella bocki has a very conserved gene arrangement in the deuterostome group, strikingly similar to that of the hemichordates and the chordates, and thus to the ancestral deuterostome gene order. Similarity to the hemichordates in particular is suggested by inversion and breakpoint analysis. Finally, while phylogenetic analyses of the mitochondrial sequences support a basal deuterostome placement, support for this decreases with the use of more sophisticated models of sequence evolution.

Show MeSH
Related in: MedlinePlus