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A close phylogenetic relationship between Sipuncula and Annelida evidenced from the complete mitochondrial genome sequence of Phascolosoma esculenta.

Shen X, Ma X, Ren J, Zhao F - BMC Genomics (2009)

Bottom Line: It shares many more similar features with the four known annelid and one echiuran mtDNAs.Firstly, sipunculans and annelids share quite similar gene order in the mitochondrial genome, with all 37 genes located on the same strand; secondly, phylogenetic analyses based on the concatenated protein sequences also strongly support the sipunculan + annelid clade (including echiurans and pogonophorans).Hence annelid "key-characters" including segmentation may be more labile than previously assumed.

View Article: PubMed Central - HTML - PubMed

Affiliation: Jiangsu Key Laboratory of Marine Biotechnology/College of Marine Science, Huaihai Institute of Technology, Lianyungang 222005, PR China. shenthin@163.com

ABSTRACT

Background: There are many advantages to the application of complete mitochondrial (mt) genomes in the accurate reconstruction of phylogenetic relationships in Metazoa. Although over one thousand metazoan genomes have been sequenced, the taxonomic sampling is highly biased, left with many phyla without a single representative of complete mitochondrial genome. Sipuncula (peanut worms or star worms) is a small taxon of worm-like marine organisms with an uncertain phylogenetic position. In this report, we present the mitochondrial genome sequence of Phascolosoma esculenta, the first complete mitochondrial genome of the phylum.

Results: The mitochondrial genome of P.esculenta is 15,494 bp in length. The coding strand consists of 32.1% A, 21.5% C, 13.0% G, and 33.4% T bases (AT = 65.5%; AT skew = -0.019; GC skew = -0.248). It contains thirteen protein-coding genes (PCGs) with 3,709 codons in total, twenty-two transfer RNA genes, two ribosomal RNA genes and a non-coding AT-rich region (AT = 74.2%). All of the 37 identified genes are transcribed from the same DNA strand. Compared with the typical set of metazoan mt genomes, sipunculid lacks trnR but has an additional trnM. Maximum Likelihood and Bayesian analyses of the protein sequences show that Myzostomida, Sipuncula and Annelida (including echiurans and pogonophorans) form a monophyletic group, which supports a closer relationship between Sipuncula and Annelida than with Mollusca, Brachiopoda, and some other lophotrochozoan groups.

Conclusion: This is the first report of a complete mitochondrial genome as a representative within the phylum Sipuncula. It shares many more similar features with the four known annelid and one echiuran mtDNAs. Firstly, sipunculans and annelids share quite similar gene order in the mitochondrial genome, with all 37 genes located on the same strand; secondly, phylogenetic analyses based on the concatenated protein sequences also strongly support the sipunculan + annelid clade (including echiurans and pogonophorans). Hence annelid "key-characters" including segmentation may be more labile than previously assumed.

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Phylogenetic tree based on seven concatenated mitochondrial PCGs. Tree topologies produced by the two methods were very similar. Only bootstrap values or posterior probabilities more than 50% are shown and the others are represented by "-". The first numbers are from Bayesian inferences (BPP) and the second numbers are from maximum likelihood analyses (BPM). The root of all trees was determined by using the data from Porifera, Cnidaria, and Placozoa species as the outgroup.
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Figure 4: Phylogenetic tree based on seven concatenated mitochondrial PCGs. Tree topologies produced by the two methods were very similar. Only bootstrap values or posterior probabilities more than 50% are shown and the others are represented by "-". The first numbers are from Bayesian inferences (BPP) and the second numbers are from maximum likelihood analyses (BPM). The root of all trees was determined by using the data from Porifera, Cnidaria, and Placozoa species as the outgroup.

Mentions: Phylogenies based on Maximum Likelihood (ML) and Bayesian analyses of the concatenated protein sequences were in almost complete agreement (Figure 4). In both cases, Sipuncula and Annelida (including echiurans and pogonophorans) form a monophyletic group (BPP = 100, BPM = 98), which strongly supports a closer relationship between Sipuncula and Annelida than with Mollusca, Brachiopoda, and some other lophotrochozoan groups. Gene arrangement comparisons are a powerful tool for phylogenetic studies, especially for the estimation of ancient relationships [25]. A survey of mitochondrial gene order revealed a great conservation of gene arrangements across sipunculans, annelids and echiurids [see additional file 5]. Both gene arrangement data and inferred amino acid sequences reveal that the sipunculan should be consistently and significantly clustered with annelids to the exclusion of molluscs and other taxa. Our findings are in general agreement with several published molecular studies, which grouped sipunculans with annelids closely [4,18,32,47-49]. Comparative morphological and embryological evidence provide an additional support for such relationship between Sipuncula and Annelida. Investigation of larval ocelli in pelagosphera larvae gave evidence for an annelid affinity rather than to molluscs [50]. This evidence is consistent with a morphological study of neural and muscle formation in the sipunculan Phascolion strombus [51]. A recent research on the neural patterning of Phascolosoma agassizii revealed sipunculan neurogenesis initially follows a segmental pattern similar to that of annelids, which suggests the segmental ancestry of Sipuncula [49]. If sipunculans did evolve from segmented worms, then their body plan must have changed extensively at or before the start of the Cambrian, followed by a remarkable period of stasis for the past half billion years [3]. The absence of segmentation in Sipuncula would then be a secondary loss [49], probably associated with the exploitation of a sedentary, burrowing lifestyle [52].


A close phylogenetic relationship between Sipuncula and Annelida evidenced from the complete mitochondrial genome sequence of Phascolosoma esculenta.

Shen X, Ma X, Ren J, Zhao F - BMC Genomics (2009)

Phylogenetic tree based on seven concatenated mitochondrial PCGs. Tree topologies produced by the two methods were very similar. Only bootstrap values or posterior probabilities more than 50% are shown and the others are represented by "-". The first numbers are from Bayesian inferences (BPP) and the second numbers are from maximum likelihood analyses (BPM). The root of all trees was determined by using the data from Porifera, Cnidaria, and Placozoa species as the outgroup.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2667193&req=5

Figure 4: Phylogenetic tree based on seven concatenated mitochondrial PCGs. Tree topologies produced by the two methods were very similar. Only bootstrap values or posterior probabilities more than 50% are shown and the others are represented by "-". The first numbers are from Bayesian inferences (BPP) and the second numbers are from maximum likelihood analyses (BPM). The root of all trees was determined by using the data from Porifera, Cnidaria, and Placozoa species as the outgroup.
Mentions: Phylogenies based on Maximum Likelihood (ML) and Bayesian analyses of the concatenated protein sequences were in almost complete agreement (Figure 4). In both cases, Sipuncula and Annelida (including echiurans and pogonophorans) form a monophyletic group (BPP = 100, BPM = 98), which strongly supports a closer relationship between Sipuncula and Annelida than with Mollusca, Brachiopoda, and some other lophotrochozoan groups. Gene arrangement comparisons are a powerful tool for phylogenetic studies, especially for the estimation of ancient relationships [25]. A survey of mitochondrial gene order revealed a great conservation of gene arrangements across sipunculans, annelids and echiurids [see additional file 5]. Both gene arrangement data and inferred amino acid sequences reveal that the sipunculan should be consistently and significantly clustered with annelids to the exclusion of molluscs and other taxa. Our findings are in general agreement with several published molecular studies, which grouped sipunculans with annelids closely [4,18,32,47-49]. Comparative morphological and embryological evidence provide an additional support for such relationship between Sipuncula and Annelida. Investigation of larval ocelli in pelagosphera larvae gave evidence for an annelid affinity rather than to molluscs [50]. This evidence is consistent with a morphological study of neural and muscle formation in the sipunculan Phascolion strombus [51]. A recent research on the neural patterning of Phascolosoma agassizii revealed sipunculan neurogenesis initially follows a segmental pattern similar to that of annelids, which suggests the segmental ancestry of Sipuncula [49]. If sipunculans did evolve from segmented worms, then their body plan must have changed extensively at or before the start of the Cambrian, followed by a remarkable period of stasis for the past half billion years [3]. The absence of segmentation in Sipuncula would then be a secondary loss [49], probably associated with the exploitation of a sedentary, burrowing lifestyle [52].

Bottom Line: It shares many more similar features with the four known annelid and one echiuran mtDNAs.Firstly, sipunculans and annelids share quite similar gene order in the mitochondrial genome, with all 37 genes located on the same strand; secondly, phylogenetic analyses based on the concatenated protein sequences also strongly support the sipunculan + annelid clade (including echiurans and pogonophorans).Hence annelid "key-characters" including segmentation may be more labile than previously assumed.

View Article: PubMed Central - HTML - PubMed

Affiliation: Jiangsu Key Laboratory of Marine Biotechnology/College of Marine Science, Huaihai Institute of Technology, Lianyungang 222005, PR China. shenthin@163.com

ABSTRACT

Background: There are many advantages to the application of complete mitochondrial (mt) genomes in the accurate reconstruction of phylogenetic relationships in Metazoa. Although over one thousand metazoan genomes have been sequenced, the taxonomic sampling is highly biased, left with many phyla without a single representative of complete mitochondrial genome. Sipuncula (peanut worms or star worms) is a small taxon of worm-like marine organisms with an uncertain phylogenetic position. In this report, we present the mitochondrial genome sequence of Phascolosoma esculenta, the first complete mitochondrial genome of the phylum.

Results: The mitochondrial genome of P.esculenta is 15,494 bp in length. The coding strand consists of 32.1% A, 21.5% C, 13.0% G, and 33.4% T bases (AT = 65.5%; AT skew = -0.019; GC skew = -0.248). It contains thirteen protein-coding genes (PCGs) with 3,709 codons in total, twenty-two transfer RNA genes, two ribosomal RNA genes and a non-coding AT-rich region (AT = 74.2%). All of the 37 identified genes are transcribed from the same DNA strand. Compared with the typical set of metazoan mt genomes, sipunculid lacks trnR but has an additional trnM. Maximum Likelihood and Bayesian analyses of the protein sequences show that Myzostomida, Sipuncula and Annelida (including echiurans and pogonophorans) form a monophyletic group, which supports a closer relationship between Sipuncula and Annelida than with Mollusca, Brachiopoda, and some other lophotrochozoan groups.

Conclusion: This is the first report of a complete mitochondrial genome as a representative within the phylum Sipuncula. It shares many more similar features with the four known annelid and one echiuran mtDNAs. Firstly, sipunculans and annelids share quite similar gene order in the mitochondrial genome, with all 37 genes located on the same strand; secondly, phylogenetic analyses based on the concatenated protein sequences also strongly support the sipunculan + annelid clade (including echiurans and pogonophorans). Hence annelid "key-characters" including segmentation may be more labile than previously assumed.

Show MeSH