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Molecular evolution of rDNA in early diverging Metazoa: first comparative analysis and phylogenetic application of complete SSU rRNA secondary structures in Porifera.

Voigt O, Erpenbeck D, Wörheide G - BMC Evol. Biol. (2008)

Bottom Line: We found base compositional and structural differences in SSU rRNA among Demospongiae, Hexactinellida (glass sponges) and Calcarea (calcareous sponges).Therefore, these features can provide alternative support for sequence-based topologies and give insights into the evolution of the molecule itself.To encourage and facilitate the application of rRNA models in phylogenetics of early metazoans, we present 52 SSU rRNA secondary structures over the taxonomic range of Porifera in a database, along with some basic tools for relevant format-conversion.

View Article: PubMed Central - HTML - PubMed

Affiliation: Dept. of Geobiology, Geoscience Centre Göttingen, University of Göttingen, D-37077 Göttingen, Germany. ovoigt@gwdg.de

ABSTRACT

Background: The cytoplasmic ribosomal small subunit (SSU, 18S) ribosomal RNA (rRNA) is the most frequently-used gene for molecular phylogenetic studies. However, information regarding its secondary structure is neglected in most phylogenetic analyses. Incorporation of this information is essential in order to apply specific rRNA evolutionary models to overcome the problem of co-evolution of paired sites, which violates the basic assumption of the independent evolution of sites made by most phylogenetic methods. Information about secondary structure also supports the process of aligning rRNA sequences across taxa. Both aspects have been shown to increase the accuracy of phylogenetic reconstructions within various taxa.Here, we explore SSU rRNA secondary structures from the three extant classes of Phylum Porifera (Grant, 1836), a pivotal, but largely unresolved taxon of early branching Metazoa. This is the first phylogenetic study of poriferan SSU rRNA data to date that includes detailed comparative secondary structure information for all three sponge classes.

Results: We found base compositional and structural differences in SSU rRNA among Demospongiae, Hexactinellida (glass sponges) and Calcarea (calcareous sponges). We showed that analyses of primary rRNA sequences, including secondary structure-specific evolutionary models, in combination with reconstruction of the evolution of unusual structural features, reveal a substantial amount of additional information. Of special note was the finding that the gene tree topologies of marine haplosclerid demosponges, which are inconsistent with the current morphology-based classification, are supported by our reconstructed evolution of secondary structure features. Therefore, these features can provide alternative support for sequence-based topologies and give insights into the evolution of the molecule itself. To encourage and facilitate the application of rRNA models in phylogenetics of early metazoans, we present 52 SSU rRNA secondary structures over the taxonomic range of Porifera in a database, along with some basic tools for relevant format-conversion.

Conclusion: We demonstrated that sophisticated secondary structure analyses can increase the potential phylogenetic information of already available rDNA sequences currently accessible in databases and conclude that the importance of SSU rRNA secondary structure information for phylogenetic reconstruction is still generally underestimated, at least among certain early branching metazoans.

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Related in: MedlinePlus

SSU rRNA secondary structure of Acanthascus dawsoni [GenBank: AF100949] (Lyssacinosida, Rossellidae). Hexactinellid-specific helical insertions within E23_1 are shown in a box. Inset: Prediction of secondary structure insertions in E23_1 within other Hexactinellida. The insertions are predicted to form two helices in Hexasterophora (Lyssacinosida + Hexactinosida), and one helix in Amphidiscophora (Semperella schulzei). *Note that Farrea occa (AF159623) represents an (in other than the displayed part) incomplete, potential pseudogene molecule.
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Figure 3: SSU rRNA secondary structure of Acanthascus dawsoni [GenBank: AF100949] (Lyssacinosida, Rossellidae). Hexactinellid-specific helical insertions within E23_1 are shown in a box. Inset: Prediction of secondary structure insertions in E23_1 within other Hexactinellida. The insertions are predicted to form two helices in Hexasterophora (Lyssacinosida + Hexactinosida), and one helix in Amphidiscophora (Semperella schulzei). *Note that Farrea occa (AF159623) represents an (in other than the displayed part) incomplete, potential pseudogene molecule.

Mentions: Porifera have the typical eukaryotic core SSU rRNA structure (see Figs. 2, 3, 4). The moderate length variation between Calcarea and most demosponges is primarily caused by insertions in unpaired regions or by elongation of helices 10, E10_1 and 43 (Table 1). In Hexactinellida, on average, these three helices are largely elongated compared to Calcarea and Demospongiae (Fig. 3), but the lengths of the E10_1 helices of some demosponge sequences fall into the same range.


Molecular evolution of rDNA in early diverging Metazoa: first comparative analysis and phylogenetic application of complete SSU rRNA secondary structures in Porifera.

Voigt O, Erpenbeck D, Wörheide G - BMC Evol. Biol. (2008)

SSU rRNA secondary structure of Acanthascus dawsoni [GenBank: AF100949] (Lyssacinosida, Rossellidae). Hexactinellid-specific helical insertions within E23_1 are shown in a box. Inset: Prediction of secondary structure insertions in E23_1 within other Hexactinellida. The insertions are predicted to form two helices in Hexasterophora (Lyssacinosida + Hexactinosida), and one helix in Amphidiscophora (Semperella schulzei). *Note that Farrea occa (AF159623) represents an (in other than the displayed part) incomplete, potential pseudogene molecule.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2289807&req=5

Figure 3: SSU rRNA secondary structure of Acanthascus dawsoni [GenBank: AF100949] (Lyssacinosida, Rossellidae). Hexactinellid-specific helical insertions within E23_1 are shown in a box. Inset: Prediction of secondary structure insertions in E23_1 within other Hexactinellida. The insertions are predicted to form two helices in Hexasterophora (Lyssacinosida + Hexactinosida), and one helix in Amphidiscophora (Semperella schulzei). *Note that Farrea occa (AF159623) represents an (in other than the displayed part) incomplete, potential pseudogene molecule.
Mentions: Porifera have the typical eukaryotic core SSU rRNA structure (see Figs. 2, 3, 4). The moderate length variation between Calcarea and most demosponges is primarily caused by insertions in unpaired regions or by elongation of helices 10, E10_1 and 43 (Table 1). In Hexactinellida, on average, these three helices are largely elongated compared to Calcarea and Demospongiae (Fig. 3), but the lengths of the E10_1 helices of some demosponge sequences fall into the same range.

Bottom Line: We found base compositional and structural differences in SSU rRNA among Demospongiae, Hexactinellida (glass sponges) and Calcarea (calcareous sponges).Therefore, these features can provide alternative support for sequence-based topologies and give insights into the evolution of the molecule itself.To encourage and facilitate the application of rRNA models in phylogenetics of early metazoans, we present 52 SSU rRNA secondary structures over the taxonomic range of Porifera in a database, along with some basic tools for relevant format-conversion.

View Article: PubMed Central - HTML - PubMed

Affiliation: Dept. of Geobiology, Geoscience Centre Göttingen, University of Göttingen, D-37077 Göttingen, Germany. ovoigt@gwdg.de

ABSTRACT

Background: The cytoplasmic ribosomal small subunit (SSU, 18S) ribosomal RNA (rRNA) is the most frequently-used gene for molecular phylogenetic studies. However, information regarding its secondary structure is neglected in most phylogenetic analyses. Incorporation of this information is essential in order to apply specific rRNA evolutionary models to overcome the problem of co-evolution of paired sites, which violates the basic assumption of the independent evolution of sites made by most phylogenetic methods. Information about secondary structure also supports the process of aligning rRNA sequences across taxa. Both aspects have been shown to increase the accuracy of phylogenetic reconstructions within various taxa.Here, we explore SSU rRNA secondary structures from the three extant classes of Phylum Porifera (Grant, 1836), a pivotal, but largely unresolved taxon of early branching Metazoa. This is the first phylogenetic study of poriferan SSU rRNA data to date that includes detailed comparative secondary structure information for all three sponge classes.

Results: We found base compositional and structural differences in SSU rRNA among Demospongiae, Hexactinellida (glass sponges) and Calcarea (calcareous sponges). We showed that analyses of primary rRNA sequences, including secondary structure-specific evolutionary models, in combination with reconstruction of the evolution of unusual structural features, reveal a substantial amount of additional information. Of special note was the finding that the gene tree topologies of marine haplosclerid demosponges, which are inconsistent with the current morphology-based classification, are supported by our reconstructed evolution of secondary structure features. Therefore, these features can provide alternative support for sequence-based topologies and give insights into the evolution of the molecule itself. To encourage and facilitate the application of rRNA models in phylogenetics of early metazoans, we present 52 SSU rRNA secondary structures over the taxonomic range of Porifera in a database, along with some basic tools for relevant format-conversion.

Conclusion: We demonstrated that sophisticated secondary structure analyses can increase the potential phylogenetic information of already available rDNA sequences currently accessible in databases and conclude that the importance of SSU rRNA secondary structure information for phylogenetic reconstruction is still generally underestimated, at least among certain early branching metazoans.

Show MeSH
Related in: MedlinePlus