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The holozoan Capsaspora owczarzaki possesses a diverse complement of active transposable element families.

Carr M, Suga H - Genome Biol Evol (2014)

Bottom Line: The families present in the genome show contrasting population histories and appear to be in different stages of their life cycles.Transcriptome data have been analyzed from multiple stages in the C. owczarzaki life cycle.Expression levels vary greatly both between families and between different stages of the life cycle, suggesting an unexpectedly complex level of transposable element regulation in a single celled organism.

View Article: PubMed Central - PubMed

Affiliation: School of Applied Sciences, University of Huddersfield, West Yorkshire, United Kingdom.

ABSTRACT
Capsaspora owczarzaki, a protistan symbiont of the pulmonate snail Biomphalaria glabrata, is the centre of much interest in evolutionary biology due to its close relationship to Metazoa. The whole genome sequence of this protist has revealed new insights into the ancestral genome composition of Metazoa, in particular with regard to gene families involved in the evolution of multicellularity. The draft genome revealed the presence of 23 families of transposable element, made up from DNA transposon as well as long terminal repeat (LTR) and non-LTR retrotransposon families. The phylogenetic analyses presented here show that all of the transposable elements identified in the C. owczarzaki genome have orthologous families in Metazoa, indicating that the ancestral metazoan also had a rich diversity of elements. Molecular evolutionary analyses also show that the majority of families has recently been active within the Capsaspora genome. One family now appears to be inactive and a further five families show no evidence of current transposition. Most individual element copies are evolutionarily young; however, a small proportion of inserts appear to have persisted for longer in the genome. The families present in the genome show contrasting population histories and appear to be in different stages of their life cycles. Transcriptome data have been analyzed from multiple stages in the C. owczarzaki life cycle. Expression levels vary greatly both between families and between different stages of the life cycle, suggesting an unexpectedly complex level of transposable element regulation in a single celled organism.

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Capsaspora owczarzaki transposable element expression. The expression levels of transposable elements were approximated by the normalized number of RNAseq reads and shown as a heatmap. (A) Values were normalized by the largest expression level, which is that of Cocv1 in adherent cells. (B) The color map is presented in log scale (values normalized to 0–1.0 range).
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evu068-F4: Capsaspora owczarzaki transposable element expression. The expression levels of transposable elements were approximated by the normalized number of RNAseq reads and shown as a heatmap. (A) Values were normalized by the largest expression level, which is that of Cocv1 in adherent cells. (B) The color map is presented in log scale (values normalized to 0–1.0 range).

Mentions: Transcription is an essential component of transposition, in order to produce catalytic proteins and, in the case of retrotransposons, RNA daughter elements. The presence of TE sequences in the RNASeq reads generated by the C. owczarzaki genome project (Sebé-Pedrós et al. 2013; Suga et al. 2013) would therefore provide indirect evidence that a family may be active. The complete RNASeq database contained 394,576,834 reads, of which 1,165,292 (0.3%) were of TE origin (tables 1–3 and fig. 4). Only one family, the LTR retrotransposon Cocv4, was essentially absent from the reads; this family presented a small number of short fragments, which did not cover the entire length of the known sequence, indicating that this family is no longer active in the sequenced culture of C. owczarzaki. The expression levels of the families vary by over three orders of magnitude and transcripts of Cocv1 dominate, with 37.5% of reads being from this family. The number of RNASeq reads shows a strong positive correlation (r = 0.846) with the number of identical paralogous copies in the genome for each family (supplementary fig. S3, Supplementary Material online). This shows that the number of identical copies (which can be viewed as reflecting the transposition rate of a family) can be considered a good predictor of a family’s expression in C. owczarzaki.Fig. 4.—


The holozoan Capsaspora owczarzaki possesses a diverse complement of active transposable element families.

Carr M, Suga H - Genome Biol Evol (2014)

Capsaspora owczarzaki transposable element expression. The expression levels of transposable elements were approximated by the normalized number of RNAseq reads and shown as a heatmap. (A) Values were normalized by the largest expression level, which is that of Cocv1 in adherent cells. (B) The color map is presented in log scale (values normalized to 0–1.0 range).
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4007536&req=5

evu068-F4: Capsaspora owczarzaki transposable element expression. The expression levels of transposable elements were approximated by the normalized number of RNAseq reads and shown as a heatmap. (A) Values were normalized by the largest expression level, which is that of Cocv1 in adherent cells. (B) The color map is presented in log scale (values normalized to 0–1.0 range).
Mentions: Transcription is an essential component of transposition, in order to produce catalytic proteins and, in the case of retrotransposons, RNA daughter elements. The presence of TE sequences in the RNASeq reads generated by the C. owczarzaki genome project (Sebé-Pedrós et al. 2013; Suga et al. 2013) would therefore provide indirect evidence that a family may be active. The complete RNASeq database contained 394,576,834 reads, of which 1,165,292 (0.3%) were of TE origin (tables 1–3 and fig. 4). Only one family, the LTR retrotransposon Cocv4, was essentially absent from the reads; this family presented a small number of short fragments, which did not cover the entire length of the known sequence, indicating that this family is no longer active in the sequenced culture of C. owczarzaki. The expression levels of the families vary by over three orders of magnitude and transcripts of Cocv1 dominate, with 37.5% of reads being from this family. The number of RNASeq reads shows a strong positive correlation (r = 0.846) with the number of identical paralogous copies in the genome for each family (supplementary fig. S3, Supplementary Material online). This shows that the number of identical copies (which can be viewed as reflecting the transposition rate of a family) can be considered a good predictor of a family’s expression in C. owczarzaki.Fig. 4.—

Bottom Line: The families present in the genome show contrasting population histories and appear to be in different stages of their life cycles.Transcriptome data have been analyzed from multiple stages in the C. owczarzaki life cycle.Expression levels vary greatly both between families and between different stages of the life cycle, suggesting an unexpectedly complex level of transposable element regulation in a single celled organism.

View Article: PubMed Central - PubMed

Affiliation: School of Applied Sciences, University of Huddersfield, West Yorkshire, United Kingdom.

ABSTRACT
Capsaspora owczarzaki, a protistan symbiont of the pulmonate snail Biomphalaria glabrata, is the centre of much interest in evolutionary biology due to its close relationship to Metazoa. The whole genome sequence of this protist has revealed new insights into the ancestral genome composition of Metazoa, in particular with regard to gene families involved in the evolution of multicellularity. The draft genome revealed the presence of 23 families of transposable element, made up from DNA transposon as well as long terminal repeat (LTR) and non-LTR retrotransposon families. The phylogenetic analyses presented here show that all of the transposable elements identified in the C. owczarzaki genome have orthologous families in Metazoa, indicating that the ancestral metazoan also had a rich diversity of elements. Molecular evolutionary analyses also show that the majority of families has recently been active within the Capsaspora genome. One family now appears to be inactive and a further five families show no evidence of current transposition. Most individual element copies are evolutionarily young; however, a small proportion of inserts appear to have persisted for longer in the genome. The families present in the genome show contrasting population histories and appear to be in different stages of their life cycles. Transcriptome data have been analyzed from multiple stages in the C. owczarzaki life cycle. Expression levels vary greatly both between families and between different stages of the life cycle, suggesting an unexpectedly complex level of transposable element regulation in a single celled organism.

Show MeSH
Related in: MedlinePlus