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| Status |
Public on Jun 30, 2024 |
| Title |
Annelid methylomes reveal ancestral developmental and ageing-associated epigenetic erosion across Bilateria |
| Organisms |
Owenia fusiformis; Capitella teleta; Dimorphilus gyrociliatus |
| Experiment type |
Methylation profiling by high throughput sequencing
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| Summary |
Background
DNA methylation in the form of 5-methylcytosine (5mC) is the most abundant base modification in animals. However, 5mC levels vary widely across taxa. Whilst vertebrate genomes are hypermethylated, in most invertebrates, 5mC concentrates on constantly and highly transcribed genes (gene body methylation; GbM) and, in some species, on transposable elements (TEs), a pattern known as ‘mosaic’. Yet, the role and developmental dynamics of 5mC and how these explain interspecific differences in DNA methylation patterns remain poorly understood, especially in Spiralia, a large clade of invertebrates comprising nearly half of the animal phyla.
Results
Here, we generate base-resolution methylomes for three species with distinct genomic features and phylogenetic positions in Annelida, a major spiralian phylum. All possible 5mC patterns occur in annelids, from typical invertebrate intermediate levels in a mosaic distribution to hypermethylation and methylation loss. GbM is common to annelids with 5mC, and methylation differences across species are explained by taxon-specific transcriptional dynamics or the presence of intronic TEs. Notably, the link between GbM and transcription decays during development, alongside a gradual and global, age-dependent demethylation in adult stages. Additionally, reducing 5mC levels with cytidine analogues during early development impairs normal embryogenesis and reactivates TEs in the annelid Owenia fusiformis.
Conclusions
Our study indicates that global epigenetic erosion during development and ageing is an ancestral feature of bilateral animals. However, the tight link between transcription and gene body methylation is likely more important in early embryonic stages, and 5mC-mediated TE silencing probably emerged convergently across animal lineages.
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| Overall design |
Methylomes of three annelid species (O. fusiformis, C. teleta and D. gyrociliatus) at different developmental timepoints to investigate the 5mC dynamics during embryogenesis and the life cycle of this animals using WGBS, EM-seq and Nanopore sequencing. To investigate the impact of DNA methylation during development, we combined cytidine analogs, RNA-seq and EM-seq.
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| Contributor(s) |
Guynes K, Sarre LA, Carrillo-Baltodano AM, Davies BE, Xu L, Liang Y, Martín-Zamora FM, Hurd PJ, de Mendoza A, Martín-Durán JM |
| Citation(s) |
39090757 |
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| Submission date |
Dec 14, 2023 |
| Last update date |
Aug 26, 2024 |
| Contact name |
Jose M Martin-Duran |
| E-mail(s) |
chema.martin@qmul.ac.uk
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| Organization name |
Queen Mary University of London
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| Street address |
Mile End road
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| City |
London |
| ZIP/Postal code |
E1 4NS |
| Country |
United Kingdom |
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| Platforms (6)
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| GPL30632 |
Illumina NovaSeq 6000 (Owenia fusiformis) |
| GPL31133 |
Illumina NovaSeq 6000 (Capitella teleta) |
| GPL34004 |
Illumina HiSeq 4000 (Owenia fusiformis) |
| GPL34005 |
Illumina NextSeq 500 (Owenia fusiformis) |
| GPL34006 |
Illumina NextSeq 500 (Dimorphilus gyrociliatus) |
| GPL34007 |
PromethION (Capitella teleta) |
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| Samples (35)
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| GSM7975254 |
RNA-seq adult stage C. teleta |
| GSM7975255 |
RNA-seq adult stage O. fusiformis |
| GSM7975256 |
RNA-seq DMSO control larva O. fusiformis, replicate 1 |
| GSM7975257 |
RNA-seq DMSO control larva O. fusiformis, replicate 2 |
| GSM7975258 |
RNA-seq 5-azacytidine treated larva O. fusiformis, replicate 1 |
| GSM7975259 |
RNA-seq 5-azacytidine treated larva O. fusiformis, replicate 2 |
| GSM7975260 |
RNA-seq Zebularine treated larva O. fusiformis, replicate 1 |
| GSM7975261 |
RNA-seq Zebularine treated larva O. fusiformis, replicate 2 |
| GSM7975262 |
WGBS O. fusiformis gastrula |
| GSM7975263 |
WGBS O. fusiformis larva |
| GSM7975264 |
WGBS O. fusiformis adult |
| GSM7975265 |
EM-seq C. teleta gastrula |
| GSM7975266 |
EM-seq C. teleta larva |
| GSM7975267 |
EM-seq C. teleta adult |
| GSM7975268 |
WGBS D. gyrociliatus adult |
| GSM7975269 |
EM-seq O. fusiformis zebularine treated larva replicate 1 |
| GSM7975270 |
EM-seq O. fusiformis zebularine treated larva replicate 2 |
| GSM7975271 |
EM-seq O. fusiformis DMSO control larva replicate 1 |
| GSM7975272 |
EM-seq O. fusiformis DMSO control larva replicate 2 |
| GSM7975273 |
EM-seq O. fusiformis 5-azacytidine treated larva replicate 1 |
| GSM7975274 |
EM-seq O. fusiformis 5-azacytidine treated larva replicate 2 |
| GSM7975275 |
Nanopore methylation calls C. teleta mature female adult replicate 1 |
| GSM7975276 |
Nanopore methylation calls C. teleta mature female adult replicate 2 |
| GSM7975277 |
Nanopore methylation calls C. teleta 1 month juvenile replicate 1 |
| GSM7975278 |
Nanopore methylation calls C. teleta 1 month juvenile replicate 2 |
| GSM7975279 |
Nanopore methylation calls C. teleta competent larva replicate 1 |
| GSM7975280 |
Nanopore methylation calls C. teleta competent larva replicate 2 |
| GSM7975281 |
Nanopore methylation calls C. teleta senescent female adult replicate 1 |
| GSM7975282 |
Nanopore methylation calls C. teleta senescent female adult replicate 2 |
| GSM8257339 |
EM-seq O. fusiformis zebularine treated larva reseq replicate 1 |
| GSM8257340 |
EM-seq O. fusiformis zebularine treated larva reseq replicate 2 |
| GSM8257341 |
EM-seq O. fusiformis DMSO control larva reseq replicate 1 |
| GSM8257342 |
EM-seq O. fusiformis DMSO control larva reseq replicate 2 |
| GSM8257343 |
EM-seq O. fusiformis oocyte |
| GSM8257344 |
EM-seq O. fusiformis sperm |
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| Relations |
| BioProject |
PRJNA1052632 |
| Supplementary file |
Size |
Download |
File type/resource |
| GSE250187_RAW.tar |
5.4 Gb |
(http)(custom) |
TAR (of BED, CGMAP, TXT) |
SRA Run Selector |
| Raw data are available in SRA |
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