Recurrent acquisition of cytosine methyltransferases into eukaryotic retrotransposons

Mendoza, Alex de; Bonnet, Amandine; Vargas-Landin, Dulce B; Ji, Nanjing; Li, Hongfei; Yang, Feng; Li, Ling; Hori, Koichi; Pflueger, Jahnvi; Buckberry, Sam; Ohta, Hiroyuki; Rosic, Nedeljka; Lesage, Pascale; Lin, Senjie; Lister, Ryan

doi:10.1038/s41467-018-03724-9

Cited by 53 publications

(82 citation statements)

References 52 publications

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“…According to our analysis of enriched gene functions in S. tridacnidorum relative to S. natans based on annotated GO terms, methylation and the biosynthesis of histidine and peptidoglycan were among the most significant (Supplementary Table 9). The enrichment of methylation is not surprising because retrotransposons of Symbiodiniaceae are known to have acquired methyltransferase domains, likely contributing to the hypermethylated nuclear genomes of these dinoflagellates 41 . The link between the extent of methylation in symbiodiniacean genomes and its representation among predicted genes can be further assessed using methylation sequencing.…”

Section: Resultsmentioning

confidence: 99%

Structural rearrangements drive extensive genome divergence between symbiotic and free-living Symbiodinium

González‐Pech¹,

Stephens²,

Chen³

et al. 2019

Preprint

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16Symbiodiniaceae are predominantly symbiotic dinoflagellates critical to corals and other reef 17 organisms. Symbiodinium is a basal symbiodiniacean lineage and includes symbiotic and free-living 18 taxa. However, the molecular mechanisms underpinning these distinct lifestyles remain little 19 known. Here, we present high-quality de novo genome assemblies for the symbiotic Symbiodinium 20 tridacnidorum CCMP2592 (genome size 1.3 Gbp) and the free-living Symbiodinium natans 21 CCMP2548 (genome size 0.74 Gbp). These genomes display extensive sequence divergence, 22sharing only ~1.5% conserved regions (≥90% identity). We predicted 45,474 and 35,270 genes for 23 S. tridacnidorum and S. natans, respectively; of the 58,541 homologous gene families, 28.5% are 24 common to both genomes. We recovered a greater extent of gene duplication and higher abundance 25 of repeats, transposable elements and pseudogenes in the genome of S. tridacnidorum than in that of 26 S. natans. These findings demonstrate that genome structural rearrangements are pertinent to 27 distinct lifestyles in Symbiodinium, and may contribute to the vast genetic diversity within the 28 genus, and more broadly in Symbiodiniaceae. Moreover, the results from our whole-genome 29 comparisons against a free-living outgroup support the notion that the symbiotic lifestyle is a 30 derived trait in, and that the free-living lifestyle is ancestral to, Symbiodinium. 31 with the potential to shift between a free-living motile stage (i.e. mastigote form) and a spherical 56 symbiotic stage (i.e. coccoid form). The genomes of facultative and recent intracellular symbionts 57 and parasites are usually very unstable, with extensive structural rearrangements, intensified activity 58 of transposable elements (TEs) and exacerbated gene duplication that leads to the accumulation of 59 pseudogenes 19,20 . Symbiotic Symbiodiniaceae are thus expected to display similar genomic features. 60In this study, we present draft de novo genome assemblies of S. tridacnidorum CCMP2592 and S. 61 natans CCMP2548. Using a comparative genomic approach, we found extensive genome-sequence 62 divergence and few shared families of predicted genes between the two species. A greater extent of 63 gene duplication, and the higher abundance of TEs and pseudogenes in S. tridacnidorum relative to 64 S. natans suggest that duplication and transposition underpin genome divergence between these 65 species. 66 5

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Section: Resultsmentioning

confidence: 99%

Structural rearrangements drive extensive genome divergence between symbiotic and free-living Symbiodinium

González‐Pech¹,

Stephens²,

Chen³

et al. 2019

Preprint

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“…Cytosine methylation has been described in genomes of eukaryotes including dinoflagellates, potentially as a mechanism for silencing of transposable elements and regulation of gene expression [32][33][34] . A recent study of the Breviolum minutum genome revealed that cytosine methylation often occurred at CG dinucleotides 35 . The impact of methylation on recovery of splice leaders in dinoflagellates remains to be systematically investigated.…”

Section: Dinosl In Full-length Transcripts Of Polarella Glacialismentioning

confidence: 99%

Polarella glacialis genomes encode tandem repeats of single-exon genes with functions critical to adaptation of dinoflagellates

Stephens

González‐Pech

Cheng

et al. 2019

Preprint

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Dinoflagellates are taxonomically diverse, ecologically important phytoplankton in marine and freshwater environments. Here, we present two draft diploid genome assemblies of the free-living dinoflagellate Polarella glacialis, isolated from the Arctic and Antarctica. For each genome, guided using full-length transcriptome data, we predicted >50,000 high-quality genes. About 68% of the genome is repetitive sequence; long terminal repeats likely contribute to intra-species structural divergence and distinct genome sizes (3.0 and 2.7 Gbp).Of all genes, ~40% are encoded unidirectionally, ~25% comprised of single exons. Multigenome comparison unveiled genes specific to P. glacialis and a common, putatively bacterial, origin of ice-binding domains in cold-adapted dinoflagellates. Our results elucidate how selection acts within the context of a complex genome structure to facilitate local adaptation. Since most dinoflagellate genes are constitutively expressed, Polarella glacialis has enhanced transcriptional responses via unidirectional, tandem duplication of single-exon genes that encode functions critical to survival in cold, low-light environments. health risks 6 . Some taxa have specialised to inhabit extreme environments, such as those found in the brine channels of polar sea ice 7-10 .Thus far, available genome data of dinoflagellates are largely restricted to symbiotic or parasitic species [11][12][13][14][15][16][17] . These lineages were chosen for sequencing because their genomes are relatively small, i.e. 0.12-4.8 Gbp. In comparison, genomes of other free-living dinoflagellates are much larger in size, ranging from ~7 Gbp in the psychrophile Polarella glacialis, to over 200 Gbp in Prorocentrum sp. based on DAPI-staining of DNA content 18 .Repeat content has been estimated at >55% in the genome sequences of some free-living dinoflagellates 19,20 ; single-exon genes have also been described 21 . Given that most dinoflagellate lineages are free-living, whole genome sequences of these taxa are critical to understand the molecular mechanisms that underpin their successful diversification in specialised environmental niches.Polarella glacialis, a psychrophilic (cold-adapted) free-living species, represents an excellent system for genomic studies of dinoflagellates for three reasons. First, it is closely related to Symbiodiniaceae (both in Order Suessiales), the family that contains the coral reef symbionts, e.g. Symbiodinium and related genera. Second, P. glacialis has been reported only in polar regions. Studying the P. glacialis genome can thus provide a first glimpse into molecular mechanisms that underlie both the evolutionary transition of dinoflagellates from a free-living to a symbiotic lifestyle, and the adaptation to extreme environments. Third, the estimated genome size of P. glacialis is still in the smaller range (~7 Gbp 18 ) of all dinoflagellate taxa, which presents a technical advantage in terms of allowing efficient genome assembly and gene prediction.

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“…Thalasiosira ) and recently in dinoflaggelates (e.g. Symbiodinium kawagutii and Symbiodinium minutum ), but its function remains elusive 20,61 . The most closely related branch to DNMT6 contains a group of bacterial DNMTs (here represented by Agrobacterium tumefaciens , Salmonella enterica , Escherichia coli ).…”

Section: Resultsmentioning

confidence: 99%

“…We found that LdDNMT is in fact a DNMT6, just as those found in L. major and T. brucei 20 . Interestingly, all other (non-Trypanosomatid) species studied so far had either multiple DNMT6 copies and/or other DNMT subfamily members in their genomes 20,61 . Therefore, Trypanosomatids might be a unique model species to further study the role of this elusive DNMT subfamily, as there can be no interaction with the effects of other DNMTs.…”

Section: Discussionmentioning

confidence: 99%

The absence of C-5 DNA methylation in Leishmania donovani allows DNA enrichment from complex samples

Cuypers

Dumetz

Meysman

et al. 2019

Preprint

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Cytosine C5 methylation is an important epigenetic control mechanism in a wide array of Eukaryotic organisms and generally carried out by proteins of C-5 DNA methyltransferase family (DNMTs). In several protozoans the status of this mechanism remains elusive, such as in Leishmania, the causative agent of the disease leishmaniasis in humans and a wide array of vertebrate animals. In this work, we show that the Leishmania donovani genome contains a C-5 DNA methyltransferase (DNMT) from the DNMT6 subfamily, of which the function is still unclear, and verified its expression at RNA level. We created viable overexpressor and knock-out lines of this enzyme and characterised their genome-wide methylation patterns using whole-genome bisulfite sequencing, together with promastigote and amastigote control lines. Interestingly, despite DNMT6 presence, we found that methylation levels were equal to or lower than 0.0003% at CpG sites, 0.0005% at CHG sites and 0.0126% at CHH sites at genome scale. As none of the methylated sites were retained after manual verification, we conclude that there is no evidence for DNA methylation in this species. We demonstrate that this difference in DNA methylation between the parasite (no detectable DNA methylation) and the vertebrate host (DNA methylation), allows enrichment of parasite versus host DNA using Methyl-CpG-binding domain columns, readily available in commercial kits. As such, we depleted methylated DNA from mixes of Leishmania promastigote and amastigote DNA with human DNA, resulting in average Leishmania:human enrichments from 62x up to 263x. These results open a promising avenue for unmethylated DNA enrichment as a pre-enrichment step before sequencing Leishmania clinical samples.

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Recurrent acquisition of cytosine methyltransferases into eukaryotic retrotransposons

Cited by 53 publications

References 52 publications

Structural rearrangements drive extensive genome divergence between symbiotic and free-living Symbiodinium

Structural rearrangements drive extensive genome divergence between symbiotic and free-living Symbiodinium

Polarella glacialis genomes encode tandem repeats of single-exon genes with functions critical to adaptation of dinoflagellates

The absence of C-5 DNA methylation in Leishmania donovani allows DNA enrichment from complex samples

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