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Romero Charria, P.

Publications and source records attributed to Romero Charria, P..

3 recordsLinked to original sources

Pervasive co-option of prokaryotic adenine methyltransferases by eukaryotic retrotransposons

Cytosine DNA methylation is broadly associated with transposable element silencing across eukaryotes, whereas 6-methyladenine (6mA) in unicellular eukaryotes is linked to actively transcribed chromatin. How transposable elements adapt to these contrasting epigenetic environments remains largely unexplored. Here we identify widely distributed eukaryotic retrotransposons encoding prokaryotic-like DNA adenine methyltransferases (DAMs). Phylogenetic analyses indicate a single ancestral acquisition from prokaryotes followed by recurrent transfers between retrotransposon classes across diverse eukaryotes. DAM-carrying LTR elements are preferentially found in species encoding AMT1, the main eukaryotic 6mA methyltransferase, and show elevated 6mA levels relative to other LTR retrotransposons in multiple lineages, accompanied by increased transcription. We further identify retrotransposons combining adenine and cytosine methyltransferases with chromodomains, indicating the assembly of unexpectedly complex epigenetic toolkits within single retrotransposon units. These findings suggest that retrotransposons have repeatedly co-opted prokaryotic-like methyltransferases to exploit host 6mA-associated chromatin, highlighting adaptation to host epigenetic landscapes as a major driver of transposable element evolution.

genomics↗

Cytosine Methylation is a marker of Viral Gene Transfer across the eukaryotes

Cytosine DNA methylation patterns vary widely across eukaryotes, with its ancestral roles being understood to have included both transposable element silencing and host gene regulation. To further explore these claims, in this study, we reevaluate the evolutionary origins of DNA methyltransferases and characterise the roles of cytosine methylation on underexplored lineages, including the amoebozoan Acanthamoeba castellanii, the glaucophyte Cyanophora paradoxa, and the heterolobosean Naegleria gruberi. Our analysis of DNA methyltransferase evolution reveals a rich ancestral eukaryotic repertoire, with several eukaryotic lineages likely subsequently acquiring enzymes through lateral gene transfer (LGT). In the three species examined, DNA methylation is enriched on young transposable elements and silenced genes, suggesting an ancestral repressive function, without the transcription-linked gene body methylation of plants and animals. Notably, the closest homologues of many of the silenced, methylated genes in diverse eukaryotes belong to viruses, including giant viruses. Given the widespread occurrence of this pattern across diverse eukaryotic groups, we propose that cytosine methylation was a silencing mechanism originally acquired from bacterial donors which was used to mitigate the expression of both transposable and viral elements, and that this function may persist in creating a permissive atmosphere for LGT in diverse eukaryotic lineages. These findings further highlight the importance of epigenetic information to annotate eukaryotic genomes, as it helps delimit potentially adaptive LGTs from silenced parasitic elements.

genomics↗

Adenine DNA methylation associated to transcription is widespread across eukaryotes

DNA methylation in the form of 5-methylcytosine (5mC) is widespread in eukaryotes, while the presence of N6-methyladenine (6mA) has sparked considerable debate. Methodological disparities in quantifying and mapping 6mA in genomic DNA have fueled this controversy. Yet, the distantly related early branching fungi, ciliates and the algae Chlamydomonas reinhardtii exhibit robust 6mA methylation patterns, but the origin and evolution of 6mA remain unknown. Here we use Oxford Nanopore modified base calling to profile 6mA at base pair resolution in 18 unicellular eukaryotes spanning all major eukaryotic supergroups. Our results reveal that only species encoding the adenine methyltransferase AMT1 display robust genomic 6mA patterns. Notably, 6mA consistently accumulates downstream of transcriptional start sites, aligning with H3K4me3-enriched nucleosomes, suggesting a conserved role in placing transcriptionally permissive nucleosomes. Intriguingly, the recurrent loss of the 6mA pathway across eukaryotes, particularly in major multicellular lineages, implies a convergent alteration in the dual methylation system of the Last Eukaryotic Common Ancestor, which featured transcription-associated 6mA and repression-associated 5mC.

genomics↗