Pervasive co-option of prokaryotic adenine methyltransferases by eukaryotic retrotransposons

Abstract

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.