Testing the Retroelement Invasion Hypothesis for the Emergence of the Ancestral Eukaryotic Cell*

Phylogenetic evidence suggests that the ancestral eukaryotic cell emerged as a result of invasion and proliferation of retroelements, selfish mobile genetic elements that copy and paste themselves within a host genome. Here we test this hypothesis by determining the pressures retroelements exert on simple genomes. We transferred two retroelements, human LINE-1 and the bacterial group II intron Ll.LtrB, into bacteria, and find that both are functional and detrimental to growth. We find, surprisingly, that retroelement lethality and proliferation is enhanced by the ability to perform eukaryotic-like nonhomologous end-joining (NHEJ) DNA repair. We show that the only stable evolutionary consequence in simple cells is maintenance of retroelements in low numbers, and that retrotransposition in eukaryotes must be finely tuned to allow proliferation.