First unraveling of the hidden and intricate evolutionary history of a bacterial group II intron family

Abstract

Abstract Bacterial group II introns are large RNA enzymes that self-splice from primary transcripts. Following excision, they can invade various DNA target sites using RNA-based mobility pathways. As fast evolving retromobile elements, which move between genetic loci within and across species, their evolutionary history was proved difficult to study and infer. Here we identified several homologs of Ll.LtrB, the model group II intron from Lactococcus lactis, and traced back their evolutionary relationship through phylogenetic analyses. Our data demonstrate that the Ll.LtrB homologs in Lactococci originate from a single and recent lateral transfer event of Ef.PcfG from Enterococcus faecalis. We also show that these introns disseminated in Lactococci following recurrent episodes of independent mobility events in conjunction with occurrences of lateral transfer. Our phylogenies identified additional lateral transfer events from the environmental clade of the more diverged Lactococci introns to a series of low-GC gram-positive bacterial species including E. faecalis. We also determined that functional intron adaptation occurred early in Lactococci following Ef.PcfG acquisition from E. faecalis and that two of the more diverged Ll.LtrB homologs remain proficient mobile elements despite the significant number of mutations acquired. This study describes the first comprehensive evolutionary history of a bacterial group II intron.