Remarkable abundance and evolution of mobile group II introns in Wolbachia bacterial endosymbionts

Abstract

The streamlined genomes of ancient obligate endosymbionts generally lack transposable elements, as a consequence of their intracellular confinement. Yet, the genomes of Wolbachia, one of the most abundant bacterial endosymbionts on Earth, are littered with transposable elements, in particular insertion sequences (ISs). This paradox raises the question of whether or not such a mobile DNA proliferation reflects a special feature of ISs. In this study, we focused on another class of transposable elements, group II introns, and conducted an in-depth analysis of their content and the microevolutionary processes responsible for their dynamics within Wolbachia genomes. We report an exceptionally high intron abundance and striking differences in copy numbers between Wolbachia strains as well as between intron families. Our bioinformatics and experimental results provide strong evidence that intron diversity is mainly caused by recent (and perhaps ongoing) mobility and horizontal transfers. Our data also support several temporally independent intron invasions during Wolbachia evolution. Furthermore, group II intron spread in some Wolbachia strains may be regulated through gene conversion-mediated inactivation of intron copies. Finally, we found introns to be involved in numerous genomic rearrangements. This underscores the high recombinogenic potential of group II introns, contrary to general expectations. Overall, our study represents the first comprehensive analysis of group II intron evolutionary dynamics in obligate intracellular bacteria. Our results show that bacterial endosymbionts with reduced genomes can sustain high loads of mobile group II introns, as hypothesized for the endosymbiont ancestor of mitochondria during early eukaryote evolution.