Emergent RNA–RNA interactions can promote stability in a facultative phototrophic endosymbiosis

Stable endosymbiosis between eukaryotic microbes has driven the evolution of further cellular complexity. Yet the mechanisms that can act to stabilize an emergent eukaryote–eukaryote endosymbiosis are unclear. Using the model facultative endosymbiotic system, Paramecium bursaria , we demonstrate that endosymbiont–host RNA–RNA interactions can drive a cost to host growth upon endosymbiont digestion. These RNA–RNA interactions are facilitated by the host RNA-interference system. For endosymbiont messenger RNA sharing a high level of sequence identity with host transcripts, this process can result in host gene knockdown. We propose that these endosymbiont–host RNA–RNA interactions—“RNA-interference collisions”—represent an emergent mechanism to sanction the host for breakdown of the endosymbiosis, promoting the stability of the facultative endosymbiotic interaction.