期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2021
卷号：118
期号：38
DOI：10.1073/pnas.2108874118
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
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.
Eukaryote–eukaryote endosymbiosis was responsible for the spread of chloroplast (plastid) organelles. Stability is required for the metabolic and genetic integration that drives the establishment of new organelles, yet the mechanisms that act to stabilize emergent endosymbioses—between two fundamentally selfish biological organisms—are unclear. Theory suggests that enforcement mechanisms, which punish misbehavior, may act to stabilize such interactions by resolving conflict. However, how such mechanisms can emerge in a facultative endosymbiosis has yet to be explored. Here, we propose that endosymbiont–host RNA–RNA interactions, arising from digestion of the endosymbiont population, can result in a cost to host growth for breakdown of the endosymbiosis. Using the model facultative endosymbiosis between
Paramecium bursaria and
Chlorella spp., we demonstrate that this mechanism is dependent on the host RNA-interference (RNAi) system. We reveal through small RNA (sRNA) sequencing that endosymbiont-derived messenger RNA (mRNA) released upon endosymbiont digestion can be processed by the host RNAi system into 23-nt sRNA. We predict multiple regions of shared sequence identity between endosymbiont and host mRNA, and demonstrate through delivery of synthetic endosymbiont sRNA that exposure to these regions can knock down expression of complementary host genes, resulting in a cost to host growth. This process of host gene knockdown in response to endosymbiont-derived RNA processing by host RNAi factors, which we term “RNAi collisions,” represents a mechanism that can promote stability in a facultative eukaryote–eukaryote endosymbiosis. Specifically, by imposing a cost for breakdown of the endosymbiosis, endosymbiont–host RNA–RNA interactions may drive maintenance of the symbiosis across fluctuating ecological conditions.
