A Secreted RNA Binding Protein Forms RNA-Stabilizing Granules in the Honeybee Royal Jelly

RNA flow between organisms has been documented within and among different kingdoms of life. Recently, we demonstrated horizontal RNA transfer between honeybees involving secretion and ingestion of worker and royal jellies. However, how the jelly facilitates transfer of RNA is still unknown. Here, we show that worker and royal jellies harbor robust RNA-binding activity. We report that a highly abundant jelly component, major royal jelly protein 3 (MRJP-3), acts as an extracellular non-sequence-specific RNA-aggregating factor. Multivalent RNA binding stimulates higher-order assembly of MRJP-3 into extracellular ribonucleoprotein granules that protect RNA from degradation and enhance RNA bioavailability. These findings reveal that honeybees have evolved a secreted dietary RNA-binding factor to concentrate, stabilize, and share RNA among individuals. Our work identifies high-order ribonucleoprotein assemblies with functions outside cells and organisms. [Display omitted] •Worker and royal jellies harbor robust RNA-binding activity•Major royal jelly protein 3 (MRJP-3) is the dietary RNA-binding factor•RNA stimulates higher-order assembly of MRJP-3 into extracellular RNP granules•MRJP-3 granules concentrate, stabilize, and enhance environmental RNA bioavailability Honeybees share RNA between individuals through secretion and ingestion of worker and royal jellies. Maori et al. identify a jelly factor, MRJP-3, that forms extracellular ribonucleoprotein granules that concentrate, protect, and enhance RNA uptake. They propose that MRJP-3 facilitates RNA transfer that drives social immunity and signaling among bees.