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

Abstract

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. ; This work was supported by Cancer Research UK (C13474/A18583 and C6946/A14492) and the Wellcome Trust (104640/Z/14/Z and 092096/Z/10/Z) to K.L.M.R, A.S., and E.A.M.; Cancer Research UK (C57233/A22356) to C.-C.L. and J.E.L.; Science without Borders doctorate scholarship (205589/2014-6; CNPq, Brazilian Federal Government) to I.C.N.; a Marie Curie Intra-European Fellowship for Career Development (PIEF-GA-2010-274406); and a Leo Baeck Scholarship and Herchel Smith Postdoctoral Fellowship (XXACC_AFGLTRB2) to E.M.