Loss of Vitellogenin Receptor Function Results in Yolk Depletion, Virome Expansion and Reduced Bacterial Load Within the Oocytes of Rhodnius prolixus
The vitellogenin receptor (VgR) mediates yolk protein uptake during oogenesis and is essential for embryogenesis in oviparous species. Here we characterize the single Rhodnius prolixus VgR isoform and uncover an unexpected role in microbial regulation within the reproductive system. The receptor displays a conserved LDLR-like structure and is highly expressed in early oocytes. RNAi-mediated VgR silencing caused defective yolk granule biogenesis, leading to the accumulation of the main yolk protein precursors, Vg and RHBP, in the hemolymph, yet oviposition and fertilization proceeded normally. The resulting eggs were yolk-depleted and non-viable. Remarkably, VgR knockdown reduced bacterial 16S rRNA levels in oocytes while promoting the expansion of several members of the core virome, a phenotype not reproduced by Vg silencing. Neither purified Vg nor changes in immune (defensin) or RNA interference pathways explained the microbial shifts. These findings indicate that VgR governs not only yolk endocytosis but also the trafficking of microbial components into developing oocytes. We propose that VgR contributes to the linking of yolk endocytic dynamics and microbial homeostasis, influencing the balance of microbial components within developing oocytes. This connection broadens the functional scope of the VgR and provides new insight into how vertical transmission processes are shaped in this major Chagas disease vector. Author summaryEgg-laying animals must load their eggs with enough nutrients to support early development. In insects, this process depends on a receptor that brings yolk proteins into the growing egg. Here, we studied this receptor in Rhodnius prolixus, a major vector of Chagas disease, and uncovered an unexpected link between yolk uptake and the microorganisms that enter the egg. When we blocked the receptor, females continued to produce and lay eggs, but these eggs failed to accumulate yolk and could not support embryonic development. Strikingly, the absence of the receptor also shifted the microbial community inside the oocyte: bacterial levels dropped, while several viruses expanded. These changes did not result from differences in yolk proteins, immune activation, or direct antimicrobial effects, indicating that the receptor itself influences microbial entry or persistence in the egg. Our findings reveal that this yolk receptor plays a dual role, providing nutrients and shaping the microbial community that is passed from mother to offspring. This work highlights an unrecognized layer of interaction between reproduction and microbial transmission in an important disease vector, offering new perspectives for understanding and potentially disrupting vertical transmission pathways.