The proteomic content of Varroa destructor gut varies according to the developmental stage of its host.

The nutritional physiology of parasites is often overlooked although it is at the basis of host-parasite interactions. In the case of Varroa destructor, one of the major pests of the Western honey bee Apis mellifera, the nature of molecules and tissues ingested by the parasite is still not completely understood. Here, the V. destructor feeding biology was explored through artificial feeding, dissection of the mite's gut and proteomic analyses. More specifically, the proteome of guts extracted from starved mites and honey bee-fed mites was compared to highlight both the parasite proteins likely involved in food processing and the honey bee proteins actually ingested by the mite. We could identify 25 V. destructor candidate proteins likely involved in the parasite digestion. As the host developmental stages infested by the mite are diverse, we also focused on the identity and on the origin of honey bee proteins ingested by the mite when it feeds on larvae, pupae or adults. We highlighted profiles of consumed honey bee proteins and their variations throughout the V. destructor life cycle. These variations matched the ones observed in the honey bee hemolymph, showing that this tissue is an important part of the mite's diet. Based on the variations of abundance of the most consumed honey bee proteins and on their functions, the potential implication of these key candidate nutrients in V. destructor reproduction is also discussed. Author summary: Varroa destructor is one of the major parasitic pests in modern beekeeping worldwide. Since it shifted host from Eastern to Western honey bees, it was shown to weaken colonies by feeding on both immature and adult stages while transmitting several deadly viruses in the process. Nutrition, an overlooked aspect of parasite biology, is thus a key to comprehend the V. destructor life cycle and its impacts on its honey bee host. We explored the feeding physiology of this ectoparasite by analysing the protein content of its isolated gut to compare it with the protein composition of the honey bee tissues ingested. We highlighted several mite proteins probably involved in digestion and many honey bee derived proteins acquired during the feeding. Honey bee hemolymph is an important part of the mite's diet although the diet could vary throughout the cycle, especially when mites feed on adult bees. The abundance of the most regularly ingested honey bee proteins such as Vitellogenin or Hexamerin varies throughout the bee development and could directly impact the parasite physiology. The analysis and identification of key proteins required for the mite's survival and reproduction will pave the way for the development of more specific control strategies. [ABSTRACT FROM AUTHOR]