Insect—symbiont gene expression in the midgut bacteriocytes of a blood-sucking parasite

Background. Animals interact with a diverse array of both beneficial and detrimental microorganisms. These interactions sometimes spark obligate symbioses where the host depends on beneficial bacteria for survival and reproduction. In insects, these obligate symbioses in many cases allow feeding on nutritionally unbalanced diets such as plant sap and vertebrate blood. It is, however, still not clear how are these obligate intracellular symbioses maintained at the cellular level for up to several hundred million years. Exact mechanisms driving host-symbiont interactions are only understood for a handful of model species and data on blood-feeding hosts with intracellular bacteria are particularly scarce.Results. Here, we analyzed interactions at the symbiotic interfaces of an obligately blood-sucking parasite of sheep, the louse fly Melophagus ovinus. We assembled a reference transcriptome from a male and female individual and used RNA-Seq with five biological replicates to compare expression in the midgut cells housing bacteria to the rest of the gut (foregut-hindgut). We focused on nutritional and immunity interactions between the insect host and its obligate symbiont Arsenophonus melophagi, and also generated lower-coverage data for three facultative bacterial symbionts (Sodalis melophagi, Bartonella melophagi, and Wolbachia sp.) and one facultative eukaryote Trypanosoma melophagium. We found strong evidence for the importance of zinc in the system likely caused by symbionts using zinc-dependent proteases when acquiring amino acids, and for likely different immunity mechanisms controlling the symbionts than in closely related tsetse flies.Conclusions. Our results show that cellular and nutritional interactions between this blood-sucking insect and its symbionts are less intimate than what was previously found in some (but not all) plant-sap sucking insects such as aphids, psyllids, whiteflies, and mealybugs. This finding is likely interconnected to several features observed in symbionts in blood-sucking arthropods, particularly their midgut intracellular localization (as opposed to being localized in truly specialized bacteriocytes), intracytoplasmic presence (as opposed to having an outermost host-derived 'symbiosomal' membrane), less severe genome reduction, and relatively recent associations caused by frequent evolutionary losses and replacements.