Proteomic Characterization of Drosophila melanogaster Proboscis

SIMPLE SUMMARY: Insects use chemical signals to locate food, interact with their environment, and for social communication. More precisely, the peripheral sensory olfactory and gustatory systems allow the detection of chemical signals coming from the environment. Volatile or sapid molecules enter the sensory organs and are transported by specialized proteins through the internal aqueous phase to the chemosensory receptors. We used proteomic analysis to identify the soluble proteins in the proboscis, an organ that is part of the gustatory system of Drosophila melanogaster. A total of 586 proteins were identified, and 19 proteins were used for further analysis. We identified two proteins implicated in the transport of molecules, such as the odorant-binding proteins OBP19d and OBP56d. Interestingly, OBP56d showed higher expression in female Drosophila, whereas OBP19d showed no sex differences. We also identified proteins implicated in the metabolism of chemicals. Other molecules, such as pheromones, were detected by the proboscis, but our analysis did not identify any of them. In conclusion, we found that the proboscis was involved in the detection of many classes of molecules that can impact feeding and sexual behavior in Drosophila melanogaster. ABSTRACT: Drosophila melanogaster flies use their proboscis to taste and distinguish edible compounds from toxic compounds. With their proboscis, flies can detect sex pheromones at a close distance or by contact. Most of the known proteins associated with probosci’s detection belong to gustatory receptor families. To extend our knowledge of the proboscis-taste proteins involved in chemo-detection, we used a proteomic approach to identify soluble proteins from Drosophila females and males. This investigation, performed with hundreds of dissected proboscises, was initiated by the chromatographic separation of tryptic peptides, followed by tandem mass spectrometry, allowing for femtomole detection sensitivity. We found 586 proteins, including enzymes, that are involved in intermediary metabolism and proteins dedicated to various functions, such as nucleic acid metabolism, ion transport, immunity, digestion, and organ development. Among 60 proteins potentially involved in chemosensory detection, we identified two odorant-binding proteins (OBPs), i.e., OBP56d (which showed much higher expression in females than in males) and OBP19d. Because OBP56d was also reported to be more highly expressed in the antennae of females, this protein can be involved in the detection of both volatile and contact male pheromone(s). Our proteomic study paves the way to better understand the complex role of Drosophila proboscis in the chemical detection of food and pheromonal compounds.