An expansive internal chemosensory system in the insect abdomen implicates Gustatory Receptors in diverse aspects of interoception

Abstract

Taste and olfactory receptors are gatekeepers that convey chemical information about the external environment. Their role in chemosensory systems has been extensively studied in several model system, which established their role in triggering discrete behavioral as well as physiological responses related to feeding and social interactions. Over time, cases of chemoreceptors expressed internally in organs not linked to the external chemosensory systems of taste and olfaction have been reported. Here, we present the existence of a complex internal chemosensory system in the abdomen of Drosophila melanogaster. We show that the adult fruit fly harbors a complex internal chemosensory system, composed of about 80 to 100 abdominal chemosensory neurons (ACSNs) expressing approximately 20 different Gustatory receptor (Gr) genes, including all sugar receptor and several members of the less conserved bitter receptor genes. The cells expressing specific Gr genes are stereotypically arranged along the entire circumference of the abdominal body wall, in proximity of muscle and fat layers. The ACSN fall into at least nine different subtypes based on co-expression analysis, projection trajectories into the Abdominal Ganglion (AG) and location of cell somata. Identification of different subpopulation of ASCNs expressing discrete combinations of Gr genes indicates that these receptor complexes have new, previously not considered roles in interoception, including monitoring of different nutrients, detection of cell metabolites and their byproducts and chemicals associated with pathogens.