A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila.

Flies, like all animals, need to find suitable and safe food. Because the principal food source for Drosophila melanogaster is yeast growing on fermenting fruit, flies need to distinguish fruit with safe yeast from yeast covered with toxic microbes. We identify a functionally segregated olfactory circuit in flies that is activated exclusively by geosmin. This microbial odorant constitutes an ecologically relevant stimulus that alerts flies to the presence of harmful microbes. Geosmin activates only a single class of sensory neurons expressing the olfactory receptor Or56a. These neurons target the DA2 glomerulus and connect to projection neurons that respond exclusively to geosmin. Activation of DA2 is sufficient and necessary for aversion, overrides input from other olfactory pathways, and inhibits positive chemotaxis, oviposition, and feeding. The geosmin detection system is a conserved feature in the genus Drosophila that provides flies with a sensitive, specific means of identifying unsuitable feeding and breeding sites.

Olfactory channels associated with the Drosophila maxillary palp mediate short- and long-range attraction.

The vinegar fly Drosophila melanogaster is equipped with two peripheral olfactory organs, antenna and maxillary palp. The antenna is involved in finding food, oviposition sites and mates. However, the functional significance of the maxillary palp remained unknown. Here, we screened the olfactory sensory neurons of the maxillary palp (MP-OSNs) using a large number of natural odor extracts to identify novel ligands for each MP-OSN type. We found that each type is the sole or the primary detector for a specific compound, and detects these compounds with high sensitivity. We next dissected the contribution of MP-OSNs to behaviors evoked by their key ligands and found that MP-OSNs mediate short- and long-range attraction. Furthermore, the organization, detection and olfactory receptor (Or) genes of MP-OSNs are conserved in the agricultural pest D. suzukii. The novel short and long-range attractants could potentially be used in integrated pest management (IPM) programs of this pest species.

Olfactory proxy detection of dietary antioxidants in Drosophila.

BACKGROUND: Dietary antioxidants play an important role in preventing oxidative stress. Whether animals in search of food or brood sites are able to judge the antioxidant content, and if so actively seek out resources with enriched antioxidant content, remains unclear. RESULTS: We show here that the vinegar fly Drosophila melanogaster detects the presence of hydroxycinnamic acids (HCAs)-potent dietary antioxidants abundant in fruit-via olfactory cues. Flies are unable to smell HCAs directly but are equipped with dedicated olfactory sensory neurons detecting yeast-produced ethylphenols that are exclusively derived from HCAs. These neurons are housed on the maxillary palps, express the odorant receptor Or71a, and are necessary and sufficient for proxy detection of HCAs. Activation of these neurons in adult flies induces positive chemotaxis, oviposition, and increased feeding. We further demonstrate that fly larvae also seek out yeast enriched with HCAs and that larvae use the same ethylphenol cues as the adults but rely for detection upon a larval unique odorant receptor (Or94b), which is co-expressed with a receptor (Or94a) detecting a general yeast volatile. We also show that the ethylphenols act as reliable cues for the presence of dietary antioxidants, as these volatiles are produced--upon supplementation of HCAs--by a wide range of yeasts known to be consumed by flies. CONCLUSIONS: For flies, dietary antioxidants are presumably important to counteract acute oxidative stress induced by consumption or by infection by entomopathogenic microorganisms. The ethylphenol pathway described here adds another layer to the fly's defensive arsenal against toxic microbes.

Decoding odor quality and intensity in the Drosophila brain.

To internally reflect the sensory environment, animals create neural maps encoding the external stimulus space. From that primary neural code relevant information has to be extracted for accurate navigation. We analyzed how different odor features such as hedonic valence and intensity are functionally integrated in the lateral horn (LH) of the vinegar fly, Drosophila melanogaster. We characterized an olfactory-processing pathway, comprised of inhibitory projection neurons (iPNs) that target the LH exclusively, at morphological, functional and behavioral levels. We demonstrate that iPNs are subdivided into two morphological groups encoding positive hedonic valence or intensity information and conveying these features into separate domains in the LH. Silencing iPNs severely diminished flies' attraction behavior. Moreover, functional imaging disclosed a LH region tuned to repulsive odors comprised exclusively of third-order neurons. We provide evidence for a feature-based map in the LH, and elucidate its role as the center for integrating behaviorally relevant olfactory information.

The CCHamide 1 receptor modulates sensory perception and olfactory behavior in starved Drosophila.

The olfactory response of the vinegar fly Drosophila melanogaster to food odor is modulated by starvation. Here we show that this modulation is not restricted to food odors and their detecting sensory neurons but rather increases the behavioral response to odors as different as food odors, repellents and pheromones. The increased behavioral responsiveness is paralleled by an increased physiological sensitivity of sensory neurons regardless whether they express olfactory or ionotropic receptors and regardless whether they are housed in basiconic, coeloconic, or trichoid sensilla. Silencing several genes that become up-regulated under starvation confirmed the involvement of the short neuropeptide f receptor in the starvation effect. In addition it revealed that the CCHamide-1 receptor is another important factor governing starvation-induced olfactory modifications.