Olfactory proxy detection of dietary antioxidants in Drosophila

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.

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.

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.