Yeast-derived volatiles orchestrate an insect-yeast mutualism with oriental armyworm moths

Abstract

Interactions among insects, plants, and microorganisms are fundamental to ecosystem dynamics, with floral nectar and pollen serving as key resources for various organisms. Yeasts, such as Metschnikowia reukaufii, commonly found in nectar, influence nectarial attraction through volatile compounds (VOCs), yet the underlying biological mechanisms remain elusive. Here, we show that isoamyl alcohol, a prominent yeast VOC, attracts oriental armyworm moths (Mythimna separata) to pollen-rich, yeast-fermented nectar. In a series of electrophysiological and behavioral assays, we show that isoamyl alcohol activates a single class of highly specific olfactory sensory neurons expressing the olfactory receptor MsepOR8. In the moth antennal lobe, these neurons target the AM2 glomerulus, which responds to isoamyl alcohol. Genetic disruption of MsepOR8 leads to complete abolition of both physiological and behavioral responses to isoamyl alcohol, resulting in an impaired ability to locate nectar sources. Moreover, we show that isoamyl alcohol-induced foraging behavior fosters a mutualistic relationship between yeast and moths to some extent, enhancing yeast dispersal and increasing moth reproductive success. Our results unveil a highly specific mechanism by which a yeast-derived VOC facilitates insect-yeast mutualism, providing insights into insect-microbe interactions within pollination ecosystems.