Microbial Odorant Detection Guides Drosophila Parasitoids Seeking Hosts in Fermenting Fruits.

While parasitoid wasps have been extensively reported to rely on plant-derived volatiles for host location, host habitats such as fermented fruits often harbor not only plants but also diverse microbial communities that are essential for hosts. This raises the question of whether parasitoid wasps exploit microbial volatiles for host location. Although some ecological evidence exists for such microbe-mediated attraction, the underlying molecular mechanisms remain largely unknown. Here, using the Leptopilina boulardi-Drosophila melanogaster system, it is reported that yeast (a ubiquitous microorganism in host habitats) attracts both Drosophila hosts and L. boulardi female parasitoids. Four yeast-derived ethyl ester volatiles that elicit olfactory attraction in female wasps are identified. Through integrated genomic and transcriptomic analyses, the complete odorant receptor repertoire of L. boulardi is characterized, and two female-biased receptors (LbouOR167 and LbouOR136) are identified as necessary for the detection of these ethyl esters. Structural and functional analyses revealed that a conserved residue, Leu159, in both receptors is essential for odorant ligand binding. These findings uncover a microbial volatile-mediated mechanism underlying parasitoid host-seeking behavior and provide novel insights into the chemical ecology of a four-party interaction involving fruit, fungi, Drosophila hosts, and their parasitoid wasps.