Yeast Volatomes Differentially Affect Larval Feeding in an Insect Herbivore

Yeasts form mutualistic interactions with insects. Hallmarks of this interaction include provision of essential nutrients, while insects facilitate yeast dispersal and growth on plant substrates. A phylogenetically ancient chemical dialogue coordinates this interaction, where the vocabulary, the volatile chemicals that mediate the insect response, remains largely unknown. Here, we used gas chromatography-mass spectrometry, followed by hierarchical cluster and orthogonal partial least-squares discriminant analyses, to profile the volatomes of six Metschnikowia spp., Cryptococcus nemorosus, and brewer's yeast (Saccharomyces cerevisiae). The yeasts, which are all found in association with insects feeding on foliage or fruit, emit characteristic, species-specific volatile blends that reflect the phylogenetic context. Species specificity of these volatome profiles aligned with differential feeding of cotton leafworm (Spodoprera littoralis) larvae on these yeasts. Bioactivity correlates with yeast ecology; phylloplane species elicited a stronger response than fruit yeasts, and larval discrimination may provide a mechanism for establishment of insect-yeast associations. The yeast volatomes contained a suite of insect attractants known from plant and especially floral headspace, including (Z)-hexenyl acetate, ethyl (2E,4Z)-deca-2,4-dienoate (pear ester), (3E)-4,8-dimethylnona-1,3,7-triene (DMNT), linalool, alpha-terpineol, beta-myrcene, or (E,E)-alpha-farnesene. A wide overlap of yeast and plant volatiles, notably floral scents, further emphasizes the prominent role of yeasts in plant-microbe-insect relationships, including pollination. The knowledge of insect-yeast interactions can be readily brought to practical application, as live yeasts or yeast metabolites mediating insect attraction provide an ample tool-box for the development of sustainable insect management. IMPORTANCE Yeasts interface insect herbivores with their food plants. Communication depends on volatile metabolites, and decoding this chemical dialogue is key to understanding the ecology of insect-yeast interactions. This study explores the volatomes of eight yeast species which have been isolated from foliage, from flowers or fruit, and from plant-feeding insects. These yeasts each release a rich bouquet of volatile metabolites, including a suite of known insect attractants from plant and floral scent. This overlap underlines the phylogenetic dimension of insect-yeast associations, which according to the fossil record long predate the appearance of flowering plants. Volatome composition is characteristic for each species, aligns with yeast taxonomy, and is further reflected by a differential behavioral response of cotton leafworm larvae, which naturally feed on foliage of a wide spectrum of broad-leaved plants. Larval discrimination may establish and maintain associations with yeasts and is also a substrate for designing sustainable insect management techniques.