The Fungal Aroma Gene ATF1 Promotes Dispersal of Yeast Cells through Insect Vectors

• Published in: Cell reports (Cambridge) Vol. 9; no. 2; pp. 425 - 432
• Main Authors: Christiaens, Joaquin F., Franco, Luis M., Cools, Tanne L., De Meester, Luc, Michiels, Jan, Wenseleers, Tom, Hassan, Bassem A., Yaksi, Emre, Verstrepen, Kevin J.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 23.10.2014; Elsevier
• Subjects: Acetates - pharmacology; Animals; Arthropod Antennae - drug effects; Arthropod Antennae - physiology; Drosophila - drug effects; Drosophila - physiology; Gene Deletion; Odorants; Proteins - genetics; Saccharomyces cerevisiae - chemistry; Saccharomyces cerevisiae - genetics; Smell
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2014.09.009

Yeast cells produce various volatile metabolites that are key contributors to the pleasing fruity and flowery aroma of fermented beverages. Several of these fruity metabolites, including isoamyl acetate and ethyl acetate, are produced by a dedicated enzyme, the alcohol acetyl transferase Atf1. However, despite much research, the physiological role of acetate ester formation in yeast remains unknown. Using a combination of molecular biology, neurobiology, and behavioral tests, we demonstrate that deletion of ATF1 alters the olfactory response in the antennal lobe of fruit flies that feed on yeast cells. The flies are much less attracted to the mutant yeast cells, and this in turn results in reduced dispersal of the mutant yeast cells by the flies. Together, our results uncover the molecular details of an intriguing aroma-based communication and mutualism between microbes and their insect vectors. Similar mechanisms may exist in other microbes, including microbes on flowering plants and pathogens. [Display omitted] •The S. cerevisiae ATF1 gene controls the production of volatile acetate esters•Aroma of ATF1 mutants elicits different neuronal activity in the fly antennal lobe•Flies are significantly more attracted to wild-type yeast than to atf1-null mutants•Addition of isoamyl acetate and ethyl acetate restores attraction of Drosophila Yeast cells produce several different volatile acetate esters. Whereas these fruity aroma compounds are key contributors to the pleasing aroma of fermented beverages like beer and wine, their physiological role for the yeast cells that produce them remains unknown. Christiaens et al. show that two acetate esters, ethyl acetate and isoamyl acetate, help to attract fruit flies that serve as vectors that promote dispersal of the yeast cells. Deletion of the yeast ATF1 gene, encoding a key acetate ester synthase, drastically reduces Drosophila attraction and therefore limits yeast dispersal.