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Ecology in the laboratory: the molecules that shape the ecological relationship between D. melanogaster and S. cerevisiae

Abstract

Drosophila melanogaster and Saccharomyces cerevisiae, two model systems of molecular biology, interact in the wild, but the chemical basis of this interaction is largely unknown. This thesis details an effort to understand the molecular basis of this ecological co-localization.

Results:

While screening a collection of wild and laboratory yeast strains for their ability to attract adult D. melanogaster (Raleigh 437), I noticed a large difference in fly preference for two nearly isogenic strains of S. cerevisiae, BY4741 and BY4742. Using standard genetic analyses, I tracked the difference in preference to lack of mitochondria in BY4742. I used gas chromatography coupled with mass spectrometry (GC-MS) to examine the volatile compounds produced by BY4741 and the mitochondria-deficient BY4742, and found that they differed in their production of many known fly attractants, including ethyl hexanoate and ethyl octanoate, which were produced at much higher levels in yeast strains with mitochondria during aerobic fermentation, a metabolic strategy that distinguishes S. cerevisiae from most other microbes.

Through a detailed investigation of the volatile profiles and RNA expression patterns produced by yeast under multiple nutritional scenarios, I determined that the production of ethyl hexanoate and ethyl octanoate during aerobic fermentation depends on the level and type of nitrogen present in the substrate. Fermentative growth on nitrogen-limited substrates requires mitochondrial engagement and the metabolic configuration employed by S. cerevisiae to contend with this nutritional scenario results in the production of these ester attractants. This nutritional scenario – high sugar but limited nitrogen – matches the composition of fruit, the natural co-localization environment for flies and yeast, suggesting that these volatiles are ecologically relevant cues for D. melanogaster.

D. melanogaster sense ethyl hexanoate and ethyl octanoate via the odorant receptor genes Or22a and Or22b. A single gene version of this locus, which is a chimera of the two ancestral copies, is segregating in natural D. melanogaster populations. I found that D. melanogaster lines harboring the chimeric locus (including Raleigh 437) show more robust preference for ethyl hexanoate and ethyl octanoate-producing S. cerevisiae cultures. This provides an ecological basis, and possibly selective advantage, for the maintenance of this allele in D. melanogaster.

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