Can yeast (S. cerevisiae) metabolic volatiles provide polymorphic signaling?

Abstract

Chemical signaling between organisms is a ubiquitous and evolutionarily dynamic process that helps to ensure mate recognition, location of nutrients, avoidance of toxins, and social cooperation. Evolutionary changes in chemical communication systems progress through natural variation within the organism generating the signal as well as the responding individuals. A promising yet poorly understood system with which to probe the importance of this variation exists between D. melanogaster and S. cerevisiae. D. melanogaster relies on yeast for nutrients, while also serving as a vector for yeast cell dispersal. Both are outstanding genetic and genomic models, with Drosophila also serving as a preeminent model for sensory neurobiology. To help develop these two genetic models as an ecological model, we have tested if - and to what extent - S. cerevisiae is capable of producing polymorphic signaling through variation in metabolic volatiles. We have carried out a chemical phenotyping experiment for 14 diverse accessions within a common garden random block design. Leveraging genomic sequences for 11 of the accessions, we ensured a genetically broad sample and tested for phylogenetic signal arising from phenotypic dataset. Our results demonstrate that significant quantitative differences for volatile blends do exist among S. cerevisiae accessions. Of particular ecological relevance, the compounds driving the blend differences (acetoin, 2-phenyl ethanol and 3-methyl-1-butanol) are known ligands for D. melanogasters chemosensory receptors, and are related to sensory behaviors. Though unable to correlate the genetic and volatile measurements, our data point clear ways forward for behavioral assays aimed at understanding the implications of this variation.

Figure 1. Genetic relationships between the 11 yeast accessions for which genomic sequence is available.

Left: Inferred proportion of ancestry estimated for 2–5 genetic clusters. Right: A Neighbor Joining tree for the same yeast accessions. All branches have bootstrap values greater than 95% except for the two marked with red lines (upper branch = 55.8, lower branch = 74.9). Color-coding on tree tips indicate the grouping of the strains according to Table 1.

Figure 2. Summaries for the ordination of non-polar GC-MS volatile data for all 14 yeast accessions (see legend inset).

A) Principal Components Analysis (PCA) on the 8 core volatiles, showing the compounds that loaded most highly on the first three significant factors (PC1-3). B) Multidimensional Scaling (MDS) of all 32 volatiles, showing the compounds that frequently explained differences between the accessions showing greatest differences along specific axes (MD1-3) in Cartesian scent space (e.g. accessions 1888 vs. 2094 along MDS2, explained largely by acetoin and isobutyric acid); see also Table S2. Note the similarity between compounds annotated with MDS axes in panel B and PC factors in panel A.