Yeast communities of diverse Drosophila species: comparison of two symbiont groups in the same hosts

Abstract

The combination of ecological diversity with genetic and experimental tractability makes Drosophila a powerful model for the study of animal-associated microbial communities. Despite the known importance of yeasts in Drosophila physiology, behavior, and fitness, most recent work has focused on Drosophila-bacterial interactions. In order to get a more complete understanding of the Drosophila microbiome, we characterized the yeast communities associated with different Drosophila species collected around the world. We focused on the phylum Ascomycota because it constitutes the vast majority of the Drosophila-associated yeasts. Our sampling strategy allowed us to compare the distribution and structure of the yeast and bacterial communities in the same host populations. We show that yeast communities are dominated by a small number of abundant taxa, that the same yeast lineages are associated with different host species and populations, and that host diet has a greater effect than host species on yeast community composition. These patterns closely parallel those observed in Drosophila bacterial communities. However, we do not detect a significant correlation between the yeast and bacterial communities of the same host populations. Comparative analysis of different symbiont groups provides a more comprehensive picture of host-microbe interactions. Future work on the role of symbiont communities in animal physiology, ecological adaptation, and evolution would benefit from a similarly holistic approach.

Fig 1

Comparison of yeast and bacterial rarefaction curves. All calculations were performed using mothur (7). OTUs were defined at the 3% divergence threshold using the average neighbor-clustering algorithm. Only the 12 populations for which both yeast and bacterial data (3) are available are shown. Library identifiers are given in Table 1. Rarefaction curves for populations MEC, NNS, and SPP are shown in Fig. S1 in the supplemental material. (A) Yeast rarefaction curves (this study). (B) Bacterial rarefaction curves (11).

Fig 2

Principal component analysis of yeast communities. (A and B) A representative sequence from each OTU was generated using mothur (67), and a tree of the sequences was generated with FastTree (57) using Amanita muscaria as an outgroup. Principal component analysis was done with the FastUniFrac Web application (26) using both the weighted (A) and the unweighted (B) algorithms. (C and D) β-Diversity principal component analysis was performed in QIIME (9) for both the abundance-based (C) and binary (D) Jaccard metrics. For clarity, overlapping data points were moved; the arrows indicate their true positions. Library identifiers are given in Table 1.

Fig 3

Plot showing Procrustes analyses of transformed PCAs of yeast and bacterial communities. Each pair of dots connected by an edge represents a paired set of yeast and bacterial data points from the same host population. The gray half of the edge is connected to the yeast data point, while the red half is connected to the bacterial data point. Note that the yeast and bacterial communities from the same hosts are no closer than a random pair of yeast and bacterial communities. The plot represents weighted, normalized UniFrac data (P = 0.076). The KiNG data file for this and the other comparisons (Table 3) is available through BioTorrents (http://www.biotorrents.net/details.php?id=263).