Abstract
Yeasts play an important role in the biology of the fruit fly, Drosophila melanogaster. In addition to being a valuable source of nutrition, yeasts affect D. melanogaster behavior and interact with the host immune system. Most experiments investigating the role of yeasts in D. melanogaster biology use the baker’s yeast, Saccharomyces cerevisiae. However, S. cerevisiae is rarely found with natural populations of D. melanogaster or other Drosophila species. Moreover, the strain of S. cerevisiae used most often in D. melanogaster experiments is a commercially and industrially important strain that, to the best of our knowledge, was not isolated from flies. Since disrupting natural host–microbe interactions can have profound effects on host biology, the results from D. melanogaster–S. cerevisiae laboratory experiments may not be fully representative of host–microbe interactions in nature. In this study, we explore the D. melanogaster-yeast relationship using five different strains of yeast that were isolated from wild Drosophila populations. Ingested live yeasts have variable persistence in the D. melanogaster gastrointestinal tract. For example, Hanseniaspora occidentalis persists relative to S. cerevisiae, while Brettanomyces naardenensis is removed. Despite these differences in persistence relative to S. cerevisiae, we find that all yeasts decrease in total abundance over time. Reactive oxygen species (ROS) are an important component of the D. melanogaster anti-microbial response and can inhibit S. cerevisiae growth in the intestine. To determine if sensitivity to ROS explains the differences in yeast persistence, we measured yeast growth in the presence and absence of hydrogen peroxide. We find that B. naardenesis is completely inhibited by hydrogen peroxide, while H. occidentalis is not, which is consistent with yeast sensitivity to ROS affecting persistence within the D. melanogaster gastrointestinal tract. We also compared the feeding preference of D. melanogaster when given the choice between a naturally associated yeast and S. cerevisiae. We do not find a correlation between preferred yeasts and those that persist in the intestine. Notably, in no instances is S. cerevisiae preferred over the naturally associated strains. Overall, our results show that D. melanogaster-yeast interactions are more complex than might be revealed in experiments that use only S. cerevisiae. We propose that future research utilize other yeasts, and especially those that are naturally associated with Drosophila, to more fully understand the role of yeasts in Drosophila biology. Since the genetic basis of host–microbe interactions is shared across taxa and since many of these genes are initially discovered in D. melanogaster, a more realistic fly-yeast model system will benefit our understanding of host–microbe interactions throughout the animal kingdom.
Highlights
Microbes are vastly important to an animal’s biology (McFall-Ngai et al, 2013)
Yeast strains naturally associated with Drosophila differ in their ability to persist in the D. melanogaster gastrointestinal tract (Fig. 1, Fig. S2 and Table 2)
There is no trend for persistence between the naturally associated yeasts and S. cerevisiae: One yeast persists at all time points (H. occidentalis), one yeast is removed at all time points (B. naardenensis), and the remaining yeasts are not consistent at different time points
Summary
Microbes are vastly important to an animal’s biology (McFall-Ngai et al, 2013). Animal-associated microbes, collectively called the microbiota, help stimulate immunity, assist in nutrient acquisition, and help maintain host homeostasis (Hooper & Macpherson, 2010; Tremaroli & Backhed, 2012; Sommer & Backhed, 2013). Many members of the D. melanogaster microbiota can be cultured using standard media under aerobic conditions, which facilitates experimental studies that associate specific microbes with their hosts (Newell et al, 2014; Chaston, Newell & Douglas, 2014). Combine this simple and culturable microbiota with well-developed genetic tools and well-described immunity pathways, such as the NF-κB, Toll, and Imd pathways (Lemaitre & Hoffmann, 2007), and D. melanogaster is a powerful model to understand host–microbe interactions
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