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Interactions between Drosophila and its natural yeast symbionts-Is Saccharomyces cerevisiae a good model for studying the fly-yeast relationship?

Hoang D, Kopp A, Chandler JA - PeerJ (2015)

Bottom Line: 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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Evolution and Ecology and Center for Population Biology, University of California , Davis, CA , USA ; Current affiliation: Program in Genomics of Differentiation, NIH/NICHD , Bethesda, MD , USA.

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.

No MeSH data available.


Related in: MedlinePlus

Yeast growth in vitro.Yeast growth as measured by optical density in a TECAN spectrophotometer. Hydrogen peroxide (H2O2) was added to mimic reactive oxygen species in the D. melanogaster intestine. The control curves (i.e., without H2O2) are drawn as solid lines and the H2O2 treatment as dotted lines. SC, S. cerevisiae; HO, H. occidentalis; HU, H. uvarum; SP, S. paradoxus; BN, B. naardenesis; DH, D. hansenii.
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fig-2: Yeast growth in vitro.Yeast growth as measured by optical density in a TECAN spectrophotometer. Hydrogen peroxide (H2O2) was added to mimic reactive oxygen species in the D. melanogaster intestine. The control curves (i.e., without H2O2) are drawn as solid lines and the H2O2 treatment as dotted lines. SC, S. cerevisiae; HO, H. occidentalis; HU, H. uvarum; SP, S. paradoxus; BN, B. naardenesis; DH, D. hansenii.

Mentions: Since intestinal reactive oxygen species are one potential factor limiting in vivo yeast growth (Ha et al., 2009), we tested yeast sensitivity to hydrogen peroxide (a generator of ROS) in vitro. Specifically, we measured yeast growth in the absence and presence of 0.5 mM hydrogen peroxide (H2O2). 1 mM H2O2 leads to approximately 50% survival in S. cerevisiae (Jamieson, 1992). One colony of each yeast species was added to individual glass test tubes containing four mL of liquid YPD media and shaken at 27 °C overnight. The following day, three replicates of each yeast was added into a 96 well plate. Each well contained 150 µL of liquid YPD media, 10 µL of mineral oil (to limit evaporation), and 10 µL of the liquid yeast culture. For the experiments testing ROS resistance, an additional 2 µL of H2O2 was added to each well, creating a final concentration of 0.5 mM H2O2. Optical density was measured every 30 min for three days using a TECAN spectrophotometer. The average for the three replicates is shown in Fig. 2. Because we did not standardize the amount of yeast cells at the start of the experiment, we are limiting our conclusions to those within strains, specifically the effect of H2O2 on growth. All raw data for the yeast growth experiments is available in Data S2.


Interactions between Drosophila and its natural yeast symbionts-Is Saccharomyces cerevisiae a good model for studying the fly-yeast relationship?

Hoang D, Kopp A, Chandler JA - PeerJ (2015)

Yeast growth in vitro.Yeast growth as measured by optical density in a TECAN spectrophotometer. Hydrogen peroxide (H2O2) was added to mimic reactive oxygen species in the D. melanogaster intestine. The control curves (i.e., without H2O2) are drawn as solid lines and the H2O2 treatment as dotted lines. SC, S. cerevisiae; HO, H. occidentalis; HU, H. uvarum; SP, S. paradoxus; BN, B. naardenesis; DH, D. hansenii.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
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getmorefigures.php?uid=PMC4556146&req=5

fig-2: Yeast growth in vitro.Yeast growth as measured by optical density in a TECAN spectrophotometer. Hydrogen peroxide (H2O2) was added to mimic reactive oxygen species in the D. melanogaster intestine. The control curves (i.e., without H2O2) are drawn as solid lines and the H2O2 treatment as dotted lines. SC, S. cerevisiae; HO, H. occidentalis; HU, H. uvarum; SP, S. paradoxus; BN, B. naardenesis; DH, D. hansenii.
Mentions: Since intestinal reactive oxygen species are one potential factor limiting in vivo yeast growth (Ha et al., 2009), we tested yeast sensitivity to hydrogen peroxide (a generator of ROS) in vitro. Specifically, we measured yeast growth in the absence and presence of 0.5 mM hydrogen peroxide (H2O2). 1 mM H2O2 leads to approximately 50% survival in S. cerevisiae (Jamieson, 1992). One colony of each yeast species was added to individual glass test tubes containing four mL of liquid YPD media and shaken at 27 °C overnight. The following day, three replicates of each yeast was added into a 96 well plate. Each well contained 150 µL of liquid YPD media, 10 µL of mineral oil (to limit evaporation), and 10 µL of the liquid yeast culture. For the experiments testing ROS resistance, an additional 2 µL of H2O2 was added to each well, creating a final concentration of 0.5 mM H2O2. Optical density was measured every 30 min for three days using a TECAN spectrophotometer. The average for the three replicates is shown in Fig. 2. Because we did not standardize the amount of yeast cells at the start of the experiment, we are limiting our conclusions to those within strains, specifically the effect of H2O2 on growth. All raw data for the yeast growth experiments is available in Data S2.

Bottom Line: 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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Evolution and Ecology and Center for Population Biology, University of California , Davis, CA , USA ; Current affiliation: Program in Genomics of Differentiation, NIH/NICHD , Bethesda, MD , USA.

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.

No MeSH data available.


Related in: MedlinePlus