Microbiota Influences Fitness and Timing of Reproduction in the Fruit Fly Drosophila melanogaster

Matthews, Melinda K; Malcolm, Jaanna; Chaston, John M.

doi:10.1128/spectrum.00034-21

Cited by 8 publications

(9 citation statements)

References 48 publications

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“…The finding that male and female flies bore comparable bacterial loads following frequent transfer to sterile diets suggests that the persistent microorganisms may occupy similar spaces and niches between the two sexes, at least for these tested strains. We focused on just one sex in our subsequent assays and elected to study female flies, in part to make our results comparable with other analyses that measured life history traits of mono-associated females flies (5-7). Overall, these results confirm that our assay allowed us to detect a range of persistence phenotypes by different bacterial strains that did not vary significantly with the sex of the flies.…”

Section: Resultsmentioning

confidence: 99%

“…One recent area of study that has gained attention in relation to D. melanogaster is that of microbiome studies. In D. melanogaster the microbiota can influence diverse D. melanogaster phenotypes and behaviors (2)(3)(4), including life history traits like fecundity (5), lifespan (6), and starvation resistance (7). The D. melanogaster gut microbiota resides primarily in the foregut and crop of the fly and is well characterized, usually comprising fewer than 100 bacterial taxa and numerically dominated by fewer than 10 taxa that are usually from the acetic acid bacteria, lactic acid bacteria, and enterobacteria (2,(8)(9)(10).…”

Section: Introductionmentioning

confidence: 99%

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Flagellar genes are associated with the colonization persistence phenotype of theDrosophila melanogastermicrobiota

Chaston

Morgan

2022

Preprint

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In this work we use Drosophila melanogaster as a model to identify bacterial genes necessary for bacteria to colonize their hosts independent of the bulk flow of diet. Early work on this model system established that dietary replenishment drives the composition of the D. melanogaster gut microbiota, and subsequent research has shown that some bacterial strains can stably colonize, or persist with, the fly independent of dietary replenishment. Here we reveal transposon insertions in specific bacterial genes that influence the bacterial colonization persistence phenotype by using a gene association approach. We initially established that different bacterial strains persist at varying levels, independent of dietary replenishment. We then repeated the analysis with an expanded panel of bacterial strains and performed a metagenome wide association (MGWA) to identify distinct bacterial genes that are significantly correlated with the colonization level of persistent bacterial strains. Based on the MGWA, we tested if 44 bacterial transposon insertion mutants from 6 gene categories affect bacterial persistence with the flies. We identified that transposon insertions in four flagellar genes, one urea carboxylase gene, one phosphatidyl inositol gene, one bacterial secretion gene, and one antimicrobial peptide (AMP) resistance gene each significantly influenced the colonization of an Acetobacter fabarum strain with D. melanogaster. Follow-up experiments revealed that each flagellar mutant was non-motile, even though the wild-type strain was motile. Taken together, these results reveal transposon insertions in specific bacterial genes, including motility genes, are necessary for at least one member of the fly microbiota to persistently colonize the fly.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Flagellar genes are associated with the colonization persistence phenotype of theDrosophila melanogastermicrobiota

Chaston

Morgan

2022

Preprint

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“…increase the lifespan of D. melanogaster, but not the female fecundity (Gould et al, 2018), and environmental factors most likely influence which strains are the most beneficial (Matthews et al, 2021). D. suzukii is attracted to volatile metabolites of these bacteria such as acetic acid, isobutyric acid and 2-methylbutyric acid (Mazzetto et al, 2016) and these compounds were emitted only from ACV lures in our study (Figures 6 and 7).…”

Section: Discussionmentioning

confidence: 62%

Section: Discussionmentioning

confidence: 99%

Lure design for Drosophila suzukii based on liquid culture of fruit epiphytic yeasts: Comparing the attractivity of fermentation volatiles for seasonal morphs

Erdei

Szelényi

Deutsch

et al. 2022

J Applied Entomology

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The spotted-wing drosophila (SWD; Drosophila suzukii (Matsumura)) is a highly polyphagous vinegar fly, endemic to East Asia (Asplen et al., 2015). Female D. suzukii have serrated ovipositors that can puncture the fruit epidermis allowing oviposition into ripening soft-skinned and stone fruits. Both larval feeding and secondary microbial infestation cause serious fruit damage and thus massive economic losses (Knapp et al., 2021). Since the fairly recent introduction to Europe and North America, D. suzukii has emerged to be a major invasive pest of stone and soft fruits cultivation worldwide (CABI 2021).

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“…One of the primary differences is likely the microbiome of the flies. The microbiome has been shown to affect lifespan and fecundity [ 51 ]. In the lab, the microbiome is mostly obtained from the parents and the lab environment, with bacteria belonging to the families Acetobacteracceae and Lactobacillaceae being the most prevalent components [ 52 – 54 ].…”

Section: Resultsmentioning

confidence: 99%

The use of non-model Drosophila species to study natural variation in TOR pathway signaling

2022

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Nutrition and growth are strongly linked, but not much is known about how nutrition leads to growth. To understand the connection between nutrition through the diet, growth, and proliferation, we need to study the phenotypes resulting from the activation and inhibition of central metabolic pathways. One of the most highly conserved metabolic pathways across eukaryotes is the Target of Rapamycin (TOR) pathway, whose primary role is to detect the availability of nutrients and to either induce or halt cellular growth. Here we used the model organism Drosophila melanogaster (D. mel.) and three non-model Drosophila species with different dietary needs, Drosophila guttifera (D. gut.), Drosophila deflecta (D. def.), and Drosophila tripunctata (D. tri.), to study the effects of dietary amino acid availability on fecundity and longevity. In addition, we inhibited the Target of Rapamycin (TOR) pathway, using rapamycin, to test how the inhibition interplays with the nutritional stimuli in these four fruit fly species. We hypothesized that the inhibition of the TOR pathway would reverse the phenotypes observed under conditions of overfeeding. Our results show that female fecundity increased with higher yeast availability in all four species but decreased in response to TOR inhibition. The longevity data were more varied: most species experienced an increase in median lifespan in both genders with an increase in yeast availability, while the lifespan of D. mel. females decreased. When exposed to the TOR inhibitor rapamycin, the life spans of most species decreased, except for D. tri, while we observed a major reduction in fecundity across all species. The obtained data can benefit future studies on the evolution of metabolism by showing the potential of using non-model species to track changes in metabolism. Particularly, our data show the possibility to use relatively closely related Drosophila species to gain insight on the evolution of TOR signaling.

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Microbiota Influences Fitness and Timing of Reproduction in the Fruit Fly Drosophila melanogaster

Cited by 8 publications

References 48 publications

Flagellar genes are associated with the colonization persistence phenotype of theDrosophila melanogastermicrobiota

Flagellar genes are associated with the colonization persistence phenotype of theDrosophila melanogastermicrobiota

Lure design for Drosophila suzukii based on liquid culture of fruit epiphytic yeasts: Comparing the attractivity of fermentation volatiles for seasonal morphs

The use of non-model Drosophila species to study natural variation in TOR pathway signaling

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