Dataset Information

The microbiota of Drosophila suzukii influences the larval development of Drosophila melanogaster.

ABSTRACT: Microorganisms play a central role in the biology of vinegar flies such as Drosophila suzukii and Drosophila melanogaster: serving as a food source to both adults and larvae, and influencing a range of traits including nutrition, behavior, and development. The niches utilized by the fly species partially overlap, as do the microbiota that sustain them, and interactions among these players may drive the development of crop diseases. To learn more about how the microbiota of one species may affect the other, we isolated and identified microbes from field-caught D. suzukii, and then characterized their effects on D. melanogaster larval development time in the laboratory. We found that the D. suzukii microbiota consistently included both yeasts and bacteria. It was dominated by yeasts of the genus Hanseniaspora, and bacteria from the families Acetobacteraceae and Enterobacteriaceae. Raising D. melanogaster under gnotobiotic conditions with each microbial isolate individually, we found that some bacteria promoted larval development relative to axenic conditions, but most did not have a significant effect. In contrast, nearly all the yeasts tested significantly accelerated larval development. The one exception was Starmerella bacillaris, which had the opposite effect: significantly slowing larval developmental rate. We investigated the basis for this effect by examining whether S. bacillaris cells could sustain larval growth, and measuring the survival of S. bacillaris and other yeasts in the larval gut. Our results suggest S. bacillaris is not digested by D. melanogaster and therefore cannot serve as a source of nutrition. These findings have interesting implications for possible interactions between the two Drosophilia species and their microbiota in nature. Overall, we found that microbes isolated from D. suzukii promote D. melanogaster larval development, which is consistent with the model that infestation of fruit by D. suzukii can open up habitat for D. melanogaster. We propose that the microbiome is an important dimension of the ecological interactions between Drosophila species.

SUBMITTER: Solomon GM

PROVIDER: S-EPMC6873876 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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The microbiota of Drosophila suzukii influences the larval development of Drosophila melanogaster.

Solomon Gabrielle M GM Dodangoda Hiruni H McCarthy-Walker Tylea T Ntim-Gyakari Rita R Newell Peter D PD

PeerJ 20191119

Microorganisms play a central role in the biology of vinegar flies such as Drosophila suzukii and Drosophila melanogaster: serving as a food source to both adults and larvae, and influencing a range of traits including nutrition, behavior, and development. The niches utilized by the fly species partially overlap, as do the microbiota that sustain them, and interactions among these players may drive the development of crop diseases. To learn more about how the microbiota of one spec ...[more]

PMID: 31763075

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Project description:To better understand how associated microorganisms ("microbiota") influence organismal aging, we focused on the model organism Drosophila melanogaster We conducted a metagenome-wide association (MGWA) as a screen to identify bacterial genes associated with variation in the D. melanogaster life span. The results of the MGWA predicted that bacterial cysteine and methionine metabolism genes influence fruit fly longevity. A mutant analysis, in which flies were inoculated with Escherichia coli strains bearing mutations in various methionine cycle genes, confirmed a role for some methionine cycle genes in extending or shortening fruit fly life span. Initially, we predicted these genes might influence longevity by mimicking or opposing methionine restriction, an established mechanism for life span extension in fruit flies. However, follow-up transcriptome sequencing (RNA-seq) and metabolomic experiments were generally inconsistent with this conclusion and instead implicated glucose and vitamin B6 metabolism in these influences. We then tested if bacteria could influence life span through methionine restriction using a different set of bacterial strains. Flies reared with a bacterial strain that ectopically expressed bacterial transsulfuration genes and lowered the methionine content of the fly diet also extended female D. melanogaster life span. Taken together, the microbial influences shown here overlap with established host genetic mechanisms for aging and therefore suggest overlapping roles for host and microbial metabolism genes in organismal aging.IMPORTANCE Associated microorganisms ("microbiota") are intimately connected to the behavior and physiology of their animal hosts, and defining the mechanisms of these interactions is an urgent imperative. This study focuses on how microorganisms influence the life span of a model host, the fruit fly Drosophila melanogaster First, we performed a screen that suggested a strong influence of bacterial methionine metabolism on host life span. Follow-up analyses of gene expression and metabolite abundance identified stronger roles for vitamin B6 and glucose than methionine metabolism among the tested mutants, possibly suggesting a more limited role for bacterial methionine metabolism genes in host life span effects. In a parallel set of experiments, we created a distinct bacterial strain that expressed life span-extending methionine metabolism genes and showed that this strain can extend fly life span. Therefore, this work identifies specific bacterial genes that influence host life span, including in ways that are consistent with the expectations of methionine restriction.

Project description:Associated microorganisms ("microbiota") play a central role in determining many animals' survival and reproduction characteristics. The impact of these microbial influences on an animal's fitness, or population growth, in a given environment has not been defined as clearly. We focused on microbiota-dependent host fitness by measuring life span and fecundity in Drosophila melanogaster fruit flies reared individually with 14 different bacterial species. Consistent with previous observations, the different bacteria significantly influenced the timing of fly life span and fecundity. Using Leslie matrices, we show that fly fitness was lowest when the microbes caused the flies to invest in life span over fecundity. Computational permutations showed that the positive fitness effect of investing in reproduction was reversed if fly survival over time was low, indicating that the observed fitness influences of the microbes could be context dependent. Finally, we showed that fly fitness is not influenced by bacterial genes that shape fly life span or fly triglyceride content, a trait that is related to fly survival and reproduction. Also, metagenome-wide association did not identify any microbial genes that were associated with variation in fly fitness. Therefore, the bacterial genetic basis for influencing fly fitness remains unknown. We conclude that bacteria influence a fly's reproductive timing more than total reproductive output and that (e.g., environmental) conditions that influence fly survival likely determine which bacteria benefit fly fitness. IMPORTANCE The ability of associated microorganisms ("microbiota") to influence animal life history traits has been recognized and investigated, especially in the past 2 decades. For many microbial communities, there is not always a clear definition of whether the microbiota or its members are beneficial, pathogenic, or relatively neutral to their hosts' fitness. In this study, we report the influence of individual members of the microbiota on Drosophila melanogaster fitness using Leslie matrices that combine the microbial influences on fly survival and reproduction into a single fitness measure. Our results are consistent with a previous report that, in the laboratory, acetic acid bacteria are more beneficial to the flies than many strains of lactic acid bacteria. We add to the previous finding by showing that this benefit depends on fly survival rate. Together, our work helps to show how the microbiota of a fly influences its laboratory fitness and how these effects may translate to a wild setting.

Dataset Information

The microbiota of Drosophila suzukii influences the larval development of Drosophila melanogaster.

Publications

The microbiota of <i>Drosophila suzukii</i> influences the larval development of <i>Drosophila melanogaster</i>.

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