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Sex-Dependent Effects of the Microbiome on Foraging and Locomotion in Drosophila suzukii.

ABSTRACT: There is growing evidence that symbiotic microbes can influence multiple nutrition-related behaviors of their hosts, including locomotion, feeding, and foraging. However, how the microbiome affects nutrition-related behavior is largely unknown. Here, we demonstrate clear sexual dimorphism in how the microbiome affects foraging behavior of a frugivorous fruit fly, Drosophila suzukii. Female flies deprived of their microbiome (axenic) were consistently less active in foraging on fruits than their conventional counterparts, even though they were more susceptible to starvation and starvation-induced locomotion was notably more elevated in axenic than conventional females. Such behavioral change was not observed in male flies. The lag of axenic female flies but not male flies to forage on fruits is associated with lower oviposition by axenic flies, and mirrored by reduced food seeking observed in virgin females when compared to mated, gravid females. In contrast to foraging intensity being highly dependent on the microbiome, conventional and axenic flies of both sexes showed relatively consistent and similar fruit preferences in foraging and oviposition, with raspberries being preferred among the fruits tested. Collectively, this work highlights a clear sex-specific effect of the microbiome on foraging and locomotion behaviors in flies, an important first step toward identifying specific mechanisms that may drive the modulation of insect behavior by interactions between the host, the microbiome, and food.

SUBMITTER: Shu R

PROVIDER: S-EPMC8141744 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Drosophila suzukii Matsumura is an invasive species of vinegar fly that has become a prominent pest of berries and other soft-skinned fruits. Unlike most other Drosophila species, female D. suzukii flies lay their eggs in ripening and ripe fruits and larvae develop within the fruit. To understand how D. suzukii larvae utilize ripe and ripening fruits, which usually have low levels of protein, we investigated the microbiota of field-captured and laboratory-reared D. suzukii flies and further examined the combined influence of diet and microbes on host fitness. Field-captured flies were associated with diverse microbiota, which varied significantly with sampling location and season. In contrast, laboratory-reared flies possessed strikingly lower bacterial abundance and diversity. A comparison of conventionally reared (CR) and germ-free (GF) flies revealed that the microbiota of D. suzukii does not alter its development significantly but decreases its life span under conditions of a nutrient-sufficient diet. However, the microbiota is essential for D. suzukii development on strawberry-based or blueberry-based fruit diets. This developmental failure could be rescued by reassociation with single bacterial or fungal species or by the addition of a high quantity of heat-killed microbes. In addition, we found that proteins are limiting with respect to fly development on fruit-based diets and that GF flies show signs of protein starvation. Taken together, our study results demonstrate that the microbiota provides key proteins required for the development of D. suzukii reared on fresh fruit. Our work shows that the impact of microbes on fly fitness depends strongly on nutritional conditions.IMPORTANCE Animals are commonly associated with specific microbes, which play important roles in host development and fitness. However, little information about the function of microbes has been available for the important invasive pest Drosophila suzukii, also known as Spotted wing drosophila. Our study results demonstrate that the abundance and structure of microbiota in D. suzukii are strongly affected by the environment, where microbes have variable roles depending on the nutritional situation. For instance, we found that the presence of microbes is deleterious for flies growing on a protein-rich diet and yet is beneficial for flies growing on a diet of protein-poor fruits. Additionally, germ-free flies must feed on microbes to obtain the necessary protein for larval development on strawberries and blueberries. Our report validates the complexity seen in host-microbe interactions and may provide information useful for D. suzukii pest control.

Project description:IntroductionThe impact of nicotine, the addictive component of both traditional cigarettes and e-cigarettes, on many physiological processes remains poorly understood. To date, there have been few investigations into the impact of nicotine on the gut microbiome, and these studies utilized oral administration rather than inhalation. This study aimed to establish if inhaled nicotine alters the gut microbiome and the effect of sex as a biological variable.MethodsFemale (n = 8 air; n = 10 nicotine) and male (n = 10 air; n = 10 nicotine) C57BL6/J mice were exposed to air (control) or nicotine vapor (12 hour/day) for 13 weeks. A fecal sample was collected from each mouse at the time of sacrifice, and the gut microbiome was analyzed by 16S rRNA gene sequencing. QIIME2, PICRUSt, and STAMP were used to detect gut bacterial differences and functional metabolic pathways.ResultsSex-specific differences were observed in both alpha and beta diversities in the absence of nicotine. While nicotine alters microbial community structure in both male and female mice as revealed by the beta diversity metric, nicotine significantly reduced alpha diversity only in female mice. A total of 42 bacterial taxa from phylum to species were found to be significantly different among the treatment groups. Finally, analysis for functional genes revealed significant differences in twelve metabolic pathways in female mice and ten in male mice exposed to nicotine compared to air controls.ConclusionsNicotine inhalation alters the gut microbiome and reduces bacterial diversity in a sex-specific manner, which may contribute to the overall adverse health impact of nicotine.ImplicationsThe gut microbiota plays a fundamental role in the well-being of the host, and traditional cigarette smoking has been shown to affect the gut microbiome. The effects of nicotine alone, however, remain largely uncharacterized. Our study demonstrates that nicotine inhalation alters the gut microbiome in a sex-specific manner, which may contribute to the adverse health consequences of inhaled nicotine. This study points to the importance of more detailed investigations into the influence of inhaled nicotine on the gut microbiota.

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Sex-Dependent Effects of the Microbiome on Foraging and Locomotion in Drosophila suzukii.

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