Gut microbiota affects development and olfactory behavior in <i>Drosophila melanogaster</i>

Qiao, Huili; Keesey, Ian W.; Hansson, Bill S.; Knaden, Markus

doi:10.1242/jeb.192500

Cited by 78 publications

(67 citation statements)

References 48 publications

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“…Additional genes of interest identified using GO Using a fecundity assay, we observed that females without a microbiome laid fewer 257 eggs than females with a microbiome. This observation confirms published 258 results [28,37,39]. Furthermore, we observed lower mRNA abundance of genes involved 259 in egg production in axenic females.…”

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confidence: 88%

“…37 Removing the microbiome (bacteria and yeast) from D. melanogaster affects a wide 38 range of traits, including the gut transcriptome, which highlights the regulatory effects 39 of the microbiome on tissue homeostasis, carbohydrate and lipid metabolism, proteolysis 40 and immunity [22][23][24][25][26]. In addition, microbiome-induced transcriptome changes underlie 41 a range of phenotypes such as larval development time [27][28][29][30], metabolite levels [30,31], 42 intestinal stem cell proliferation [32,33], behavior [34,35], longevity [28,33,36] and 43 reproductive capacity [28,[37][38][39]. 44…”

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Interactions between the microbiome and mating influence the female’s transcriptional profile inDrosophila melanogaster

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Ahmed-Braimah

Wolfner

et al. 2020

Preprint

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Drosophila melanogaster females undergo a variety of post-mating changes that 1 influence their activity, feeding behavior, metabolism, egg production and gene 2 expression. These changes are induced either by mating itself or by sperm or seminal 3 fluid proteins. In addition, studies have shown that axenic females-those lacking a 4 microbiome-have altered fecundity compared to females with a microbiome, and that 5 the microbiome of the female's mate can influence reproductive success. However, the 6 extent to which post-mating changes in transcript abundance are affected by 7 microbiome state is not well-characterized. Here we investigated fecundity and the 8 post-mating transcript abundance profile of axenic or control females after mating with 9 either axenic or control males. We observed interactions between the female's 10 microbiome and her mating status: transcripts of genes involved in reproduction and 11 genes with neuronal functions were differentially abundant depending on the females' 12 microbiome status, but only in mated females. In addition, immunity genes showed 13 varied responses to either the microbiome, mating, or a combination of those two 14 factors. We further observed that the male's microbiome status influences the fecundity 15 of both control and axenic females, while only influencing the transcriptional profile of 16 axenic females. Our results indicate that the microbiome plays a vital role in the 17 post-mating switch of the female's transcriptome. 18 1 Introduction 19 Reproductive success is determined by the cumulative effects of behavioral and 20 physiological changes that a female undergoes after mating. In Drosophila, these 21 post-mating responses include sperm storage, increased oocyte production and 22 ovulation, a decrease in sleep and the female's propensity to remate, alterations to the 23 female's immune system, and changes in feeding frequency, gut morphology and 24 physiology (reviewed in [1]). These phenotypic changes are accompanied by extensive 25 transcriptome changes across several female tissues [2-11]. These transcriptome changes 26 typically reach their highest magnitude at around six hours after mating [5, 10], and 27often include genes that encode proteolytic/metabolic enzymes and immune response 28 genes [5,[9][10][11]. Furthermore, these female post-mating responses are influenced by an 29 1/28 interplay between the genotypes of the female and her mate [12][13][14][15][16], and are induced in 30 part by male ejaculate components that are transferred to the female during 31 mating [1, 4-6, 17, 18]. The post-mating changes in metabolism and food uptake are 32 thought to be required to meet the high energetic demands of oocyte production [19,20], 33 and can be potentially be influenced by transient factors such as the host microbiome. 34In recent years, Drosophila melanogaster has emerged as a valuable model to study 35 fundamental principles of host-microbiome interactions, owing to the availability of 36 genetic resources and a well-characterized and easily-m...

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supporting

confidence: 88%

mentioning

confidence: 99%

Interactions between the microbiome and mating influence the female’s transcriptional profile inDrosophila melanogaster

Delbare

Ahmed-Braimah

Wolfner

et al. 2020

Preprint

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“…Similarly, numerous investigations have been devoted to elucidating the role of intestinal microflora in mammals (Pasinetti et al, 2018;Roselli et al, 2017) and fishes (Gómez & José Luis, 2010;Zhou, Ringø, Olsen, & Song, 2018). Although studying entomic intestinal microflora remains relatively novel, its development and metabolism, even behavior is shown to be similar to the gut microbiota of the other animals (Ayayee, Muñoz-Garcia, & Keeney, 2018;Qiao, Keesey, Hansson, & Knaden, 2019;Xia et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Variation in the pH of experimental diets affects the performance ofLymantria dispar asiaticalarvae and its gut microbiota

Zeng

Shi

Guo

et al. 2020

Arch Insect Biochem Physiol

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To study dietary pH effects on Lymantria dispar asiatica larvae and provide a theoretical basis for its control in different forests, phosphate buffers (PBs) of pH 6, 7, and 8 were used to prepare experimental diets. The diet prepared with pH 6 PB was named as DPB6, with pH 8 PB as DPB8, and with pH 7 PB as DPB7 (control). The dietary pH was 5.00 in DPB6, 6.05 in control, and 6.50 in DPB8. After feeding on the diets with different pH values for 84 hr, fourth‐instar caterpillars were randomly collected. Growth and various physiological traits were determined and 16S recombinant DNA sequencing was performed using the intestinal microflora of surviving larvae. Results showed that the mortality was 30% in DPB6, and 10% in DPB8, while no mortality was observed in control. The partial least squares discriminant analyses suggested that diets prepared with PB of different pH resulted in different food intake, amount of produced feces, weight gain, digestive enzyme activities, and antioxidant enzyme activities in larvae. Interestingly, both the highest weight gain and the lowest total antioxidant capacities were seen in control larvae. Results also showed that the larval gut microbiota community structure was significantly affected by dietary pH. Moreover, linear discriminant analysis effect size suggested that the family Acetobacteraceae in control, genus Prevotella in DPB8, and genus Lactococcus, family Flavobacteriaceae, family Mitochondria, and family Burkholderiaceae in DPB6 contributed to the diversity of the larval gut microbial community.

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“…The previous study suggested that intestinal microflora was involved in human's physical and mental health (Petersen, Skov, Thyssen, & Jensen, ; Stricoff & Robinson, ). Similarly, intestinal microflora plays diverse functions in invertebrate, such as olfactory behavior regulation (Qiao, Keesey, Hansson, & Knaden, ), metabolism (Ayayee, Muñoz‐Garcia, & Keeney, ; B. Chen et al, ), and immune (Lee, Lee, & Lee, ; Martemyanov et al, ; Xia et al, ). In addition, consistent changes of gut microbial community and host development indicated that the gut microbiota might be involved in the entomic development (B. Chen et al, ).…”

Section: Introductionmentioning

confidence: 99%

“…The previous study suggested that intestinal microflora was involved in human's physical and mental health (Petersen, Skov, Thyssen, & Jensen, 2019;Stricoff & Robinson, 2018). Similarly, intestinal microflora plays diverse functions in invertebrate, such as olfactory behavior regulation (Qiao, Keesey, Hansson, & Knaden, 2019), metabolism (Ayayee, Muñoz-Garcia, & Keeney, 2018;B. Chen et al, 2016), and immune (Lee, Lee, & Lee, 2017;Martemyanov et al, 2016;Xia et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Ambient temperature‐mediated enzymic activities and intestinal microflora in Lymantria dispar larvae

Zeng

Shi

et al. 2019

Arch Insect Biochem Physiol

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To understand how ambient temperature affect the gypsy moth larvae, and provide a theoretical basis for pest control in different environments. Fourth instar gypsy moth larvae were incubating for 3 hr at 15℃, 20℃, 25℃, 30℃, 35℃, and 40℃, respectively. Afterward, digestive and antioxidant enzyme activities, total antioxidant capacity, and intestinal microflora community were analyzed to reveal how the caterpillars respond to ambient temperature stress. Results showed that both digestive and antioxidant enzymes were regulated by the ambient temperature. The optimum incubation temperatures of protease, amylase, trehalase, and lipase in gypsy moth larvae were 30℃, 25℃, and 20℃, respectively. When the incubation temperature was deviated optimum temperatures, digestive enzyme activities would be downregulated depending on the extent of temperature stress. In addition, glutathione S‐transferase, peroxidase, catalase, and polyphenol oxidase would be activated under a sufferable temperature stress, but superoxide dismutase and carboxylesterase (CarE) would be inhibited. In addition, results showed that the top two abundant phyla were Proteobacteria and Firmicutes. The phylum Firmicutes abundance was decreased and phylum Proteobacteria abundance was increased by ambient temperature stress. Moreover, it suggested that gypsy moth caterpillars at different ambient temperature mainly differed from each other by Escherichia‐Shigella and Bifidobacterium in control, Acinetobacter in T15, and Lactobacillus in T40, respectively.

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Gut microbiota affects development and olfactory behavior in Drosophila melanogaster

Cited by 78 publications

References 48 publications

Interactions between the microbiome and mating influence the female’s transcriptional profile inDrosophila melanogaster

Interactions between the microbiome and mating influence the female’s transcriptional profile inDrosophila melanogaster

Variation in the pH of experimental diets affects the performance ofLymantria dispar asiaticalarvae and its gut microbiota

Ambient temperature‐mediated enzymic activities and intestinal microflora in Lymantria dispar larvae

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