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

Abstract

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...

Differences in Postmating Transcriptional Responses between Conspecific and Heterospecific Matings inDrosophila

“…This hypothesis is difficult to assess at this time as ejaculate microbiomes have not been characterized in Drosophila . However, a recent study shows that some immune genes in D. melanogaster are up-regulated after mating even if the male is germ-free, indicating that copulation and/or ejaculate proteins are sufficient to initiate a postmating immune response ( Delbare et al. 2020 ).…”

Arc1 and the microbiota together modulate growth and metabolic traits inDrosophila

“…We initially identified Arc1 from a screen for transcripts showing differential abundance in the heads of GF vs. CV/GNO adult flies. Notably, Arc1 was recently designated a “core” microbiome-response gene in Drosophila , as it consistently appears in published RNA-seq studies focused on the gut or whole animals (Delbare et al, 2020). Our study further reveals that microbiota-dependent Arc1 mRNA and protein changes vary in direction and magnitude between the gut and the head/brain, and among different populations of Arc1-positive cells in the brain (Fig.…”

Beneficial Lactiplantibacillus plantarum promote Drosophila growth by down-regulating the expression of PGRP-SC1

“…In addition, it has been shown that fly growth promotion mediated by gut microbes results, at least in part, from the upregulation of digestive enzyme expression in the midgut via IMD/Relish activity (37). These insights came from comparing Drosophila with a microbiota (either single-strain associations or complex communities) versus without a microbiota (germ-free condition) (25, 28, 29, 33, 37, 38), and they largely contributed to our knowledge of the molecular mechanisms underlying the role of gut microbes in host physiology. Nevertheless, not all bacterial species or strains associated with Drosophila microbiota are beneficial.…”