Common structuring principles of the Drosophila melanogaster microbiome on a continental scale and between host and substrate

Abstract

Summary The relative importance of host control, environmental effects and stochasticity in the assemblage of host‐associated microbiomes is being debated. We analysed the microbiome among fly populations that were sampled across Europe by the European Drosophila Population Genomics Consortium (DrosEU). In order to better understand the structuring principles of the natural D. melanogaster microbiome, we combined environmental data on climate and food‐substrate with dense genomic data on host populations and microbiome profiling. Food‐substrate, temperature, and host population structure correlated with microbiome structure. Microbes, whose abundance was co‐structured with host populations, also differed in abundance between flies and their substrate in an independent survey. This finding suggests common, host‐related structuring principles of the microbiome on different spatial scales.

Horizontal gene transfer-mediated bacterial strain variation affects host fitness

“…A difference between our-and these previous studies is that although Gluconobacter is frequently associated with D. melanogaster under natural conditions [54][55][56][57], it is neither an obligate symbiont nor is it restricted to the fly gut. Given occurence in the environment and the opportunity for horizontal transfer of the bacterium between hosts, there is currently no evidence that the fly host significantly affects Gluconobacter evolution.…”

“…Species from this genus can benefit Drosophila development [28]. One isolate was Commensalibacter intestini that might have a probiotic function in D. melanogaster [71] and is enriched in flies over substrate in wild-caught flies [57]. As an outgroup and to get a baseline for the fitness effect of an ingested pathogen, we added Providencia sneebia, that is highly pathogenic when entering the hemolyph [72].…”

“…Waterworth et al [94] suggested that the acquisition of genes to produce a defensive compound via HGT was key to the domestication of a bacterial defensive symbiont in beetles. We speculate that similar scenarios might be plausible for nutritional benefits in Drosophila because (i) mechanisms of host selection work efficiently for environmentally acquired bacteria [95][96][97][98], (ii) stable, strain specific associations of Drosophila with mutualistic bacteria have been reported [50], and (iii) evidence for host selection in the fly is accumulating in the laboratory [45,99] as well as under natural conditions [55,57]. Because the result of HGT here provides a potential benefit to the host under thiamine poor conditions that are often encountered under natural conditions e.g.…”

“…In order to increase the power of the approach and consider variation at low taxonomic levels, we concentrated on variation within a taxonomically restricted group of bacteria. Therefore, we focused our study on Gluconobacter, a bacterial genus that is commonly associated with D. melanogaster under natural conditions [54][55][56][57]. We assessed fitness parameters on grape juice based fly food as a near natural food source.…”

Host evolutionary history and ecological context modulate the adaptive potential of the microbiome

“…2). Acetobacter are common in flies, both in laboratory settings and wild environments [17,[49][50][51][52]. Furthermore, Acetobacter are sugar specialists and tolerate highly acidic environments, like during vinegar fermentation [53].…”