Stable association of a Drosophila-derived microbiota with its animal partner and the nutritional environment throughout a fly population’s life cycle

Abstract

In the past years, the fruit fly Drosophila melanogaster has been extensively used to study the relationship between animals and their associated microbes. Compared to the one of wild populations, the microbiota of laboratory-reared flies is less diverse, and comprises fewer bacterial taxa; nevertheless, the main commensal bacteria found in fly microbiota always belong to the Acetobacteraceae and Lactobacillaceae families. The bacterial communities associated with the fly are environmentally acquired, and the partners engage in a perpetual re-association process. Adult flies constantly ingest and excrete microbes from and onto their feeding substrate, which are then transmitted to the next generation developing within this shared habitat. We wanted to analyze the potential changes in the bacterial community during its reciprocal transfer between the two compartments of the niche (i.e. the fly and the diet). To address this question, we used a diverse, wild-derived microbial community and analyzed its relationship with the fly population and the nutritive substrate in a given habitat. Here we show that the community was overall well maintained upon transmission to a new niche, to a new fly population and to their progeny, illustrating the stable association of a Drosophila-derived microbiota with its fly partner and the nutritional environment. These results highlight the preponderant role of the nutritional substrate in the dynamics of Drosophila/microbiota interactions, and the need to fully integrate this variable when performing such studies.

Commensal bacteria act as a broad genetic buffer in Drosophila during chronic under-nutrition

“…We thus wondered if a natural and more complex gut microbiota can also buffer growth variation like Lp WJL . To address this question, we rendered a population of wild flies collected in a nearby garden germ-free, and re-associated them with their own fecal microbial community[15]. In three out of four experimental repeats, growth variation is significantly reduced in the larval population fed on food inoculated with fecal microbiota (Fig.S3d and data not shown), and the cumulative CV and variances derived from each food cap were significantly higher in the GF population (Fig.S3e and S3f).…”

Environmental specificity and evolution in Drosophila-bacteria symbiosis

“…transstadial transmission from the larval to the adult stage) and pseudo-vertically during oviposition (i.e. from mothers to offspring) (Bakula 1969; Starmer et al 1988; Spencer 1992; Ridley et al 2012; Wong et al 2015; Téfit et al 2018). Second, host immune system participates to the destruction of harmful gut bacteria and the retention of beneficial ones (Lee et al 2017; Lee et al 2018).…”

“…Studies have shown that bacterial microbiota composition appears to be determined by the laboratory where the Drosophila flies were reared more than by their species (Chandler et al 2011; Staubach et al 2013), demonstrating these symbionts are largely acquired from the fly environment. Empirical studies have nonetheless shown pseudo-vertical transmission of bacteria from mothers to offspring also occurs in the laboratory (Bakula 1969; Ridley et al 2012; Wong et al 2015; Téfit et al 2018). Microbiota composition differences between laboratory and field flies have led authors to argue that symbiotic phenomena as observed in the laboratory may not reflect those occurring in natural conditions (Chandler et al 2011; Winans et al 2017).…”

Environmental specificity in Drosophila-bacteria symbiosis affects host developmental plasticity

“…Studies have shown that bacterial microbiota composition is determined by laboratory conditions more than Drosophila species (Chandler et al 2011;Staubach et al 2013), demonstrating these symbionts are largely acquired from fly environment. Empirical studies have nonetheless shown pseudo-vertical transmission of bacteria from mothers to offspring also occurs in the laboratory (Bakula 1969;Ridley et al 2012;Wong et al 2015;Téfit et al 2018). Microbiota composition differences between laboratory and field flies have led authors to argue that symbiotic phenomena as observed in the laboratory may not reflect those occurring in natural conditions (Chandler et al 2011;Winans et al 2017).…”