Maternally-transmitted microbiota affects odor emission and preference in Drosophila larva

Abstract

Experimental studies show that early sensory experience often affects subsequent sensory preference, suggesting that the heterogeneity of sensory cues in nature could induce significant inter-individual behavioral variation, potentially contributing to maintain intraspecific diversity. To test this hypothesis, we explored the behavioral effect induced by variation in the levels of a self-produced chemical, acetoin, and its link with intraspecific diversity. Acetoin is a pheromone-like substance produced by gut-associated microorganisms in Drosophila. Using wild-type Drosophila melanogaster populations producing variable acetoin levels, we (i) characterized factors involved in this variation and (ii) manipulated some of these factors to affect acetoin responses in larvae. We found that increased and decreased variations in acetoin levels were caused by microorganisms associated with the outside and inside of the egg, respectively. Wild-type larvae preferred acetoin-rich food only when they both produced and were exposed to substantial amounts of acetoin. The removal of the outside of the egg or the genetic alteration of olfaction abolished this preference. In contrast, larvae exposed to high doses of synthetic acetoin were repulsed by acetoin. The similar effects obtained with freshly caught wild-type lines suggest that this acetoin “production-preference” link underlies the diversity of acetoin-producing microorganisms among natural D. melanogaster populations.

First step of odorant detection in the olfactory epithelium and olfactory preferences differ according to the microbiota profile in mice

“…Olfactory preferences are also essential in feeding behaviour [34] and the diversity of food ingested has an impact on the microbiota [33,35]. Our present work indicates that the microbiota could play a key role in shaping the chemical senses and thus the feeding behaviour of mammals as it has recently been shown in insects [36][37][38][39]. It could be one piece of the puzzle in the microbiota-brain axis, as stabilizing the type of food ingested will in turn maintain the microbiota population.…”

The microbiota influences the Drosophila melanogaster life history strategy

“…Thus, the many Acetobacteraceae that are highly competitive in aerobic environments with high concentrations of sugars and other readily assimilated nutrients (Lievens et al, 2015;Wong et al, 2015) may represent a reliable cue for high-nutrient but ephemeral resources, favouring a "fast" phenotype of the host, while many Lactobacillales, which utilize complex carbon and nitrogen sources that are consumed more slowly (Duar et al, 2017), favour a "slow" phenotype of the host. Evidence from several studies suggest that the blend of fermentation products produced by microbial communities of different composition in the food and gut of Drosophila may represent a reliable cue for habitats of different nutritional content and persistence (Farine, Habbachi, Cortot, Roche, & Ferveur, 2017;Fischer et al, 2017;Kim, Huang, McMullen, Newell, & Douglas, 2018).…”

Metabolic Basis for Mutualism between Gut Bacteria and Its Impact on the Drosophila melanogaster Host

“…In either case, the volatiles would signal that a potential substrate for oviposition is lower in sugar and higher in protein than one lacking interspecies metabolic exchange, i.e., a nutrient profile more conducive to rapid larval development (32). Food preferences of both larvae and adults are influenced by microbes in the food source, as well as the identity of the microbes with which the animals were raised (39,43,60). These findings suggest a dynamic in which cooperation between microbes could be reinforced because the host is conditioned to seek out microbiota with a familiar metabolic profile.…”