Commensal Gut Bacteria Buffer the Impact of Host Genetic Variants on Drosophila Developmental Traits under Nutritional Stress

Abstract

Eukaryotic genomes encode several buffering mechanisms that robustly maintain invariant phenotypic outcome despite fluctuating environmental conditions. Here we show that the Drosophila gutassociated commensals, represented by a single facultative symbiont, Lactobacillus plantarum (Lp WJL), constitutes a so far unexpected buffer that masks the contribution of the host's cryptic genetic variation (CGV) to developmental traits while the host is under nutritional stress. During chronic under-nutrition, Lp WJL consistently reduces variation in different host phenotypic traits and ensures robust organ patterning during development; Lp WJL also decreases genotype-dependent expression variation, particularly for development-associated genes. We further provide evidence that Lp WJL buffers via reactive oxygen species (ROS) signaling whose inhibition impairs microbiota-mediated phenotypic robustness. We thus identified a hitherto unappreciated contribution of the gut facultative symbionts to host fitness that, beyond supporting growth rates and maturation timing, confers developmental robustness and phenotypic homogeneity in times of nutritional stress.

How gut microbiome interactions affect nutritional traits of Drosophila melanogaster

“…Although most research on this topic has been conducted on Drosophila associated with a single bacterial strain (e.g. Chaston et al, 2014;Ma et al, 2019;Shin et al, 2011), there is growing interest in the effects of among-microbe interactions on various fly traits (Aranda-Díaz et al, 2020;Consuegra et al, 2020;Fischer et al, 2017;Gould et al, 2018;Judd et al, 2018;Sommer and Newell, 2019). Here, we demonstrate that the impact of a microbial community on metabolism-related traits, especially lipid content, cannot be predicted reliably from the study of mono-associations because the effect of individual microorganisms is strongly influenced by other microorganisms, especially yeast-bacterial interactions, and by host sex.…”

Integrative developmental ecology: a review of density-dependent effects on life-history traits and host-microbe interactions in non-social holometabolous insects

“…Theoretical and empirical work shows that strong stabilising selection eliminate genetic variability in the population [e.g., (Barton and Keightley 2002;Brooks et al 2005;Hunt et al 2007;Johnson and Barton 2005)]. Density-dependent host-microbe interactions can decrease frequency of extreme phenotypes by buffering against genetic variance of the host and negative ecological or nutritional conditions [see discussion above; (Ma et al 2019)]. This can modulate the opportunity for and potentially the strength of -stabilising selection in a population; a possible consequence of this process is that genetic variability in a population might be partly maintained in the population, as the frequencies of extreme phenotypes decrease due to the 'buffering' effects of host-microbe interactions.…”

How commensal microbes shape the physiology of Drosophila melanogaster

“…In addition to their contribution to host nutrition, commensals influence the development of their host through the action of Reactive Oxygen Species (ROS). While Drosophila is under nutritional stress, L. plantarum reduces the phenotypic variation in certain developmental traits attributed to cryptic genetic variation by buffering transcriptional variation in developmental genes [25]. As a result, larvae associated with L. plantarum vary less in size than GF larvae and adult flies emerging from these L. plantarum-associated larvae show less developmental traits abnormalities, such as wing patterning defects.…”