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

Eukaryotic genomes encode several buffering mechanisms that robustly maintain invariant phenotypic outcome despite fluctuating environmental conditions. Here we show that the Drosophila gut-associated commensals, represented by a single facultative symbiont, Lactobacillus plantarum (LpWJL), 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, LpWJL consistently reduces variation in different host phenotypic traits and ensures robust organ patterning during development; LpWJL also decreases genotype-dependent expression variation, particularly for development-associated genes. We further provide evidence that LpWJL 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. [Display omitted] •Upon nutritional stress, fly commensals buffer the effects of cryptic genetic variants•Fly gut commensals buffer transcriptional variation in developmental genes•Fly commensals buffer phenotypic heterogeneity and mediate developmental canalization•Compromising ROS activities impair microbial buffering capacity Biological Sciences; Microbiology; Oral Microbiology