How gut transcriptional function of Drosophila melanogaster varies with the presence and composition of the gut microbiota

Abstract

Despite evidence from laboratory experiments that perturbation of the gut microbiota affects many traits of the animal host, our understanding of the effect of variation in microbiota composition on animals in natural populations is very limited. The core purpose of this study on the fruit fly Drosophila melanogaster was to identify the impact of natural variation in the taxonomic composition of gut bacterial communities on host traits, with the gut transcriptome as a molecular index of microbiota-responsive host traits. Use of the gut transcriptome was validated by demonstrating significant transcriptional differences between the guts of laboratory flies colonized with bacteria and maintained under axenic conditions. Wild Drosophila from six field collections made over two years had gut bacterial communities of diverse composition, dominated to varying extents by Acetobacteraceae and Enterobacteriaceae. The gut transcriptomes also varied among collections and differed markedly from those of laboratory flies. However, no overall relationship between variation in the wild fly transcriptome and taxonomic composition of the gut microbiota was evident at all taxonomic scales of bacteria tested for both individual fly genes and functional categories in Gene Ontology. We conclude that the interaction between microbiota composition and host functional traits may be confounded by uncontrolled variation in both ecological circumstance and host traits (e.g., genotype, age physiological condition) under natural conditions, and that microbiota effects on host traits identified in the laboratory should, therefore, be extrapolated to field population with great caution.

Correlation and causation between the microbiome, Wolbachia and host functional traits in natural populations of drosophilid flies

“…(The variability in transcriptional profiles did not differ between the sexes, precluding the alternative explanation that the few correlations in males reflected insufficient transcriptional variation.) Similar sex differences in transcriptional response to the microbiota have been obtained for laboratory‐reared D. melanogaster , in which fourfold more genes were differentially expressed between germ‐free flies and flies colonized with a standardized microbiota in female flies than males (Bost, Franzenburg et al, ). This difference may have a nutritional basis.…”

“…We conclude by considering how this study links to the call for greater research effort on microbiomes in natural populations of animals and plants (Hird, ; Perez‐Jaramillo, Carrion, Hollander, & Raaijmakers, ). The tight environmental controls and simplifying conditions of laboratory studies facilitate the study of fundamental mechanisms, but there is increasing evidence that some important processes and interactions are not displayed under laboratory conditions (Bost, Franzenburg et al, ; Ericsson et al, ). However, pursuing the general goal to study microbiomes in natural populations requires evidence that reliable patterns in host–microbiome interactions can be detected, despite uncontrolled environmental variation.…”

Functional variation in the gut microbiome of wild Drosophila populations

“…All 24 samples of pooled fly guts and four negative controls comprising template‐free samples were homogenized in 500 μl TRIzol with 500 μl 0.1‐mm glass beads (Scientific Industries, Bohemia, NY) on an MP Fastprep24 at 4.5 M/S for 2 × 30 s. The procedure of Bost et al. () was used for dual extraction of DNA and RNA. Briefly, total nucleic acids were extracted by phase separation with chloroform.…”

Introduction: The host‐associated microbiome: Pattern, process and function

“…Varying gene expression did not, however, correlate with particular bacteria detected in wild flies. Transcriptional profiles were, instead, seemingly influenced by the abiotic environment, specifically through fly exposure to metallic insecticides (e.g., copper) (Bost et al., ). These results identify challenges for understanding the natural relevance of symbiosis, even in well‐studied systems.…”