The microbiome buffers tadpole hosts from heat stress: a hologenomic approach to understand host–microbe interactions under warming

Phenotypic plasticity is an important strategy that animals employ to respond and adjust to changes in their environment. Plasticity may occur via changes in host gene expression or through functional changes in their microbiomes, which contribute substantially to host physiology. Specifically, the presence and function of host-associated microbes can impact how animals respond to heat stress. We previously demonstrated that ‘depleted’ tadpoles, with artificially disrupted microbiomes, are less tolerant to heat than ‘colonized’ tadpoles, with more natural microbiomes. However, the mechanisms behind these effects are unclear. Here, we compared gene expression profiles of the tadpole gut transcriptome, and tadpole gut microbial metagenome, between colonized and depleted tadpoles under cool or warm conditions. Our goal was to identify differences in host and microbial responses to heat between colonized and depleted tadpoles that might explain their observed differences in heat tolerance. We found that depleted tadpoles exhibited a much stronger degree of host gene expression plasticity in response to heat, while the microbiome of colonized tadpoles was significantly more heat sensitive. These patterns indicate that functional changes in the microbiome in response to heat may allow for a dampened host response, ultimately buffering hosts from the deleterious effects of heat stress. We also identified several specific host and microbial pathways that could be contributing to increased thermal tolerance in colonized tadpoles including amino acid metabolism, vitamin biosynthesis and ROS scavenging pathways. Our results demonstrate that the microbiome influences host plasticity and the response of hosts to environmental stressors.