Mammals show distinct functional gut microbiome dynamics to identical series of environmental stressors

The ability of the gut microbiome has been posited as an additional axis of animals’ phenotypic plasticity. However, whether and how such plasticity varies across hosts with different biological features remains unclear. We performed a captivity experiment to compare how the taxonomic, phylogenetic, and functional microbial dynamics varied across a series of temperature and dietary disturbances in two mammals: the insectivorous-specialist Crocidura russula and the omnivorous-generalist Apodemus sylvaticus. Combining genome-resolved metagenomics, metabolic pathway distillation and joint species distribution modeling, we observed that, although microbiome alpha diversity of both species remained stable, C. russula exhibited substantially higher variability and directionality of microbial responses than A. sylvaticus. Our results indicate that the intrinsic properties (e.g., diversity and functional redundancy) of microbial communities coupled with physiological attributes (e.g., thermal plasticity) of hosts shape the taxonomic, phylogenetic, and functional response of gut microbiomes to environmental stressors, which might influence their contribution to the acclimation and adaptation capacity of animal hosts. IMPORTANCE: In our manuscript, we report the first interspecific comparative study about the plasticity of the gut microbiota. We conducted a captivity experiment that exposed wild-captured mammals to a series of environmental challenges over 45 days. We characterized their gut microbial communities using genome-resolved metagenomics and modeled how the taxonomic, phylogenetic, and functional microbial dynamics varied across a series of disturbances in both species. Our results indicate that the intrinsic properties (e.g., diversity and functional redundancy) of microbial communities coupled with physiological attributes (e.g., thermal plasticity) of hosts shape the taxonomic, phylogenetic, and functional response of gut microbiomes to environmental stressors, which might influence their contribution to the acclimation and adaptation capacity of animal hosts.