Ranavirus epizootics and gut bacteriome dysbiosis in tadpoles: evidence for the Anna Karenina Principle?
Host-associated microbial communities (microbiomes) play critical roles in animal health and disease, yet their responses to pathogens under natural conditions remain poorly understood. We investigated gut bacterial community (bacteriome) dynamics in wood frog (Rana sylvatica [Lithobates sylvaticus]) tadpoles during natural ranavirus outbreaks to understand how pathogen-induced disturbances shape microbiome diversity, composition, and function. Using 16S rRNA sequencing, we compared bacteriomes of tadpoles in ponds experiencing ranavirus-induced die-offs with those from unaffected reference ponds before, during, and after mortality events. Ranavirus infection significantly altered gut bacteriome composition and increased microbiome variability (dispersion), consistent with the Anna Karenina Principle. Tadpoles with high infection intensities exhibited reduced bacterial diversity and pronounced shifts in community structure, characterized by enrichment of specific taxa such as Cetobacterium and Turicibacter, which have been linked previously to antiviral immunity and gut health. Predicted functional analyses revealed shifts toward carbohydrate metabolism pathways during die-offs, suggesting microbial adaptation to altered host physiology under infection stress. Notably, bacteriome disruptions were detectable even before die-offs occurred, highlighting potential early-warning microbiome indicators of infection. In one recovering population post-epizootic, we observed partial recovery of the bacteriome, indicating potential microbial resilience. Our findings demonstrate that ranavirus epizootics profoundly disrupt gut microbiomes in wild amphibian populations while simultaneously eliciting potentially adaptive microbial responses. These insights underscore the complex interplay between host immunity, microbiome dynamics, and environmental conditions during disease outbreaks, highlighting opportunities for microbiome-based interventions to support amphibian conservation.