Timing Is Everything: The Effect of Exposure to Pollution on Wildlife Gut Microbiota Is Contingent on Season

Exposure to environmental pollutants can disrupt the gut microbiota, but how pollutants impact natural, seasonal changes in wildlife gut microbiota remains unknown. We quantified how exposure to radionuclides affected temporal changes in the gut microbiota of bank voles (Clethrionomys glareolus) inhabiting the Chornobyl Exclusion Zone (CEZ), Ukraine. Wild-caught bank voles from contaminated and uncontaminated areas within the CEZ were released into field enclosures that differed in their levels of environmental radionuclides so that the gut microbiota could be longitudinally sampled from animals experiencing a known difference in contamination. Using 16S rRNA amplicon sequencing, we uncovered pronounced seasonal changes in alpha and beta diversity. Underlying this seasonal variation, exposure to radionuclides had a significant influence on beta diversity. Notably, the Bacillota (formerly Firmicutes) to Bacteroidota (formerly Bacteroidetes) (F:B) ratio and the number and composition of differentially abundant bacterial genera differed with time. Exposure to environmental radionuclides did not increase the dispersion in gut microbiota beta diversity. This contrasts with expectations of the Anna Karenina principle for microbiota, which predicts that exposure to a stressor leads to more stochastic, individualised changes in community composition, resulting in increased variation among individuals. Our data demonstrate how a cross-sectional study can fail to capture the wider effects of pollutants on the gut microbiota of wild animals because of natural, seasonal dynamics in the microbial communities. Also, we highlight the importance of temporal monitoring of wildlife to uncover context-dependent effects of pollutants on microbiota. Exposure to radionuclides is associated with changes in the gut microbiota of wild bank voles, but in a seasonally contingent manner that is likely shaped by interactions between host diet, physiology and the level of environmental stress.