Comparable response of wild rodent gut microbiome to anthropogenic habitat contamination.

Species identity is thought to dominate over environment in shaping wild rodent gut microbiota, but it remains unknown whether the responses of host gut microbiota to shared anthropogenic habitat impacts are species-specific or if the general gut microbiota response is similar across host species. Here, we compare the influence of exposure to radionuclide contamination on the gut microbiota of four wild mouse species: Apodemus flavicollis, A. sylvaticus, A. speciosus and A. argenteus. Building on the evidence that radiation impacts bank vole (Myodes glareolus) gut microbiota, we hypothesized that radiation exposure has a general impact on rodent gut microbiota. Because we sampled (n = 288) two species pairs of Apodemus mice that occur in sympatry in habitats affected by the Chernobyl and Fukushima nuclear accidents, these comparisons provide an opportunity for a general assessment of the effects of exposure to environmental contamination (radionuclides) on gut microbiota across host phylogeny and geographical areas. In general agreement with our hypothesis, analyses of bacterial 16S rRNA gene sequences revealed that radiation exposure alters the gut microbiota composition and structure in three of the four species of Apodemus mice. The notable lack of an association between the gut microbiota and soil radionuclide contamination in one mouse species from Fukushima (A. argenteus) probably reflects host "radiation escape" through its unique tree-dwelling lifestyle. The finding that host ecology can modulate effects of radiation exposure offers an interesting counterpoint for future analyses into effects of radiation or any other toxic exposure on host and its associated microbiota. Our data show that exposure to radionuclide contamination is linked to comparable gut microbiota responses across multiple species of rodents.

Applying the Anna Karenina principle for wild animal gut microbiota: Temporal stability of the bank vole gut microbiota in a disturbed environment.

Gut microbiota play an important role in host health. Yet, the drivers and patterns of microbiota imbalance (dysbiosis) in wild animals remain largely unexplored. One hypothesised outcome of stress on animal microbiomes is a destabilised microbial community that is characterised by an increase in inter-individual differences compared with microbiomes of healthy animals, which are expected to be (a) temporally stable and (b) relatively similar among individuals. This set of predictions for response of microbiomes to stressors is known as the Anna Karenina principle (AKP) for animal microbiomes. We examine the AKP in a wild mammal inhabiting disturbed environments by conducting a capture-mark-recapture survey of bank voles Myodes glareolus in areas that contrast in levels of radionuclide contamination (Chernobyl, Ukraine). Counter to key predictions of the AKP, bank voles that are not exposed to radionuclides harbour variable (increased inter-individual differences) and temporally dynamic gut microbiota communities, presumably tracking the natural spatio-temporal variation in resources. Conversely, bank voles exposed to radionuclides host more similar gut microbiota communities that are temporally stable, potentially due to a dysbiosis or selection (on host or bacteria) imposed by chronic radiation exposure. The implication of these data is that environmental stress (radiation exposure) can constrain the natural spatial and temporal variation of wild animal gut microbiota.

The effect of chronic low-dose environmental radiation on organ mass of bank voles in the Chernobyl exclusion zone.

PURPOSE: Animals are exposed to environmental ionizing radiation (IR) externally through proximity to contaminated soil and internally through ingestion and inhalation of radionuclides. Internal organs can respond to radioactive contamination through physiological stress. Chronic stress can compromise the size of physiologically active organs, but studies on wild mammal populations are scarce. The effects of environmental IR contamination on organ masses were studied by using a wild rodent inhabiting the Chernobyl exclusion zone (CEZ). MATERIAL AND METHODS: The masses of brain, heart, kidney, spleen, liver and lung were assessed from bank voles (Myodes glareolus) captured from areas across radioactive contamination gradient within the CEZ. Relative organ masses were used to correct for the body mass of an individual. RESULTS: Results showed a significant negative correlation between IR level in the environment and relative brain and kidney mass. A significant positive correlation between IR and relative heart mass was also found. Principal component analysis (PCA) also suggested positive relationship between IR and relative spleen mass; however, this relationship was not significant when spleen was analyzed separately. There was no apparent relationship between IR and relative liver or lung mass. CONCLUSIONS: Results suggest that in the wild populations even low but chronic doses of IR can lead to changes in relative organ mass. The novelty of these result is showing that exposure to low doses can affect the organ masses in similar fashion as previously shown on high, acute, radiation doses. These data support the hypothesis that wildlife might be more sensitive to IR than animals used in laboratory studies. However, more research is needed to rule out the other indirect effects such as radiosensitivity of the food sources or possible combined stress effects from e.g. infections.

Exposure to environmental radionuclides is associated with altered metabolic and immunity pathways in a wild rodent.

Wildlife inhabiting environments contaminated by radionuclides face putative detrimental effects of exposure to ionizing radiation, with biomarkers such as an increase in DNA damage and/or oxidative stress commonly associated with radiation exposure. To examine the effects of exposure to radiation on gene expression in wildlife, we conducted a de novo RNA sequencing study of liver and spleen tissues from a rodent, the bank vole Myodes glareolus. Bank voles were collected from the Chernobyl Exclusion Zone (CEZ), where animals were exposed to elevated levels of radionuclides, and from uncontaminated areas near Kyiv, Ukraine. Counter to expectations, we did not observe a strong DNA damage response in animals exposed to radionuclides, although some signs of oxidative stress were identified. Rather, exposure to environmental radionuclides was associated with upregulation of genes involved in lipid metabolism and fatty acid oxidation in the livers - an apparent shift in energy metabolism. Moreover, using stable isotope analysis, we identified that fur from bank voles inhabiting the CEZ had enriched isotope values of nitrogen: such an increase is consistent with increased fatty acid metabolism, but also could arise from a difference in diet or habitat between the CEZ and elsewhere. In livers and spleens, voles inhabiting the CEZ were characterized by immunosuppression, such as impaired antigen processing, and activation of leucocytes involved in inflammatory responses. In conclusion, exposure to low dose environmental radiation impacts pathways associated with immunity and lipid metabolism, potentially as a stress-induced coping mechanism.

Exposure to environmental radionuclides associates with tissue-specific impacts on telomerase expression and telomere length.

Telomeres, the protective structures at the ends of chromosomes, can be shortened when individuals are exposed to stress. In some species, the enzyme telomerase is expressed in adult somatic tissues, and potentially protects or lengthens telomeres. Telomeres can be damaged by ionizing radiation and oxidative stress, although the effect of chronic exposure to elevated levels of radiation on telomere maintenance is unknown for natural populations. We quantified telomerase expression and telomere length (TL) in different tissues of the bank vole Myodes glareolus, collected from the Chernobyl Exclusion Zone, an environment heterogeneously contaminated with radionuclides, and from uncontaminated control sites elsewhere in Ukraine. Inhabiting the Chernobyl Exclusion Zone was associated with reduced TL in the liver and testis, and upregulation of telomerase in brain and liver. Thus upregulation of telomerase does not appear to associate with longer telomeres but may reflect protective functions other than telomere maintenance or an attempt to maintain shorter telomeres in a stressful environment. Tissue specific differences in the rate of telomere attrition and apparent radiosensitivity weaken the intra-individual correlation in telomere length among tissues in voles exposed to radionuclides. Our data show that ionizing radiation alters telomere homeostasis in wild animal populations in tissue specific ways.