Skin and gut microbiomes of a wild mammal respond to different environmental cues

Abstract

Background: Animal skin and gut microbiomes are important components of host fitness. However, the processes that shape the microbiomes of wildlife are poorly understood, particularly with regard to exposure to environmental contaminants. We used 16S rRNA amplicon sequencing to quantify how exposure to radionuclides impacts the skin and gut microbiota of a small mammal, the bank vole Myodes glareolus, inhabiting areas within and outside the Chernobyl Exclusion Zone (CEZ), Ukraine.

Results: Skin microbiomes of male bank voles were more diverse than females. However, the most pronounced differences in skin microbiomes occurred at a larger spatial scale, with higher alpha diversity in the skin microbiomes of bank voles from areas within the CEZ, whether contaminated by radionuclides or not, than in the skin microbiomes of animals from uncontaminated locations outside the CEZ, near Kyiv. Similarly, irrespective of the level of radionuclide contamination, skin microbiome communities (beta diversity) showed greater similarities within the CEZ, than to the areas near Kyiv. Hence, bank vole skin microbiome communities are structured more by geography than the level of soil radionuclides. This pattern presents a contrast with bank vole gut microbiota, where microbiomes could be strikingly similar among distant (~ 80 km of separation), uncontaminated locations, and where differences in microbiome community structure were associated with the level of radioactivity. We also found that the level of (dis)similarity between the skin and gut microbiome communities from the same individuals was contingent on the potential for exposure to radionuclides.

Conclusions: Bank vole skin and gut microbiomes have distinct responses to similar environmental cues and thus are structured at different spatial scales. Our study shows how exposure to environmental pollution can affect the relationship between a mammalian host's skin and gut microbial communities, potentially homogenising the microbiomes in habitats affected by pollution.

Keywords: Anthropogenic impact; Biodiversity; Ionising radiation; Pollution; Skin microbiome; Wild mammal.

Fig. 1

Map of the study areas with bank vole trapping locations shown by points. Replicate sites within each area (e.g. CH1-3, CL1-2 and KL1-2) are shown, with areas contaminated (CH) and uncontaminated (CL) with radionuclides within the Chernobyl Exclusion Zone (CEZ) and uncontaminated area near Kyiv (KL), Ukraine. Colour of the point indicates differences in environmental radiation levels, CH, red (10–198.7 μGy/h); CL, green (0.12–0.55 μGy/h) and KL, green (0.15–0.55 μGy/h). Dashed line represent the border around the CEZ (area of ~ 2050 km²). Figure was created using ggmap v.2.6.1 package in R

Fig. 2

Measures of alpha diversity for the skin microbiome of bank voles inhabiting areas that differ in levels of environmental radiation. Box-and-whisker plots represent the median and interquartile range of alpha diversity estimates (i.e. number of observed OTUs, Shannon index). Each box plot represent a replicate site from contaminated (CH1-3) and uncontaminated (CL1-2) with radionuclides areas within the Chernobyl Exclusion Zone and uncontaminated area near Kyiv (KL1-2), Ukraine

Fig. 3

Differences in bank vole skin microbiome beta diversity associated with environmental radiation exposure. PCoA on Bray–Curtis dissimilarity distances between bank vole skin microbiome profiles among the three study areas. Each point represents a single sample (n = 151), shape indicate host sex, coloured according to study area: CH, red (n = 64); CL, blue (n = 44); KL, green (n = 43). Ellipses represent a 95% CI around the cluster centroid

Fig. 4

Differences in gut and skin microbiome beta diversity associated with environmental radiation exposure. PCoA on Bray–Curtis dissimilarity distances between bank vole (a) gut and (b) skin microbiomes profiles among the three study areas. Each point represents a single sample (n = 93), shape indicate host sex, coloured according to study area: CH, red (n = 36); CL, blue (n = 28); KL, green (n = 29). Ellipses represent a 75% CI around the cluster centroid for each study area replicate site. Correlation between (c) gut and (d) skin microbiome communities dissimilarity and geographical distance (km) among bank vole trapping locations. The correlation significance was tested using Mantel tests; lines denote the linear regression model

Fig. 5

Community dissimilarity between gut and skin microbiomes within each study area. Box-and-whisker plots represent the median and interquartile range of Bray–Curtis distance between samples. Each box plot represent contaminated (CH) and uncontaminated (CL) with radionuclides study areas within the Chernobyl Exclusion Zone and uncontaminated area near Kyiv (KL), Ukraine

Fig. 6

Random forest (RF) classification of skin and gut microbiomes associated with bank voles inhabiting areas contaminated (CH) and uncontaminated (CL) with radionuclides within the Chernobyl Exclusion Zone and uncontaminated area near Kyiv (KL), Ukraine. a Each row of the confusion matrix from RF analysis represent the study area, the colour intensity indicates within-group coherence and correspond to the fraction of samples that were predicted by the classifier to belong to the study area specified by each column. b Class error estimates indicate the integrity of each study area given the skin and gut microbial communities analysed