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

Abstract

BackgroundAnimal 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.ResultsSkin 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.ConclusionsBank 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.Electronic supplementary materialThe online version of this article (10.1186/s40168-018-0595-0) contains supplementary material, which is available to authorized users.

Assessing similarities and disparities in the skin microbiota between wild and laboratory populations of house mice

“…Of note, farm is nearly the only factor found to influence microbial traits in the standing communities, whereas other factors such as weight and BMI are significant for many traits in the active communities. Further, similar to other studies reporting an influence of geography on the composition of skin microbiota of wild mammals [14,[29][30][31], we observe a pattern of similarity-distance decay, which is stronger in the standing communities. Taken together, the observation of potential non-skinresident taxa and a more prominent influence of environmental variables or their proxies (similarity-distance decay) at the DNA level suggest that RNA-based profiling may reduce environmental noise in studies of the mouse skin microbiota.…”

“…The house mouse is a key model organism for microbiome research and is intensively studied [20][21][22][23]. Although several studies examined the gut microbiota of free-living mice [24][25][26][27][28] or the skin microbiota of other mammals [14,[29][30][31] still nothing is known about the normal range of variation of skin microbiota in wild house mice, nor how closely the microbial communities of laboratory mice, which are housed under controlled conditions and experience little to no external stimuli, reflect the natural state of microbial composition in the wild.…”

Two hundred and fifty-four metagenome-assembled bacterial genomes from the bank vole gut microbiota

“…We found low (r < 0.2) correlations ( Supplementary Table 6) in the abundances of the MAGs among most pairs of samples (see Supplementary Table 5 for mean coverages per sample and MAG, which were calculated using ANVI'O v.5.2 39,40 as the 'mean coverage of a contig divided by overall sample mean coverage'). Hence, these MAGs exhibit substantial variation in their abundance among individuals and timepoints (Supplementary Table 5), which is consistent with expected levels of inter-individual and temporal variation in rodent gut microbiota community composition 14,[16][17][18] . The notable exceptions to these low pairwise correlations in MAG abundance were the comparisons of MAG abundances between the pairs of independent, replicate DNA extractions (r = 0.999 for samples 25 and T25, and r = 1.000 for samples 69 and T96) (Supplementary Table 6).…”

“…Here we present a description of 254 draft bacterial genomes (MAGs) that we estimate to be 50% or more complete and with ≤10% contamination. Phylogenetic analysis of these MAGs indicates that they comprise a typical gut microbiota for rodents within the superfamily Muroidea [13][14][15][16][17] , being dominated by members of the Bacteroidetes (n = 132) and Firmicutes (n = 80), but with some Spirochaetes (n = 15) and Proteobateria (n = 11) ( Fig. 1).…”

“…the Chernobyl Exclusion Zone, Ukraine (51.30 N, 30.07 E) during May-June (faecal sample 1) and June-July 2016 (faecal sample 2). Full details of the live trapping procedures are provided in Lavrinienko et al 16,17 . All procedures were performed in accordance with legal requirements and regulations from the Ukrainian authorities (957-i/16/05/2016) and the Animal Experiment Board in Finland (ESAVI/7256/04.10.07/2014).…”