Impacts of radiation exposure on the bacterial and fungal microbiome of small mammals in the Chernobyl Exclusion Zone.

Rachael E Antwis,Catherine L Barnett,Michael D Wood,Ross Fawkes,Elaine Potter,Sergey Gaschak,Lee Walker,Joseph A Jackson,Nicholas A Beresford

doi:10.1111/1365-2656.13507

Abstract

Environmental impacts of the 1986 Chernobyl Nuclear Power Plant accident are much debated, but the effects of radiation on host microbiomes have received little attention to date. We present the first analysis of small mammal gut microbiomes from the Chernobyl Exclusion Zone in relation to total absorbed dose rate, including both caecum and faeces samples. We provide novel evidence that host species determines fungal community composition, and that associations between microbiome (both bacterial and fungal) communities and radiation exposure vary between host species. Using ambient versus total weighted absorbed dose rates in analyses produced different results, with the latter more robust for interpreting microbiome changes at the individual level. We found considerable variation between results for faecal and gut samples of bank voles, suggesting faecal samples are not an accurate indicator of gut composition. Associations between radiation exposure and microbiome composition of gut samples were not robust against geographical variation, although we identified families of bacteria (Lachnospiraceae and Muribaculaceae) and fungi (Steccherinaceae and Strophariaceae) in the guts of bank voles that may serve as biomarkers of radiation exposure. Further studies considering a range of small mammal species are needed to establish the robustness of these potential biomarkers.

Highlights

Previous studies in the Chernobyl Exclusion Zone (CEZ) have only considered the bacterial microbiome of one small mammal species using faecal samples; here we report on the faecal microbiome of four small mammal species using faecal samples, as well as the first direct analysis of the gut microbiome using caecum samples from bank voles
We found evidence that faecal communities are associated with radiation exposure independent of geographic location, but that these communities were not representative of true gut communities
We have identified two bacterial (Lachnospiraceae and Muribaculaceae) and two fungal (Steccherinaceae and Strophariaceae) families in the guts of bank voles, which may serve as biomarkers of exposure to radiation

Summary

| MATERIALS AND METHODS

The study was undertaken in line with ethical approval obtained from the University of Salford. We used Spearman's rank correlation (with Benjamini–Hochberg corrected p values and False Discovery Rate adjustment) in the associate function of the microbiome package (Lahti & Shetty, 2017) to identify relationships between the two radiation dose measures (ambient and total) and clr-transformed 16S and ITS rRNA sequence data, agglomerated to genus level These analyses were conducted separately for the gut and faecal samples, according to host species. The PERMANOVA showed total absorbed dose rate category (F1,128 = 3.096, R2 = 0.022, p = 0.001), site category (i.e. inside or outside the Red Forest; F1,128 = 2.266, R2 = 0.016, p = 0.001; Figure S8) and sampling site (F14,128 = 1.549, R2 = 0.156, p = 0.001) had a detectable effect on bacterial community beta-diversity of bank vole guts, but sex did not (F1,128 = 1.219, R2 = 0.009, p = 0.056).

Findings

| DISCUSSION

| CONCLUSIONS