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

Anton Lavrinienko,Eugene Tukalenko,Rasmus Hindström,Timothy A Mousseau,Anni Hämäläinen,Phillip C Watts,Zbyszek Boratyński,Kati Kivisaari,Tapio Mappes

doi:10.1111/mec.15945

Abstract

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.

Highlights

Gut microbiota provide many essential services to their animal hosts, including provision of diverse metabolites and nutrients, and protection against pathogens and toxic compounds (Parfrey et al, 2018; Suzuki, 2017)
We directly compared the generality of radiation-associated changes in the bank vole gut microbiota to the patterns observed in A. flavicollis and A. sylvaticus; we examined three species that occur in sympatry in habitats affected by the Chernobyl nuclear accident
Species identity is thought to dominate over environment in shaping wild rodent gut microbiota (Knowles et al, 2019), but it remains unknown whether host gut microbiota responses to similar anthropogenic habitat characteristics are species-specific or comparable across host species

Summary

| INTRODUCTION

Gut microbiota provide many essential services to their animal hosts, including provision of diverse metabolites and nutrients, and protection against pathogens and toxic compounds (Parfrey et al, 2018; Suzuki, 2017) As persistence of these functions impact host health, variation of the gut microbiota composition holds importance for determining animals’ adaptive potential in the face of environmental change (Alberdi et al, 2016). Bank voles inhabiting areas contaminated by radionuclides can be identified by their distinct gut microbiota It remains unknown whether such gut microbiota responses to radiation exposure are specific to bank voles or represent a more general pattern similar across other wild rodents from Chernobyl, or even other nuclear accident sites contaminated with radionuclides, such as Fukushima. We predicted (ii) that such altered community composition would be characterized by an increase in the ratio of the Firmicutes to Bacteroidetes phyla (F:B), which could possibly act as a “biomarker” of exposure to radiation; (iii) that exposure to radiation would have little notable effect on the diversity of mouse gut microbiota; and (iv) that exposure to radiation would select for distinct gut microbiota structure in wild mice as found for bank voles

| MATERIALS AND METHODS

| Study design

| RESULTS

Findings

| DISCUSSION