Low-level environmental metal pollution is associated with altered gut microbiota of a wild rodent, the bank vole (Myodes glareolus)

Ilia Rodushkin,Phillip C. Watts,Eugene Tukalenko,Ilze Brila,Anton Lavrinienko,Tapio Mappes,Frauke Ecke,Eva R. Kallio

doi:10.1016/j.scitotenv.2021.148224

Abstract

Mining and related industries are a major source of metal pollution. In contrast to the well-studied effects of exposure to metals on animal physiology and health, the impacts of environmental metal pollution on the gut microbiota of wild animals are virtually unknown. As the gut microbiota is a key component of host health, it is important to understand whether metal pollution can alter wild animal gut microbiota composition. Using a combination of 16S rRNA amplicon sequencing and quantification of metal levels in kidneys, we assessed whether multi-metal exposure (the sum of normalized levels of fifteen metals) was associated with changes in gut microbiota of wild bank voles (Myodes glareolus) from two locations in Finland. Exposure to increased metal load was associated with higher gut microbiota species diversity (α-diversity) and altered community composition (β-diversity), but not dispersion. Multi-metal exposure and increased levels of several metals (Cd, Hg, Pb and Se) were associated with differences in the abundance of microbial taxa, especially those within the families Clostridiales vadinBB60 group, Desulfovibrionaceae, Lachnospiraceae, Muribaculaceae and Ruminococcaceae. Our data indicate that even low-level metal pollution can affect the diversity of microbiota and be associated with deterministic differences in composition of host gut microbiota in wild animal populations. These findings highlight the need to study a broader range of metals and their cocktails that are more representative of the types of environmental exposure experienced by wild animals.

Highlights

Anthropogenic release of metals into the environment is an important cause of stress and detrimental health effects in many wildlife populations (Acevedo-Whitehouse and Duffus, 2009)
Community composition was affected by host traits (BCI and sex), and environmental factors (Table S7)
Gut microbiota is thought to be an important part of wildlife health, but little is known about the association between anthropogenic environmental disturbance and gut microbiota diversity and composition

Summary

Introduction

Anthropogenic release of metals into the environment is an important cause of stress and detrimental health effects in many wildlife populations (Acevedo-Whitehouse and Duffus, 2009). Biological impacts of exposure to metals are diverse, including effects on metabolism, reproduction and functioning of immune and nervous systems (Sparling, 2017), depending on the metal, dose, organism affected and its developmental timing of exposure. While diverse effects of exposure to metal pollution on organisms have been quite well-studied, it is less clear whether metal pollution is associated with an impact on the community of host-associated microbes in natural populations. Host's gut microbiota can be influenced by factors such as host's diet (David et al, 2014; Youngblut et al, 2019), reproductive status (Mallott et al, 2020) and age (Heitlinger et al, 2017)

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