Exposure to environmental radionuclides is associated with altered metabolic and immunity pathways in a wild rodent

Abstract

Wildlife inhabiting environments contaminated by radionuclides face putative detrimental effects of exposure to ionizing radiation, with biomarkers such as an increase in DNA damage and/or oxidative stress commonly associated with radiation exposure. To examine the effects of exposure to radiation on gene expression in wildlife, we conducted a de novo RNA sequencing study of liver and spleen tissues from a rodent, the bank vole Myodes glareolus. Bank voles were collected from the Chernobyl Exclusion Zone (CEZ), where animals were exposed to elevated levels of radionuclides, and from uncontaminated areas near Kyiv, Ukraine. Counter to expectations, we did not observe a strong DNA damage response in animals exposed to radionuclides, although some signs of oxidative stress were identified. Rather, exposure to environmental radionuclides was associated with upregulation of genes involved in lipid metabolism and fatty acid oxidation in the livers – an apparent shift in energy metabolism. Moreover, using stable isotope analysis, we identified that fur from bank voles inhabiting the CEZ had enriched isotope values of nitrogen: such an increase is consistent with increased fatty acid metabolism, but also could arise from a difference in diet or habitat between the CEZ and elsewhere. In livers and spleens, voles inhabiting the CEZ were characterized by immunosuppression, such as impaired antigen processing, and activation of leucocytes involved in inflammatory responses. In conclusion, exposure to low dose environmental radiation impacts pathways associated with immunity and lipid metabolism, potentially as a stress‐induced coping mechanism.

Infection Load and Prevalence of Novel Viruses Identified from the Bank Vole Do Not Associate with Exposure to Environmental Radioactivity

“…Thus, a greater diversity of bank vole viruses are likely to be uncovered given an increased sampling effort across the bank vole's geographic distribution. To estimate whether viruses had caused long-term adverse effects in these five animals, we compared their body condition index to the animals without virus reads in spleen or liver [40,62]. The body condition index was calculated as the standardized residual values from a linear regression of weight against head width, where positive values reflect better body condition.…”

“…Parvoviruses are non-enveloped viruses with two terminal hairpin structures, which prime replication [39]. Parvoviruses infect vertebrate (Parvovirinae) and invertebrate (Densovirinae) hosts [40]. The subfamily Parvovirinae is divided into eight genera based on the proteins they transcribe: Amdoparvovirus, Aveparvovirus, Bocaparvovirus, Dependoparvovirus, Erythroparvovirus, Copiparvovirus, Protoparvovirus, and Tetraparvovirus [54].…”

“…We used spleen and liver RNA-sequencing data for bank voles from Ukraine [40] (NCBI SRA: SRP15797) to test whether the plasma viruses were able to produce systemic infection. Since the RNA-sequencing data were poly-A selected and the genomes of mosavirus and hepacivirus sequences did not have a clear poly-A track, our analysis might have underestimated viral load by showing fewer virus sequences than actually existed in the samples for these viruses.…”

“…Virus activation by irradiation may be facilitated by radiation-mediated immunosuppression that makes the host more susceptible to virus infection and replication [33][34][35], or by radiation-induced activation of the DNA repair proteins that some viruses utilize in their replication [36,37]. Wild bank voles exposed to chronic low-dose (up to 20 µGy/h) environmental radiation show activated transcription of DNA repair proteins [38] and inhibited apoptosis [39], and show signs of immunosuppression [40]. As these processes may support virus replication, we predicted an elevated viral load in bank voles inhabiting areas contaminated by radionuclides compared with uncontaminated areas.…”

Exposure to environmental radionuclides alters mitochondrial DNA maintenance in a wild rodent

“…heteroplasmy, in muscle tissue of bank voles inhabiting the CEZ (Kesäniemi et al 2018). While changes in gene expression are observed in voles inhabiting the contaminated CEZ areas (Kesäniemi et al 2019a), the elevated level of genetic variation seen using mitochondrial markers in bank voles within the CEZ is explained by demographic processes rather than exposure to environmental radiation (Meeks et al 2009). More generally, our data show how human impacts on the environment can affect mitochondrial dynamics in wildlife.…”