Chronic exposure to lead and cadmium pollution results in genomic instability in a model biomonitor species (Apodemus flavicollis Melchior, 1834)

Polymetal dust is a common industrial pollutant. While the use of remediation filters and equipment in lead smelters has reduced pollutant emission, surrounding areas remain contaminated due to the long-term transfer of heavy metals along the food chain. Here we assess the mutagenic potential of the lead-zinc smelter near Plovdiv (Bulgaria) situated in an area that has been contaminated with heavy metals for 60 years. We aimed to evaluate the genomic response of the yellow-necked mouse (A. flavicollis), a biomonitor species, in three sampling sites along the pollution gradient. Mice from Strandzha Natural Park were used as a negative control. The bioaccumulation rate of two non-essential heavy metals, lead (Pb) and cadmium (Cd), in liver tissues was determined by atomic absorption spectroscopy. Genetic alterations attributable to chronic exposure to trace levels of heavy metals were assessed in different blood cell populations using two independent methods: a micronucleus test was applied to evaluate the clastogenic and aneugenic alterations in erythrocytes, while a comet assay was used to assess DNA instability, as evidenced by single- and double-stranded breaks and alkali-labile sites, in leucocytes. We observed elevated levels of Pb and Cd in livers derived from mice from the impacted area: the mean Pb concentration (21.38 ± 8.77 μg/g) was two-fold higher than the lowest-observed-adverse-effect levels (LOAELs), while the mean Cd concentration (13.95 ± 9.79 μg/g) was extremely close to these levels. The mean levels of Pb and Cd in livers derived from mice from the impacted area were 31-fold and 63-fold higher, respectively, than the levels measured in mice from the control area. The mean frequency of micronuclei was significantly higher (four-fold) than that observed in the control animals. Furthermore, parameters measured by the comet assay, % tail DNA, tail length and tail moment, were significantly higher in the impact area, indicating the degree of genetic instability caused by exposure to heavy metals. In conclusion, this study shows that despite the reported reduction in lead and cadmium emissions in Bulgaria in recent years, A. flavicollis individuals inhabiting areas subject to long-term contamination exhibit significant signs of DNA damage.