Earthworm stress transcriptomics exposed to mine tailings

Global demand for critical minerals is driving extensive mining projects with the unfortunate generation of immense amounts of mine waste. Mine tailings include large contents of potentially harmful elements including Pb and Zn. The characterization and the rehabilitation of industrial residue sites and mine tailings in Ireland represents an important challenge for the environment. While different rehabilitation strategies have been well studied based on plant performance and geochemical analyses, there is much less information available about the impacts of mine tailing and their rehabilitation on soil infauna, including earthworms, despite their essential role in soil ecology. This study fills an important gap by exploring the bioavailability, potential transfer, and toxicity for key metal contaminants in the earthworm Eisenia fetida exposed different dilutions of Pb/Zn mine tailings. We performed chronic exposures following standard guidelines, measured element concentrations in worms, and investigated targeted stress biomarkers along with transcriptomics on earthworm coelomocytes. Earthworms accumulated potentially toxic levels of Arsenic (As), Lead (Pb) and Zinc (Zn). Biomarkers responses revealed an upregulation of Heat shock protein 70 (HSP70) expression which was correlated with bioaccumulated As levels and catalase (CAT) expression was decreased in the 75% mine tailings treatment. Our transcriptomics study provided the first high quality coelomocyte transcriptome for E. fetida with 98,553 genes. We identified 24 transcripts that were responsive to the mine tailings treatments including a non-receptor tyrosine protein kinase, upregulated across all treatments, genes involved in protease assembly, mitochondrial transport, a methylcytocine dioxygenase, and several transcripts with homology to arginase I. Overall, our results reveal that earthworms respond to Pb/Zn tailings through cellular stress responses in immune cells that are correlated with As bioaccumulation. These findings suggest that Pb/Zn mine tailing remediation is feasible and not likely to result in acute toxicity to soil infauna, but As levels should be monitored and methods to sequester or immobilize the As should be pursued to reduce chronic impacts.