Histopathological and molecular effects on the gills and kidneys of Oligosarcus argenteus chronically exposed to metal-contaminated tailings from the Fundão dam collapse

The Fundão dam failure (2015) was the largest mining-related environmental disaster worldwide; however, the long-term effects of continuous exposure to metals on fish remain poorly understood. Thus, this study conducted a morphological, physiological and molecular evaluation of the gills and kidney of Oligosarcus argenteus exposed to metals from the Fundão dam collapse. Four quarterly samplings were performed at three sites: S1 (Piranga River, reference), S2 (Doce River, directly impacted), and S3 (Doce River, 75 km downstream of S2). The gills and kidney were sampled for morphological, morphometric, immunohistochemical, TUNEL assay, and Western blotting analyses. Metal measurements showed higher levels of Al, Fe, and Mn in the water and As, Fe, and Mn in the sediment at the impacted sites. Structural alterations in the gills and kidney were more pronounced at S2. Several cellular and tissue alterations were detected, and the degree of tissue change (DTC index) was higher at S2 and S3 for both organs. The biomarker proteins metallothionein 1 (MT1), HSP70, catalase (CAT), caspase-3 (CASP3), and HMGB1 were immunolocalized primarily in epithelial, pillar, and ionocyte cells in the gills and renal tubular epithelium in the kidney. Expression of MT1, CAT, and CASP3 was higher in S2 for the gills and kidney, except for MT1 for the latter. Proportion of TUNEL-positive cells was higher in S2 for both organs. We conclude that the physiological effects of contamination from the Fundão dam collapse persist in the long term, including signs of oxidative stress, apoptosis, and necrosis, as well as structural and histopathological changes in fish gills and kidney.