Prediction of adverse effects of effluents containing phenolic compounds in the Ba River on the ovary of fish (Hemiculter leucisculus) using transcriptomic and metabolomic analyses

Abstract

The aim of this work was to evaluate the endocrine disrupting effects on the ovarian development of sharpbelly (Hemiculter leucisculus) caused by effluents containing phenolic compounds. This was achieved using integrated transcriptomic and metabolomic analyses, along with histopathological examinations. Sharpbelly, an indigenous freshwater fish widely distributed in East Asia, were collected by pole fishing from three sampling sites in the Ba River. These sampling sites include a mid-stream site near a wastewater outfall and a reference site located upstream and a far field comparison site located downstream. In sharpbelly collected near the wastewater discharge, the oocyte development was activated, compared to the other two sites. Histopathological alterations in the fish ovaries were likely due to the upregulated steroid hormone biosynthesis process, as suggested by the differentially expressed genes (e.g., hsd3b, hsd17b1) and differentially accumulated metabolites (e.g., pregnenolone). Additionally, under the stress of effluents containing phenolic compounds, genes related to the signaling pathways for oxidative phosphorylation and leukocyte transendothelial migration were dysregulated, suggesting the potential induction of inflammation and several ovarian diseases. Overall, these findings suggest that effluents containing phenolic compounds influence ovary development and reproductive function of female sharpbelly. Whether there is any resulting dysfunction of folliculogenesis, abnormality of ovulation, production of premature eggs and/or potential induction of ovarian cancers remains to be determined by further studies, for a better evaluation on effluents containing phenolic compounds to the fish fertility and the health of their offspring, and even the stability of the wild fish population. Notably, the integration of transcriptomics and metabolomics can complement the routine chemical analysis to comprehensively monitor the effects of wastewater treatment plant effluents on the health of wild fish.