Low-temperature-induced disruption of reproductive axis and sperm vitality via stress axis in Monopterus albus

Abstract

The ricefield eel (Monopterus albus) is inherently timid and highly sensitive to stress. Our previous studies have shown that low-temperature weather could significantly affect the sperm vitality of ricefield eels. This study aims to investigate the regulatory mechanism of low-temperature effects on testicular function and sperm vitality in ricefield eels. The ricefield eels were initially reared at low (10 °C) and normal (25 °C) temperatures for 24 h. Low temperatures were found to induce the expression of pituitary pro-opiomelanocortin (POMC) and testes insulin-like growth factor-binding protein 1 (IGFBP1) mRNA expression, suggesting that the reduction in sperm vitality could be attributed to the activation of the stress axis. Moreover, the results indicated a significant decrease in sperm occupancy and count in the testes, along with a reduced percentage of motile sperm. Subsequent transcriptome analysis showed substantial inhibition of reproductive hormone genes (gnrh1, lh, and fsh) in the brain and pituitary, and downregulation of meiosis-related genes (dmc1, rec8, and sycp3) in the testes. These findings suggest that low temperatures might disrupt testicular development and spermatogenesis by inhibiting the reproductive axis. Metabolomics analysis then demonstrated a significant reduction in the levels of metabolites related to glycolysis, fatty acid metabolism, and the tricarboxylic acid (TCA) cycle in the testes after low-temperature treatment. Interestingly, the expression of zona pellucida sperm-binding proteins 3 and 4 (ZP3 and ZP4), which may affect sperm vitality and spermatogenesis, was significantly induced by low temperatures in the testes. In conclusion, these findings suggested that low temperatures might affect testicular function and sperm vitality by simultaneously activating the stress axis and inhibiting the reproductive axis and energy metabolism in the testes.