Simple SummaryApostichopus japonicusis a temperate marine invertebrate and an economically important aquatic echinoderm species in China. As a benthic organism, sea cucumbers feed on small benthic particulate matter and are easily affected by pollutants. Therefore, for conservation purposes, it is important to elucidate the effects of specific pollutants on these animals. Bisphenol A (BPA) has been identified as an endocrine disruptor that functions as an estrogen analog and typically causes reproductive toxicity by interfering with the endocrine system. We identified the G protein-coupled estrogen receptor 1 inA. japonicusand found that both BPA and estradiol could activate the estrogen-receptor-mediated mitogen-activated protein kinase signaling pathway. Using biological approaches, we have confirmed the estrogen-analog bioactivity of BPA on sea cucumbers by direct interaction with the estrogen receptor. We also determined that BPA affects the reproduction of sea cucumbers by metabolic disruption in ovary tissue.AbstractThe sea cucumber,Apostichopus japonicus,is a marine benthic organism that feeds on small benthic particulate matter and is easily affected by pollutants. Bisphenol A (BPA, 4,4′-isopropylidenediphenol) has been identified as an endocrine disruptor. It is ubiquitously detectable in oceans and affects a variety of marine animals. It functions as an estrogen analog and typically causes reproductive toxicity by interfering with the endocrine system. To comparatively analyze the reproductive effects of estradiol (E2) and BPA on sea cucumbers, we identified a G protein-coupled estrogen receptor 1 (GPER1) inA. japonicusand investigated its effects on reproduction. The results showed that BPA and E2exposure activatedA. japonicusAjGPER1, thereby mediating the mitogen-activated protein kinase signaling pathways. High-level expression ofAjGPER1in the ovarian tissue was confirmed by qPCR. Furthermore, metabolic changes were induced by 100 nM (22.83 μg/L) BPA exposure in the ovarian tissue, leading to a notable increase in the activities of trehalase and phosphofructokinase. Overall, our findings suggest that AjGPER1 is directly activated by BPA and affects sea cucumber reproduction by disrupting ovarian tissue metabolism, suggesting that marine pollutants pose a threat to the conservation of sea cucumber resources.