Trophic transfer of chromium from Bellamya aeruginosa drives edema in medicinal leech Whitmania pigra via the ROS-FoxO-ENaC signaling.

Environmental accumulation of chromium in aquatic food webs presents a growing threat to animal and human health. While previous studies established a link between intestinal dysbiosis and Whitmania pigra edema disease (WPE), the underlying mechanisms remain poorly understood. In this study, we demonstrate that Bellamya aeruginosa collected from polluted freshwater habitats bioaccumulates Cr and transmits it through the food chain, inducing WPE under the conditions of this experiment. Cr (VI) exposure via feeding or immersion led to disrupted gut microbiota, elevated reactive oxygen species (ROS), and suppressed of the FoxO signaling axis in W. pigra. This redox imbalance altered expression of epithelial sodium channels (ENaCα) and Na⁺/K⁺-ATPase, impairing osmotic regulation and leading to fluid retention. Furthermore, Cr (VI) triggered caspase-9-dependent mitochondrial apoptosis pathway in intestinal and muscular tissues, and upregulated inflammatory cytokines. Importantly, toxicokinetic modeling revealed preferential Cr accumulation in visceral tissues of B. aeruginosa, which could be effectively mitigated through a 16-20 day depuration period in clean water. These findings provide mechanistic evidence for Cr (VI) trophic toxicity and support practical remediation strategies to ensure feed safety and environmental health.