Juvenile apple snails as new biomonitors of freshwater pollution: Insight into copper and lead toxicity and underlying molecular mechanisms

Abstract

Environmental pollutants, such as heavy metals, pose significant threats to organisms across different trophic levels in the aquatic environment. Although the effects of heavy metals have been extensively studied in a limited number of model organisms, their toxicity and underlying mechanisms remain poorly understood in numerous aquatic invertebrates. Here, we underscore the potential of the apple snail Pomacea canaliculata as an environmental bioindicator for freshwater heavy metal pollution, advancing biomonitoring methodologies. By integrating physiological, enzymatic, transcriptomic, and proteomic analyses, we conducted a thorough evaluation of the toxic effects and mechanisms of copper (Cu) and lead (Pb) on juvenile snails. Our results demonstrated that juvenile P. canaliculata was more sensitive to Cu and Pb compared with other aquatic invertebrates with heart rate drop serving as a reliable indicator of metal exposure. Antioxidant enzyme activity exhibited a distinct response, increasing at low Pb concentrations but decreasing at high concentrations, while Cu suppressed the activity even at a low concentration. At the molecular level, a total of 467 and 267 differentially expressed genes and 629 and 204 differentially expressed proteins were identified in the juveniles exposed to sublethal concentrations of Cu (40 μg/L) and Pb (1500 μg/L) for 72 h, respectively. Functional analysis further revealed distinct molecular toxicity in P. canaliculata. Under Pb exposure, key pathways related to cellular oxidant detoxification, transmembrane transporter activity, and ATP hydrolysis activity were enriched, while Cu significantly activated chitin binding, oxidoreductase activity and extracellular region. Overall, our findings highlight the exceptional capacity of P. canaliculata juveniles to differentiate the toxicity and molecular toxic mechanisms of heavy metals, establishing this species as an important and sensitive biomonitor for accurately assessing freshwater heavy metal pollution. This advancement enhances our understanding of ecological health and offers valuable tools for policymakers and conservationists to address the impacts of environmental contaminants.