Earthworm survival adaptations to arsenate exposure: Links between behavioral inhibition, mitochondrial dysfunction, and oxidative stress responses

Abstract

The threshold for arsenic (As) in agricultural soils is increasing, posing a significant risk to human health through the food chain. The efficacy of vermiremediation to remove As has been constrained by the limited understanding of earthworms' survival adaptions. Hence, the present study aimed to investigate the responses and underlying potential mechanisms of Eisenia fetida to arsenate (As-V). The RT-PCR and enzyme analysis results showed that the antioxidant system regulated their expressions, thus maintaining the balance of generating and eliminating reactive oxygen species (ROS). Accumulated ROS attacked the mitochondrial respiratory chain, and upregulated complex gene expressions to mitigate the decreases in respiratory intensity and ATP levels. Subsequently, the inhibitory effects on feeding, digestion, and reproduction behavior were observed. These findings elucidated the dose-dependent effects of As-V on earthworm biomass loss and mortality, which exhibited 34.4 % and 33.3 % increments, respectively, at As exposure of 200 mg/kg after 28 days. Furthermore, “U-shaped” curves indicated that earthworms had a potential As tolerance threshold of 100 mg/kg. A stress response index (SRI) showed that As-V had a dose-dependent effect on earthworm integrative stress, with an observed potential adaptive inflection point after prolonged exposure time. Partial least squares path modelling (PLS-PM) confirmed that oxidative stress predominantly influenced earthworm survival, with a path coefficient of 0.52. Oxidative stress had a positive regulatory effect by influencing mitochondrial function and inhibiting behavioral activity. These findings provide insights for comprehensive understanding of earthworm survival adaptation to As-V, and help to diagnose, assess and remediate soil As contamination.