Cadmium disrupts energy metabolism in the Harmonia axyridis via mediating trehalose metabolism pathway: A multi-omics analysis

Cadmium (Cd), a ubiquitous heavy metal pollutant, threatens the ecological functions of the natural enemy insect Harmonia axyridis, though the molecular mechanisms of its toxicity remain poorly understood. Here, we first determined the 48-h median lethal concentration (LC₅₀) of Cd for third‑instar H. axyridis larvae as 7.667 mg/mL. Using a multi‑omics approach, we then analyzed larval responses to injected Cd stress at LC₂₅, LC₅₀, and LC₇₅ concentrations. Transcriptomics revealed 1986, 1471, and 1433 differentially expressed genes (DEGs) in the respective treatment groups, including down‑regulated genes encoding α,α‑trehalase (TRE) and maltase‑glucoamylase involved in carbohydrate metabolism. Metabolomics identified 907, 294, and 511 differential metabolites (DMs) across the three Cd exposures, with significant accumulation of sucrose and sucrose 6'‑phosphate in the LC₅₀ group. Integrated omics analysis showed that both DEGs and DMs were co‑enriched in starch and sucrose metabolism and galactose metabolism pathways. Furthermore, Cd transferred through the soil‑plant‑aphid‑ladybug food chain disrupted trehalose metabolism, leading to reduced carbohydrate levels, suppressed trehalase activity, and altered expression of key metabolic genes. Together, these results indicate that Cd‑induced downregulation of trehalose‑related genes causes upstream carbohydrate accumulation (e.g., sucrose) and disrupts the trehalose metabolic pathway, ultimately impairing energy homeostasis. This study uncovers a novel mechanism by which heavy metal pollution affects natural enemy insects via metabolic interference. Our findings highlight the potential disruption of pest control in agroecosystems under heavy metal stress and provide critical molecular targets for assessing the ecological risk of Cd pollution on beneficial insects.