Copper-based nanoparticles trigger fitness decline in parasitoid wasps via gut microbiota-induced fatty acid...

The application of copper-based nanoparticles (Cu-based NPs, e.g., CuO-NPs and Cu-NPs) as nanopesticides represents a promising avenue for sustainable agriculture. However, their potential ecotoxicological effects on beneficial arthropods, particularly parasitoid wasps which are crucial for biological pest control, remain poorly understood. Here, we investigated the chronic toxicity of CuO-NPs and Cu-NPs to the endoparasitoid wasp Asobara japonica and elucidated the underlying mechanisms. We found that dietary exposure induced concentration-dependent lethality, primarily driven by released copper ions rather than the particles themselves. Sublethal exposure severely impaired wasp fitness, with reduced host-searching locomotion thereby mediating a decline in parasitism efficiency. Mechanistically, integrated transcriptomic and metabolomic analyses revealed a coordinated downregulation of some key genes in fatty acid homeostasis pathways and a consequent decline in free fatty acid levels. This disruption in energy mobilization likely compromised the energy supply necessary for sustained activity, thereby explaining the observed locomotion behavioral deficits. Furthermore, Cu-based NPs exposure selectively altered the rare gut microbiota, and shifts in specific bacterial genera correlated with the suppression of host fatty acid metabolism genes. Our results demonstrate that Cu-based NPs impair parasitoid wasp fitness through the disruption of gut microbiome homeostasis and energy metabolism, highlighting the need to consider these impacts in nanomaterial risk assessment for sustainable agriculture.