Trophic Transfer of Metal Oxide Nanoparticles in the Tomato- Food Chain: Effects on Phyllosphere Microbiota, Insect Oxidative Stress, and Gut Microbiome.

Understanding the trophic transfer and ecological cascade effects of nanofertilizers and nanopesticides in terrestrial food chains is crucial for assessing their nanotoxicity and environmental risks. Herein, the trophic transfer of LaO (nLaO) and CuO (nCuO) nanoparticles from tomato leaves to (Lepidoptera: Noctuidae) caterpillars and their subsequent effects on caterpillar growth and intestinal health were investigated. We found that 50 mg/L foliar nLaO and nCuO were transferred from tomato leaves to , with particulate trophic transfer factors of 1.47 and 0.99, respectively. While nCuO exposure reduced larval weight gain more (34.7%) than nLaO (11.3%), owing to higher oxidative stress (e.g., MDA and HO) and more serious intestinal pathological damage (i.e., crumpled columnar cell and disintegrated goblet cell) by nCuO. Moreover, nCuO exposure led to a more compact antagonism between the phyllosphere and gut microbiomes compared to nLaO. Specifically, nCuO exposure resulted in a greater increase in pathogenic bacteria (e.g., , , and ) and a more significant decrease in probiotics (e.g., and ) than nLaO, ultimately destroying larval intestinal immunity. Altogether, our findings systematically revealed the cascade effect of metal oxide nanomaterials on higher trophic consumers through alteration in the phyllosphere and insect gut microbiome interaction, thus providing insights into nanotoxicity and environmental risk assessment of nanomaterials applied in agroecosystems.