Perfluorooctanoic acid accumulation in honeybee tissues and its impact on the immune system and gut microbiota

Perfluorooctanoic acid (PFOA) is not only a pressing environmental concern in oceans, but also in terrestrial ecosystems. However, little is known about its potential impacts on pollinators. Here, we evaluated the physical and biological effects of different concentrations of PFOA (0.1 and 1 mg/L) on Apis cerana cerana . Exposure to PFOA reduced survival rate and body weight, with preferential gut enrichment. Histopathology revealed that PFOA caused thinning of the midgut wall, damage to the peritrophic membrane, and degradation of the basement membrane. Activities of enzymes in midgut, including amylase, protease, and lipase, were inhibited. Mechanistic studies indicated that PFOA induced intestinal cell apoptosis by up-regulating the expression of Caspase-3 / 8 gene and accumulating reactive oxygen species. Meanwhile, PFOA inhibited honeybees' detoxification genes, antioxidant and antimicrobial peptide genes, and affected the activities of key enzymes. Additionally, PFOA altered gut microbiota structure, decreasing Lactobacillus abundance and enriching Snodgrassella and Gilliamella , with down-regulated energy-related pathways. This study reveals that PFOA exerts its toxicity through multiple ways, including gut damage, immune suppression and disruption of microbiota. It provides important evidence for assessing the risks of PFOA to pollinators and also shed light on the potential effects of PFOA in terrestrial ecosystems. • PFOA causes gut damage and reduces the digestive capacity of bees. • PFOA induces the accumulation of ROS in the gut and promotes gut cell apoptosis. • The presence of PFOA can elicit antioxidant and detoxification responses in bees. • The presence of PFOA influences changes in the gut microbiome. • Alterations in gut microbiome functionality have the potential to affect host physiology.