Core gut symbionts enhance honeybee (Apis mellifera) resilience to flumethrin stress by upregulating host immunity

The widespread use of flumethrin has significantly jeopardized the survival of bees. However, the mechanisms by which bees and their intestinal microorganisms resist flumethrin remain to be elucidated. Therefore, this study aimed to explore the mechanism by which the gut microbiota of bees assist the bee host in resiling flumethrin stress. Bees were exposed to various concentrations of flumethrin (0.01, 0.1, and 1 mg/L) for 14 days, subsequently, performance parameters (body weight, gut weight, and food intake) and gut microbiota diversity and composition were assessed. Then, the performance parameters and mRNA expression of bees colonized by core gut bacteria (Bombilactobacillus mellis, Lactobacillus apis, Snodgrassella alvi, Bartonella apis, and Gilliamella apicola) and exposed to 1 mg/L flumethrin were evaluated. Chronic flumethrin exposure significantly reduced survival rate and gut weight, damaged intestinal structure, and induced gut microbiota dysbiosis in bees. However, gut colonization by B. mellis, S. alvi, and G. apicola significantly improved survival rate, body weight, and intestinal weight in bees. Importantly, G. apicola colonization significantly enhanced honeybees resilience to flumethrin, as evidenced by a significant increase in survival rate from 65.8 to 94.1% after G. apicola colonization. Moreover, bacterial gut colonization significantly upregulated the mRNA expression of immune detoxification genes, including superoxide dismutase, catalase, Toll, defensin-1, and abaecin, in bees. Collectively, these findings indicate that gut bacteria confer protection against flumethrin-induced stress by enhancing host immunity, underscoring the critical role of the gut microbiota in mediating honeybee resilience to environmental pollutants.