A gut bacterial supplement for Asian honey bee (Apis cerana) enhances host tolerance to nitenpyram: Insight from microbiota–gut–brain axis

Abstract

The widespread use of neonicotinoid pesticides has severely impacted honey bees, driving population declines. Gut microbiota are increasingly recognized for their role in mitigating pesticide toxicity. This study evaluated the ability of Gilliamella sp. G0441, a core microbiome member of the Asian honey bee (Apis cerana), to confer resistance to the toxicity of a neonicotinoid nitenpyram. Newly emerged Asian honey bees were first colonized with gut microbiota in the source colony, then divided into four treatments: SS (fed sucrose solution throughout), SN (fed sucrose solution, then exposed to nitenpyram), GS (fed Gilliamella, then sucrose solution), and GN (fed Gilliamella, then exposed to nitenpyram), and their responses—mortality, food consumption, body weight, and sucrose sensitivity—were assessed. The protective effects of Gilliamella administration on the host were further validated using a microbiota-free bee model. Gilliamella supplementation significantly mitigated nitenpyram-induced appetite suppression, weight loss, impaired learning, and gut microbiota disruption. Mechanistic analyses revealed that nitenpyram disrupted brain metabolism via the intestinal MAPK pathway, reducing ascorbate and aldarate metabolism. Prophylactic Gilliamella treatment reversed these effects, restored metabolic balance, and modulated esterase E4 expression, enhancing pesticide resistance. This study underscores Gilliamella's vital role in honey bee resilience to neonicotinoids, offering insights into the microbiota-gut-brain axis (MGBA) as a pathway for enhancing pesticide tolerance and ecological health.