Mild chronic exposure to pesticides alters physiological markers of honey bee health without perturbing the core gut microbiota

The honey bee gut hosts a specialized microbiota that plays a critical role in bee health through the stimulation of the immune system and an involvement in digestion. However, the gut also constitutes the primary site of exposure to a wide variety of pesticides ingested by honey bees during foraging, and feeding on stored honey and beebread. Recent studies highlighted that exposure to glyphosate can have negative effects on specific members of the core gut microbiota of honey bee workers. However, these studies exposed bees to relatively high glyphosate concentrations and did not assess the possible interactions with other pesticides. Here, we chronically exposed newly emerged honey bees to an environmental concentration of imidacloprid, glyphosate and difenoconazole, individually and in ternary mixture. We studied the effects of these exposures on the establishment of the gut microbiota, the physiological status, the longevity, and food consumption of the host. The core bacterial species were not affected by the exposure to the three pesticides at these environmental concentrations. Negative effects were observed but they were restricted to few transient non-core bacterial species. However, in the absence of the core microbiota, the pesticides induced physiological disruption by directly altering the detoxification system, the antioxidant defenses, and the metabolism of the host. Our study indicates that even mild exposure to pesticides can directly alter the physiological homeostasis of newly emerged honey bees and particularly if the individuals are dysbiotic (i.e. mostly lack the core microbiota). This highlights the importance of an early establishment of a healthy gut bacterial community to strengthen the natural defenses of the honey bee against xenobiotic stressors.