Dietary Contamination with a Neonicotinoid (Clothianidin) Gradient Triggers Specific Dysbiosis Signatures of Microbiota Activity along the Honeybee (Apis mellifera) Digestive Tract

Abstract

Pesticides are increasing honeybee (Apis mellifera) death rates globally. Clothianidin neonicotinoid appears to impair the microbe–immunity axis. We conducted cage experiments on newly emerged bees that were 4–6 days old and used a 16S rRNA metataxonomic approach to measure the impact of three sublethal clothianidin concentrations (0.1, 1 and 10 ppb) on survival, sucrose syrup consumption and gut microbiota community structure. Exposure to clothianidin significantly increased mortality in the three concentrations compared to controls. Interestingly, the lowest clothianidin concentration was associated with the highest mortality, and the medium concentration with the highest food intake. Exposure to clothianidin induced significant variation in the taxonomic distribution of gut microbiota activity. Co-abundance network analysis revealed local dysbiosis signatures specific to each gut section (midgut, ileum and rectum) were driven by specific taxa. Our findings confirm that exposure to clothianidin triggers a reshuffling of beneficial strains and/or potentially pathogenic taxa within the gut, suggesting a honeybee’s symbiotic defense systems’ disruption, such as resistance to microbial colonization. This study highlights the role of weak transcriptional activity taxa in maintaining a stable honeybee gut microbiota. Finally, the early detection of gut dysbiosis in honeybees is a promising biomarker in hive management for assessing the impact exposure to sublethal xenobiotics.