Pollen Polysaccharides Drive the Strain-Level Assembly and Competitive Dynamics of Bifidobacterium in the Honeybee Gut

The gut microbiota orchestrates host health by influencing nutrition, immunity, and behavior. Bifidobacterium species are early colonizers maintaining gut homeostasis in honeybees. Despite these critical roles, strain-level dynamics and driving forces behind microbial competition during social transmission remain poorly understood. Here, we established six field-mimicking colonies to track Bifidobacterium communities across successive generations of newly emerged workers. Social transmission markedly reshaped community structure, generating distinct trajectories among phylotypes. OTU10 consistently dominated, reaching a median relative abundance of 77%, whereas OTU61 and OTU43146 were progressively outcompeted or lost. Comparative genomics of five representative species identified 69 carbohydrate-active enzyme families, with GH43 glycosyl hydrolases driving genomic divergence. Bifidobacterium polysaccharolyticum encoded an expanded CAZyme repertoire, supporting rapid growth on glucose and arabinan and indicating an r-selected strategy. In vitro and in vivo competition assays demonstrated that nutrient availability and priority effects act as key ecological filters. Pollen favored Bifidobacterium apousia , whereas sucrose-only diets promoted B. polysaccharolyticum . Moreover, early colonizers excluded later arrivals to some extent, highlighting priority effects. Together, these findings reveal how pollen polysaccharides and transmission bottlenecks interact to structure the strain-level landscape of the social microbiome.