Strain diversity and host specificity of the gut symbiont Gilliamella in Apis mellifera, Apis cerana and Bombus terrestris.

Social bees, with their specialized gut microbiota and societal transmission between individuals, provide an ideal model for studying host-gut microbiota interactions. While the functional disparities arising from strain-level diversity of gut symbionts and their effects on host health have been studied in Apis mellifera and bumblebees, studies focusing on host-specific investigations of individual strains across different honeybee hosts remain relatively unexplored. In this study, the complete genomic sequences of 17 strains of Gilliamella from A. mellifera, Apis cerana and Bombus terrestris were analyzed. The analysis revealed that the strains of A. mellifera display a more expansive genomic and functional content compared to the strains of A. cerana and B. terrestris. Phylogenetic analysis showed a deep divergence among the Gilliamella strains from different hosts. Additionally, biochemistry tests and antibiotic susceptibility tests revealed that gut strains from A. mellifera exhibited a more extensive pathway for carbohydrate metabolism and a greater resistance to antibiotics than gut strains from A. cerana and B. terrestris. Strains from A. mellifera and A. cerana showed higher colonization efficiency and competitive ability whithin their respective host species, indicating a higher degree of host-specific adaptation of local gut microbiota. In addition, colonization by A. mellifera-derived strain triggers a stronger transcriptional response in the host than A. cerana-derived strain. The variation in the number of differentially expressed genes and the involvement of distinct signaling pathways across these two host species suggest species-specific adaptations to Gilliamella strains. These findings suggest that despite occupying similar niches in the bee gut, strain-level variations can influence microbial functions, and their impact on host physiological functions may vary across different strains.