The dual facets of a honey bee gut symbiont Frischella perrara

Honey bees are the most important pollinators worldwide. Recently, they have been developed as models for gut microbiota studies. Frischella perrara, a symbiont colonizing the bee pylorus, causes formation of a scab-like region with disrupted cellular organization. Using gnotobiotic bees, we found that the colonization by F. perrara reduced bee lifespan but increased the survivorship of bees following challenge with an opportunistic pathogen, Serratia marcescens. F. perrara produces a genotoxin, colibactin. Interestingly, a gene knockout mutant that cannot produce colibactin did not show protective effect, indicating that colibactin production contributes to the protection. Snodgrassella alvi, a key microbiota species, possesses the clbS gene that encodes an immune protein for colibactin. The knockout of clbS in S. alvi abated its colonization when F. perrara was present. The influence of F. perrara colonization on core members of the gut community was further assessed using a defined community. We found that the abundance of F. perrara was negatively correlated with that of Gilliamella spp. This negative correlation was also observed in natural bees, consistent with interspecies competition in the bee gut. Intriguingly, we found that clbS is widely distributed among core taxa of the bee gut community but not among the non-core taxa or bee pathogens. This suggests that F. perrara and colibactin generate selective pressure on core gut community members and present a barrier to pathogens. Overall, F. perrara has effects that are both positive and negative for the bees.