Emerging infectious diseases (EIDs) pose a risk to human welfare, both directly1 and indirectly, by affecting managed livestock and wildlife that provide valuable resources and ecosystem services, such as the pollination of crops2. Honey bees (Apis mellifera), the prevailing managed insect crop pollinator, suffer from a range of emerging and exotic high impact pathogens3,4 and population maintenance requires active management by beekeepers to control them. Wild pollinators such as bumble bees (Bombus spp.) are in global decline5,6, one cause of which may be pathogen spillover from managed pollinators like honey bees7,8 or commercial colonies of bumble bees9. In our study, a combination of infection experiments with landscape scale field data indicates that honey bee EIDs are indeed widespread infectious agents within the pollinator assemblage. The prevalence of deformed wing virus (DWV) and the exotic Nosema ceranae is linked between honey bees and bumble bees, with honey bees having higher DWV prevalence, and sympatric bumble bees and honey bees sharing DWV strains; Apis is therefore the likely source of at least one major EID in wild pollinators. Lessons learned from vertebrates10,11 highlight the need for increased pathogen control in managed bee species to maintain wild pollinators, as declines in native pollinators may be caused by interspecies pathogen transmission originating from managed pollinators.

Lactic acid bacteria (LAB) are well recognized beneficial host-associated members of the microbiota of humans and animals. Yet LAB-associations of invertebrates have been poorly characterized and their functions remain obscure. Here we show that honeybees possess an abundant, diverse and ancient LAB microbiota in their honey crop with beneficial effects for bee health, defending them against microbial threats. Our studies of LAB in all extant honeybee species plus related apid bees reveal one of the largest collections of novel species from the genera Lactobacillus and Bifidobacterium ever discovered within a single insect and suggest a long (>80 mya) history of association. Bee associated microbiotas highlight Lactobacillus kunkeei as the dominant LAB member. Those showing potent antimicrobial properties are acquired by callow honey bee workers from nestmates and maintained within the crop in biofilms, though beekeeping management practices can negatively impact this microbiota. Prophylactic practices that enhance LAB, or supplementary feeding of LAB, may serve in integrated approaches to sustainable pollinator service provision. We anticipate this microbiota will become central to studies on honeybee health, including colony collapse disorder, and act as an exemplar case of insect-microbe symbiosis.