Exploring the interactions between Nosema ceranae infection and the honey bee gut microbiome

Managed colonies of the European honey bee, Apis mellifera, have faced considerable losses in recent years. A widespread contributing factor is a microsporidian pathogen, Nosema ceranae, which occurs worldwide, is increasingly resistant to antibiotic treatment, and can alter the host's immune response and nutritional uptake. These obligate gut pathogens share their environment with a natural honey bee microbiome whose composition can affect pathogen resistance. We tested the effect of N. ceranae infection on this microbiome by feeding 5 day-old adult bees that had natural, fully developed microbiomes with live N. ceranae spores (40,000 per bee) or a sham inoculation, sterile 2.0 M sucrose solution. We caged and reared these bees in a controlled lab environment and tracked their mortality over 12 d, after which we dissected them, measured their infection levels (gut spore counts), and analyzed their microbiomes. Bees fed live spores had two-fold higher mortality by 12 d and 36.5-fold more spores per bee than controls. There were also strong colony effects on infection levels, and 9% of spore-inoculated bees had no spore counts at all (defined as fed-spores-but-not-infected). Nosema ceranae infection had significant but subtle effects on the gut microbiomes of experimentally infected bees, bees with different infection levels, and fed-spores-but-not-infected vs. bees with gut spores. Specific bacteria, including Gilliamella ASVs, were positively associated with infection, indicating that multiple strains of core gut microbes either facilitate or resist N. ceranae infection. Future studies on the interactions between bacterial, pathogen, and host genotypes would be illuminating.