Microbiome Structure Influences Infection by the Parasite Crithidia bombi in Bumble Bees

Recent declines in bumble bee populations are of great concern and have prompted critical evaluations of the role of pathogen introductions and host resistance in bee health. One factor that may influence host resilience when facing infection is the gut microbiota. Previous experiments withBombus terrestris , a European bumble bee, showed that the gut microbiota can protect againstCrithidia bombi , a widespread trypanosomatid parasite of bumble bees. However, the particular characteristics of the microbiome responsible for this protective effect have thus far eluded identification. Using wild and commercially sourcedBombus impatiens , an important North American pollinator, we conducted cross-wise microbiota transplants to naive hosts of both backgrounds and challenged them with aCrithidia parasite. As withB. terrestris , we find that microbiota-dependent protection againstCrithidia operates inB. impatiens . LowerCrithidia infection loads were experimentally associated with high microbiome diversity, large gut bacterial populations, and the presence ofApibacter ,Lactobacillus Firm-5, andGilliamella spp. in the gut community. These results indicate that even subtle differences between gut community structures can have a significant impact on a microbiome's ability to defend against parasite infections.IMPORTANCE Many wild bumble bee populations are under threat due to human activity, including through the introduction of pathogens via commercially raised bees. Recently, it was found that the bumble bee gut microbiota can help defend against a common parasite,Crithidia bombi , but the particular factors contributing to this protection are unknown. Using both wild and commercially raised bees, we conducted microbiota transplants to show that microbiome diversity, total gut bacterial load, and the presence of certain core members of the microbiota may all impact bee susceptibility toCrithidia infection. Bee origin (genetic background) was also a factor. Finally, by examining this phenomenon in a previously uninvestigated bee species, our study demonstrates that microbiome-mediated resistance toCrithidia is conserved across multiple bumble bee species. These findings highlight how intricate interactions between hosts, microbiomes, and parasites can have wide-ranging consequences for the health of ecologically important species.