Microbial Metamorphosis: Symbiotic bacteria and fungi proliferate during diapause and may enhance overwintering survival in a solitary bee

Host-microbe interactions underlie the development and fitness of many macroorganisms including bees. While many social bees benefit from vertically transmitted gut bacteria, solitary bees, which comprise the vast majority of species diversity within bees, lack a specialized gut microbiome. Here we examine the composition and abundance of bacteria and fungi throughout the complete life cycle of a ground-nesting solitary bee Anthophora bomboides standfordiana. In contrast to expectations, immature bee stages maintain a distinct core microbiome consisting of Actinobacteria and fungi in the genus Moniliella. Diapausing larval bees hosted the most abundant and distinctive bacteria and fungi, attaining 33 and 52 times their initial copy number, respectively. We tested two adaptive hypotheses regarding microbial functions for overwintering bees. First, using isolated bacteria and fungi, we found that Streptomyces from brood cells inhibited the growth of multiple pathogenic filamentous fungi, suggesting a role in pathogen protection during the long period of diapause. Second, sugar alcohol composition changed in tandem with major changes in microbial abundance suggesting links with bee metabolism or overwintering biology. Our results suggest that Anthophora bomboides hosts a conserved core microbiome that may provide key fitness advantages through larval development and overwintering, and raises the question of how this microbiome is transmitted between generations. The present work suggests that focus on adult gut microbiomes in solitary bees may overlook microbial symbionts within brood cells that could play diverse roles in bee fitness, and that exploration of microbes associated with immature bees may uncover novel microbial effects on insect hosts.