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Title: Microbial diversity associated with the pollen stores of captive-bred bumble bee colonies

Author
item DHARAMPAL, PRARCHANA - University Of Wisconsin
item DIAZ-GARCIA, LUIS - University Of Wisconsin
item HAASE, MAX A.B. - University Of Wisconsin
item Zalapa, Juan
item CURRIE, CAMERON - University Of Wisconsin
item HITTINGER, CHRIS - University Of Wisconsin
item Steffan, Shawn

Submitted to: Insects
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/10/2020
Publication Date: 4/16/2020
Citation: Dharampal, P., Diaz-Garcia, L., Haase, M., Zalapa, J.E., Currie, C., Hittinger, C., Steffan, S.A. 2020. Microbial diversity associated with the pollen stores of captive-bred bumble bee colonies. Insects. 11(4):250. https://doi.org/10.3390/insects11040250.
DOI: https://doi.org/10.3390/insects11040250

Interpretive Summary: Pollen-provisions offer a unique, rich resource, supporting a diverse, yet distinctive array of well-adapted microbiota, which provide their bee hosts with a variety of benefits including fermentation of raw pollen, preservation of pollen-provisions, production of nutritional supplements, and inhibition of pathogens. Perturbations in the diversity and/or abundance of the microbial community can alter the dynamics of this bee-microbe symbiosis with unpredictable impacts on bee health. Larval bees, in particular, may rely heavily on the core hive microbiota such as Lactobacillus and Candida, that are fundamental to pollen-fermentation. Aside from these two taxa, the microbiome of pollen-provisions may be quite distinctive. The divergence in community structure may be linked to variability in microbes obtained from the pollination environment, or the differences in socially transmitted microbes derived from the bee digestive tract. The various stages of pollen digestion are mediated by an ecological succession of microbes with disparate metabolic capacities, which may be another contributing factor to the temporal shifts in the microbiome. This study establishes a baseline of microbial diversity for bumble bee (Bombus impatiens) pollen-provisions, permitting future work to examine the impacts of stressors on the microbiome of these provisions. Impact: These findings suggest that the emergent effect of these taxonomically different, yet functionally comparable communities, satisfy the metabolic demands of their host, likely due to a degree of functional redundancy among generalist taxa.

Technical Abstract: Bees harbor a diversity of nutrient-provisioning symbiotic microbes within their hive environment. These microbes facilitate the fermentation of raw pollen to more nutritious pollen-provisions for larval consumption. Although they perform several vital ecosystem services to ensure host fitness, little is known about the taxonomic diversity of microbes within pollen-provisions. Using 16S rRNA and ITS-based gene analysis, this study offers the first insight into the fungal and bacterial communities within the pollen-provisions of bumble bees. In two separate trials (Trials A and B) conducted using replicate hives from different suppliers, the microbiome of pollen-provisions showed comparable representation across the phyla Firmicutes, Proteobacteria, Bacteroidetes, Actinobacteria, and Ascomycota. However, in-depth analysis revealed significant differences in phylogenetic composition between the two trials. Overall, the microbial communities of Trial A were more replete with fungal taxa than those of Trial B, while Trial B exhibited more bacterial diversity. The fungal community of Trial A had diverse representatives from Saccharomycetes, Eurotiomycetes, and Dothideomycetes, whereas Trial B was comprised almost entirely of true yeasts. The bacterial community of Trial A was dominated by Lactobacillaceae, and Trial B harbored families within the Proteobacteria and Bacteroidetes. Only Lactobacillus and Candida appeared as a shared core microbiota among all hives, but such microbes are ubiquitous in the environment, and thus the observed variability was likely due to idiosyncrasies in environmentally and socially acquired microbes. Importantly, all colonies were active and productive in terms of colony growth, suggesting that the beneficial function of the pollen microbiome derives from functionally similar, mutualistic microbial communities. Collectively, these results reveal not only that pollen-provisions support diverse, specialized microbial communities, but also that such pollen-borne communities can be taxonomically quite different, even while they are functionally similar. Given the importance of bee-microbe symbioses, the characterization of their microbial communities may be critical for bee conservation efforts.