Social Interaction is Unnecessary for Hindgut Microbiome Transmission in Honey Bees: The Effect of Diet and Social Exposure on Tissue-Specific Microbiome Assembly

Authors: Anderson, Kirk; Ricigliano, Vincent; COPELAND, D. - University Of Arizona; Mott, Brendon; MAES, P. - University Of Arizona

Submitted to: Microbial Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/25/2022
Publication Date: 5/2/2022
Citation: Anderson, K.E., Ricigliano, V.A., Copeland, D., Mott, B.M., Maes, P. 2022. Social Interaction is Unnecessary for Hindgut Microbiome Transmission in Honey Bees: The Effect of Diet and Social Exposure on Tissue-Specific Microbiome Assembly. Microbial Ecology. https://doi.org/10.1007/s00248-022-02025-5.
DOI: https://doi.org/10.1007/s00248-022-02025-5

Interpretive Summary: The adult honey bee is a model for host-microbial interactions with experimental designs evolving towards a reliance on worker bees exposed to artificially constructed and experimentally introduced groups of gut bacteria with known genome information. But research on gut microbiome assembly lacks tissue specificity and adequate control for the social and hive environment. Here we investigated the effects of diet and social isolation on tissue-specific bacterial and fungal colonization of two hindgut regions (ileum and rectum). We found that both treatment factors significantly influenced early hindgut colonization explaining different proportions of community variation. Exposure to fresh hive materials in social isolation resulted in gut bacterial communities that were significantly larger, but taxonomically and structurally similar to those of the natural colony environment. Diets of no pollen or altered pollen in social isolation resulted in more atypical bacterial communities with altered community structure and tissue-specific reductions of functionally important core bacteria. Compared to natural colony conditions, social isolation markedly reduced fungal abundance in the gut, suggesting that exposure to the active hive environment plays a critical role in early gut colonization. The dynamics of gut microbiome assembly are multi-modal, involving exposure, early succession, diet, strain compatibility, social interaction, and host control. Our findings contribute novel insights into factors influencing the assembly and maintenance of honey bee gut microbiota and facilitate future experimental designs.

Technical Abstract: Honey bees are a model for host–microbial interactions with experimental designs evolving towards conventionalized worker bees. Research on gut microbiome transmission and assembly has examined only a fraction of factors associated with the colony and hive environment. Here, we studied the efects of diet and social isolation on tissue-specifc bacterial and fungal colonization of the midgut and two key hindgut regions. We found that both treatment factors signifcantly infuenced early hindgut colonization explaining similar proportions of microbiome variation. In agreement with previous work, social interaction with older workers was unnecessary for core hindgut bacterial transmission. Exposure to natural eclosion and fresh stored pollen resulted in gut bacterial communities that were taxonomically and structurally equivalent to those produced in the natural colony setting. Stressed diets of no pollen or autoclaved pollen in social isolation resulted in decreased fungal abundance and bacterial diversity, and atypical microbiome structure and tissue-specifc variation of functionally important core bacteria. Without exposure to the active hive environment, the abundance and strain diversity of keystone ileum species Gilliamella apicola was markedly reduced. These changes were associated with signifcantly larger ileum microbiotas suggesting that extended exposure to the active hive environment plays an antibiotic role in hindgut icrobiome establishment. We conclude that core hindgut microbiome transmission is facultative horizontal with 5 of 6 core hindgut species readily acquired from the built hive structure and natural diet. Our fndings contribute novel insights into factors infuencing assembly and maintenance of honey bee gut microbiota and facilitate future experimental designs.