Early queen development in honey bees: Social context and queen breeder source affect gut microbiota and associated metabolism

Authors: Copeland, Duan; Anderson, Kirk; Mott, Brendon

Submitted to: Microbiology Spectrum
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/5/2022
Publication Date: 7/18/2022
Citation: Copeland, D.C., Anderson, K.E., Mott, B.M. 2022. Early queen development in honey bees: Social context and queen breeder source affect gut microbiota and associated metabolism. Microbiology Spectrum. 10(4). https://doi.org/10.1128/spectrum.00383-22.
DOI: https://doi.org/10.1128/spectrum.00383-22

Interpretive Summary: Honey bee queen failures rank consistently among the top reasons for colony failure, with decreased egg production of aging queens as a primary cause. Here we investigate the change in gut microbes and immunity in young queens during colony introduction. Recently mated queens were placed into environments with very different metabolic demand; active colonies requiring massive egg production, or queen storage systems used for the maintenance of multiple non-laying queens. After three weeks we sequenced the microbiota and immune and oxidative stress genes across four alimentary tract niches of the early queen gut. Microbiota and gene expression in the queen gut differed by both time and early environment.Perhaps related to lower metabolic output, queen bank queens resembled older queens with less Alpha 2.1 and greater abundance of Bifidobacterium in the rectum, and large blooms of S. alvi in the ileum. Differences in the expression of oxidative stress genes in the midgut and rectum were associated with the colony environment. In the ileum, upregulation of most immune and oxidative stress genes occurred regardless of colony environment, suggesting a post-mating developmental process associated with microbial succession. The metabolic demand associated with egg production may be directly linked to the dominance of Alpha 2.1 in the hindgut. Results are important for beekeepers and queen breeders seeking to standardize queen production, introduction, and replacement.

Technical Abstract: The highly social honey bee has dense populations but a significantly reduced repertoire of immune genes relative to solitary species, suggesting a greater reliance on social immunity. Here we investigate immune gene expression and gut microbial succession in queens during colony introduction. Recently mated queens were placed into an active colony or a storage hive for multiple queens: a queen-bank. Feeding intensity, social context, and metabolic demand differ greatly between the two environments. After 3 weeks, we examined gene expression associated with oxidative stress and immunity and performed high-throughput sequencing of the queen gut microbiome across four alimentary tract niches. Microbiota and gene expression in the queen hindgut differed by time, queen breeder source, and metabolic environment. In the ileum, upregulation of most immune and oxidative stress genes occurred regardless of treatment conditions, suggesting postmating effects on gut gene expression. Counterintuitively, queens exposed to the more social colony environment contained significantly less bacterial diversity indicative of social immune factors shaping the queens microbiome. Queen bank queens resembled much older queens with decreased Alpha 2.1, greater abundance of Lactobacillus firm5 and Bifidobacterium in the hindgut, and significantly larger ileum microbiotas, dominated by blooms of Snodgrassella alvi. Combined with earlier findings, we conclude that the queen gut microbiota experiences an extended period of microbial succession associated with queen breeder source, postmating development, and colony assimilation.