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. Article 00383-22. 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: 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 gut microbial succession and immune gene expression 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 a queen storage system for the maintenance of multiple non-laying queens. After three weeks we deep sequenced 16S rRNA genes and used qPCR to analyze 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. Result are important for beekeepers and queen breeders seeking to standardize queen production, introduction and replacement.