Changes in gut microbiota and metabolism associated with phenotypic plasticity in the honey bee Apis mellifera

Authors: Copeland, Duan; MAES, P. - University Of Arizona; Mott, Brendon; Anderson, Kirk

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/17/2022
Publication Date: 12/9/2022
Citation: Copeland, D.C., Maes, P., Mott, B.M., Anderson, K.E. 2022. Changes in gut microbiota and metabolism associated with phenotypic plasticity in the honey bee Apis mellifera. Frontiers in Microbiology. 13. Article 1059001. https://doi.org/10.3389/fmicb.2022.1059001.
DOI: https://doi.org/10.3389/fmicb.2022.1059001

Interpretive Summary: Honey bees exhibit an elaborate social structure that corresponds with worker aging and division of labor. Young workers perform tasks inside the hive, while older workers forage outside the hive. Critical to colony survival and reproduction, the work force can respond rapidly to changes in the environment or colony age structure and assume emergency tasks, resulting in young foragers or old nurses. We hypothesized that social structure affects the microbiome, more specifically, that behavioral task independent of age would generate differences in gut microbiota and host physiology. We used high throughput sequencing to track gut microbial succession, and measured gene expression and oxidative protein damage associated with behavioral task and age. We found that both age and behavioral task could explain differences in midgut and ileum microbiota, but host gene expression was best explained by an interaction of task and age. An extended nursing role in early life stabilized the ratio abundance of keystone bacteria in the gut, while precocious foraging resulted in poor bacterial establishment, nutrient deficient gene expression, and increased oxidative damage. Our results suggest that the physiological cost of early foraging is extreme, and highlight the progression of colony dwindling, a common but misunderstood process.

Technical Abstract: Honey bees exhibit an elaborate social structure based in part on an agerelated division of labor. Young workers perform tasks inside the hive, while older workers forage outside the hive, tasks associated with distinct diets and metabolism. Critical to colony fitness, the work force can respond rapidly to changes in the environment or colony demography and assume emergency tasks, resulting in young foragers or old nurses. We hypothesized that both task and age affect the gut microbiota consistent with changes to host diet and physiology. We performed two experiments inducing precocious foragers and reverted nurses, then quantified tissue-specific gut microbiota and host metabolic state associated with nutrition, immunity and oxidative stress. In the precocious forager experiment, both age and ontogeny explained differences in midgut and ileum microbiota, but host gene expression was best explained by an interaction of these factors. Precocious foragers were nutritionally deficient, and incurred higher levels of oxidative damage relative to agematched nurses. In the oldest workers, reverted nurses, the oxidative damage associated with age and past foraging was compensated by high Vitellogenin expression, which exceeded that of young nurses. Host-microbial interactions were evident throughout the dataset, highlighted by an age-based increase of Gilliamella abundance and diversity concurrent with increased carbonyl accumulation and CuZnSOD expression. The results in general contribute to an understanding of ecological succession of the worker gut microbiota, defining the species-level transition from nurse to forager.