Honey bee nutritranscriptomics reveals key insights towards precision nutrition.

INTRODUCTION: Honey bees are essential managed pollinators faced by nutritional deficiencies which contributes to worldwide colony losses. The integration of nutrition science with genomics offers a powerful approach to optimize honey bee health by augmenting immune function and resilience to stressors through precision diet interventions. OBJECTIVES: To uncover the impact of honey bee genetics on core physiological responses to natural and artificial diets. METHODS: Two honey bee genetic backgrounds (Russian and Pol-line) were fed diets consisting of sugar, pollen, and microalgae biomass from either Chlorella vulgaris or spirulina. Nutrigenetic variation was assessed by body weight measurements followed by transcriptome sequencing. Standard differential gene expression analysis and supervised machine learning algorithms were used to measure genotype-specific transcriptional responses to the diets. RESULTS: Known (i.e., vitellogenin and Jhe, hex70a) and novel (i.e., Glob1, slif and sad) biomarkers of nutritional health exhibited a significant genetics-by-diet interaction. Furthermore, Russian bees featured a contracted transcriptional response, and a transcriptomic signature of delayed behavioral maturation as compared to Pol-line bees, suggesting alternative nutrient assimilation strategies between the two genetic backgrounds. Regardless of diet, Russian bees had significantly lower abundance of a major viral pathogen (DWV). Lastly, higher expression of humoral and cellular immune genes was detected in microalgae-fed bees, though spirulina was significantly more immunogenic than Chlorella. CONCLUSION: Genetic background plays a key role in shaping honey bee responses to nutrition. By identifying novel biomarkers of nutritional status, our results support the unique benefits of two microalgae species as functional feed additives. Furthermore, these results reveal the importance of genetics as a consideration when optimizing supplemental feed for an agricultural pollinator. These findings contribute towards the development of tailored nutrition strategies and artificial diets to improve honey bee health.