The Comparison of Antioxidant Performance, Immune Performance, IIS Activity and Gut Microbiota Composition between Queen and Worker Bees Revealed the Mechanism of Different Lifespan of Female Casts in the Honeybee

SIMPLE SUMMARY: Queen bees and worker bees are natural animal models for studying aging because queen bees live about 20 times longer than worker bees, despite both developing from fertilized eggs. Nutrition (intake of royal jelly or not) is a well-known external factor that causes the different lifespan between queens and workers. Exploring the nutrient-mediated molecular mechanism is of great significance to study the universal regularity of aging in animals. In this study, we systematically compared the differences of antioxidant, immune, IIS and gut microbiota composition between queens and workers. Of these, antioxidant, immune and IIS are the conserved mechanisms of aging. The gut microbiota are upstarts in regulating host health. We found that queens had stronger antioxidant capacity and lower immune pathway and IIS activity than workers. Queens also had supernal beneficial bacterium over workers. This study suggested that antioxidant, immune, IIS, and gut symbiotic bacteria all may contribute to the longevity of queens. This study provides more insights into revealing the mechanisms of queens’ longevity. ABSTRACT: Queen bees and worker bees both develop from fertilized eggs, whereas queens live longer than workers. The mechanism of this phenomenon is worth exploring. Antioxidant capacity, immune and IIS are the conserved mechanisms of aging. The importance of gut bacteria for health prompted us to connect with bee aging. Therefore, the differences of antioxidant, immune, IIS and gut microflora between queen and worker bees were compared to find potential mechanisms of queens’ longevity. The results showed queens had stronger antioxidant capacity and lower immune pathway and IIS activity than workers. The higher expression level of catalase and SOD1/2 in queens resulted in the stronger ROS scavenging ability, which leads to the lower ROS level and the reduced accumulation of oxidative damage products in queens. The lower IMD expression and higher antimicrobial peptides (AMPs) expressions in queens suggested that queens maintain lower immune pathway activity and stronger immune capacity than workers. Gut bacteria composition analysis indicated that queens had supernal Acetobacteraceae (notably Commensalibacter and Bombella), Lactobacillus and Bifidobacterium over workers. In conclusion, antioxidant, immune, IIS, and gut symbiotic bacteria all contribute to the longevity of queens. This study provides more insights into revealing the mechanisms of queens’ longevity.