Honey bee core hindgut microbiome transmission does not require social interaction: The effect of diet and social exposure on tissue-specific microbiome assembly

Honey bees are a model for host-microbial interactions with experimental designs evolving towards conventionalized worker bees. Research on gut microbiome transmission and assembly has examined only a fraction of factors associated with the colony and hive environment. Here we studied the effects of diet and social isolation on tissue-specific bacterial and fungal colonization of the midgut and two key hindgut regions. We found that both treatment factors significantly influenced early hindgut colonization explaining similar proportions of microbiome variation. In agreement with previous work, social interaction with older workers was unnecessary for core hindgut bacterial transmission. Exposure to natural eclosion and fresh stored pollen resulted in gut bacterial communities that were taxonomically and structurally equivalent to those produced in the natural colony setting. Stressed diets of no pollen or altered pollen in social isolation resulted in atypical microbiome structure and tissue-specific variation of functionally important core bacteria. However, no exposure to the active hive environment markedly reduced the abundance of both fungi and keystone species Gilliamella apicola in the ileum. These changes were associated with significantly larger ileum microbiotas suggesting that extended exposure to the active hive environment plays an antibiotic role in hindgut microbiome establishment. We conclude that core hindgut microbiome transmission is facultative horizontal with 5 of 6 core hindgut species readily acquired from the built hive structure and natural diet. Our findings contribute novel insights into factors influencing assembly and maintenance of honey bee gut microbiota and facilitate future experimental designs.

蜜蜂被视为宿主-微生物相互作用的研究模型，其实验设计逐步趋向于标准化的工蜂。关于肠道微生物群传播和组装的研究，仅考察了与群体和蜂箱环境相关的部分因素。本研究探讨了饮食和社交隔离对中肠及两个关键后肠区域组织特异性细菌和真菌定植的影响。我们发现，两种处理因素均显著影响了早期后肠定植，解释了微生物群变异的相似比例。与先前研究一致，与老年工蜂的社交互动对于核心后肠细菌的传播并非必需。接触自然羽化和新鲜储存的花粉导致的中肠细菌群落，在分类学和结构上与自然蜂群环境产生的群落相当。在社会隔离状态下，无花粉或花粉改变的应激饮食导致微生物群结构异常和组织特异性功能重要核心细菌的变化。然而，未接触活跃蜂箱环境显著降低了回肠中真菌和关键物种Gilliamella apicola的丰度。这些变化与显著更大的回肠微生物群相关联，表明长期接触活跃蜂箱环境在 hindgut 微生物群建立中发挥着抗生素的作用。我们得出结论，核心后肠微生物群的传播是选择性的水平传播，其中6个核心后肠物种中的5个可以轻易地从蜂箱结构和自然饮食中获得。我们的发现为影响蜜蜂肠道微生物群组装和维护的因素提供了新的见解，并促进了未来实验设计的发展。