College of Food Science and Nutritional Engineering, China Agricultural University, Beijing, 100083, China.
Shandong Institute of Plant Protection, Shandong Academy of Agricultural Sciences, Jinan, 250100, China.
Microbiome. 2021 Nov 4;9(1):216. doi: 10.1186/s40168-021-01163-1.
Microbial acquisition and development of the gut microbiota impact the establishment of a healthy host-microbes symbiosis. Compared with other animals, the eusocial bumblebees and honeybees possess a simple, recurring, and similar set of gut microbiota. However, all bee gut phylotypes have high strain-level diversity. Gut communities of different bee species are composed of host-specific groups of strains. The variable genomic regions among strains of the same species often confer critical functional differences, such as carbon source utilization, essential for the natural selection of specific strains. The annual bumblebee colony founded by solitary queens enables tracking the transmission routes of gut bacteria during development stages.
Here, we first showed the changes in the microbiome of individual bumblebees across their holometabolous life cycle. Some core gut bacteria persist throughout different stages of development. Gut microbiota of newly emerged workers always resembles those of their queens, suggesting a vertical transmission of strains from queens to the newborn workers. We then follow the dynamic changes in the gut community by comparing strain-level metagenomic profiles of queen-worker pairs longitudinally collected across different stages of the nest development. Species composition of both queen and worker shifts with the colony's growth, and the queen-to-worker vertical inheritance of specific strains was identified. Finally, comparative metagenome analysis showed clear host-specificity for microbes across different bee hosts. Species from honeybees often possess a higher level of strain variation, and they also exhibited more complex gene repertoires linked to polysaccharide digestion. Our results demonstrate bacterial transmission events in bumblebee, highlighting the role of social interactions in driving the microbiota composition.
By the community-wide metagenomic analysis based on the custom genomic database of bee gut bacteria, we reveal strain transmission events at high resolution and the dynamic changes in community structure along with the colony development. The social annual life cycle of bumblebees is key for the acquisition and development of the gut microbiota. Further studies using the bumblebee model will advance our understanding of the microbiome transmission and the underlying mechanisms, such as strain competition and niche selection. Video Abstract.
微生物的获取和肠道微生物群的发展影响健康宿主-微生物共生体的建立。与其他动物相比，真社会性熊蜂和蜜蜂具有简单、重复且相似的肠道微生物群。然而，所有蜜蜂肠道菌群都具有高度的菌株多样性。不同蜜蜂物种的肠道群落由宿主特异性的菌株群组成。同一物种菌株之间的可变基因组区域通常赋予关键的功能差异，例如碳源利用，这对于特定菌株的自然选择至关重要。由独居蜂王建立的年度熊蜂群体使我们能够在发育阶段追踪肠道细菌的传播途径。
在这里，我们首先展示了个体熊蜂在其全变态生命周期中微生物组的变化。一些核心肠道细菌在不同的发育阶段都能持续存在。新出现的工蜂的肠道微生物群总是与它们的蜂王相似，这表明菌株从蜂王垂直传递给新生的工蜂。然后，我们通过比较不同巢发育阶段纵向收集的蜂王-工蜂对的菌株水平宏基因组谱，跟踪肠道群落的动态变化。蜂王和工蜂的物种组成随着群体的增长而变化，并确定了特定菌株从蜂王到工蜂的垂直遗传。最后，比较宏基因组分析显示了不同蜜蜂宿主之间微生物的明显宿主特异性。来自蜜蜂的物种通常具有更高水平的菌株变异，并且它们还表现出与多糖消化相关的更复杂的基因库。我们的结果表明，在熊蜂中存在细菌传播事件，突出了社会相互作用在驱动微生物群落组成中的作用。
通过基于蜜蜂肠道细菌定制基因组数据库的全群落宏基因组分析，我们以高分辨率揭示了菌株传递事件以及随着群体发育的群落结构动态变化。熊蜂的社会性年度生命周期是获取和发展肠道微生物群的关键。使用熊蜂模型的进一步研究将推进我们对微生物组传播和潜在机制的理解，例如菌株竞争和生态位选择。
