College of Food Science and Nutritional Engineering, China Agricultural University, Beijing, 100083, China.
Microbiome. 2021 Nov 17;9(1):225. doi: 10.1186/s40168-021-01174-y.
Honey bee gut microbiota transmitted via social interactions are beneficial to the host health. Although the microbial community is relatively stable, individual variations and high strain-level diversity have been detected across honey bees. Although the bee gut microbiota structure is influenced by environmental factors, the heritability of the gut members and the contribution of the host genetics remains elusive. Considering bees within a colony are not readily genetically identical due to the polyandry of the queen, we hypothesize that the microbiota structure can be shaped by host genetics.
We used shotgun metagenomics to simultaneously profile the microbiota and host genotypes of bees from hives of four different subspecies. Gut composition is more distant between genetically different bees at both phylotype- and "sequence-discrete population" levels. We then performed a successive passaging experiment within colonies of hybrid bees generated by artificial insemination, which revealed that the microbial composition dramatically shifts across batches of bees during the social transmission. Specifically, different strains from the phylotype of Snodgrassella alvi are preferentially selected by genetically varied hosts, and strains from different hosts show a remarkably biased distribution of single-nucleotide polymorphism in the Type IV pili loci. Genome-wide association analysis identified that the relative abundance of a cluster of Bifidobacterium strains is associated with the host glutamate receptor gene specifically expressed in the bee brain. Finally, mono-colonization of Bifidobacterium with a specific polysaccharide utilization locus impacts the alternative splicing of the gluR-B gene, which is associated with an increased GABA level in the brain.
Our results indicated that host genetics influence the bee gut composition and suggest a gut-brain connection implicated in the gut bacterial strain preference. Honey bees have been used extensively as a model organism for social behaviors, genetics, and the gut microbiome. Further identification of host genetic function as a shaping force of microbial structure will advance our understanding of the host-microbe interactions. Video abstract.
通过社交互动传递的蜜蜂肠道微生物群有益于宿主健康。尽管微生物群落相对稳定，但在蜜蜂中检测到个体变异和高菌株水平的多样性。尽管蜜蜂肠道微生物群结构受环境因素影响，但肠道成员的遗传性和宿主遗传的贡献仍然难以捉摸。考虑到由于蜂王的多配偶制，巢内的蜜蜂不易在遗传上完全相同，我们假设微生物群结构可以由宿主遗传决定。
我们使用 shotgun 宏基因组学同时分析了来自四个不同亚种蜂群的蜜蜂的微生物群和宿主基因型。在系统发育型和“序列离散种群”水平上，遗传上不同的蜜蜂之间的肠道组成更为遥远。然后，我们在通过人工授精产生的杂种蜜蜂的巢内进行了连续传代实验，结果表明，在社交传播过程中，蜜蜂的微生物组成在不同批次中发生了巨大变化。具体来说，来自 Snodgrassella alvi 系统发育型的不同菌株优先被遗传上不同的宿主选择，而来自不同宿主的菌株在 Type IV pili 基因座的单核苷酸多态性分布上表现出明显的偏倚。全基因组关联分析确定，一组双歧杆菌菌株的相对丰度与特定在蜜蜂大脑中表达的谷氨酸受体基因有关。最后，特定多糖利用基因座的双歧杆菌单定植会影响 gluR-B 基因的选择性剪接，这与大脑中 GABA 水平的增加有关。
我们的结果表明，宿主遗传影响蜜蜂肠道组成，并提出了肠道-大脑连接与肠道细菌菌株偏好有关的假说。蜜蜂已被广泛用作社交行为、遗传学和肠道微生物组的模型生物。进一步确定宿主遗传功能作为微生物结构塑造力量将有助于我们理解宿主-微生物相互作用。视频摘要。
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