Division of labor in honey bee gut microbiota for plant polysaccharide digestion
Division of labor in honey bee gut microbiota for plant polysaccharide digestion
复制标题
蜜蜂肠道微生物群消化植物多糖的分工
DOI：
10.1073/pnas.1916224116
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发表时间：
2019-12-17
影响因子：
11.1
通讯作者：
Moran, Nancy A.
中科院分区：
文献类型：
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作者：
Zheng, Hao;Perreau, Julie;Moran, Nancy A.
意义 蜜蜂和其他群居蜜蜂拥有专门的肠道微生物群，主要由 5 个共同进化的细菌簇组成。蜜蜂吃花粉，花粉中含有多种多糖，这些多糖是可能被肠道细菌消化的富含能量的底物。在培养细菌的基因组序列和宏基因组数据中鉴定出多糖降解基因，揭示双歧杆菌和吉利亚梅拉消化蜜蜂肠道中的多糖。在这两种情况下，个体菌株的这些能力各不相同。多糖降解基因聚集在双歧杆菌基因组内，并响应特定底物而表达。其他蜂肠道细菌物种不能降解多糖，并且某些物种依赖其他物种的氨基酸。这项工作提供了关于细菌物种如何分化到宿主肠道内不同生态位的见解。蜜蜂从花蜜和脂质中获取碳水化合物；花粉中还含有氨基酸，花粉还含有多糖，包括纤维素、半纤维素和果胶。这些潜在的能源可以通过微生物酶活性降解和发酵，从而产生可供宿主利用的短链脂肪酸。然而，单个微生物群成员对多糖消化的贡献仍不清楚。通过对细菌分离株基因组和蜜蜂肠道微生物群宏基因组的分析，我们确定双歧杆菌和吉利亚梅拉菌是半纤维素和果胶的主要降解者。双歧杆菌和吉利亚梅拉在与多糖消化相关的基因库中表现出广泛的菌株水平多样性。蜜蜂的品系比熊蜂的品系拥有更多的此类基因。在双歧杆菌中，编码碳水化合物活性酶的基因位于专门用于多糖利用的基因座内，就像来自人类肠道的拟杆菌一样。在体外和体内，碳水化合物活性酶编码基因的表达都会因特定的半纤维素而上调。代谢组学分析证明，在实验中被不同品系殖民的蜜蜂会产生独特的肠道代谢组谱，其中特定单糖富集，这与基因组数据的预测相对应。其他 3 个核心肠道物种簇（斯诺德格拉斯菌属和 2 个乳酸菌簇）几乎没有或没有多糖消化基因。总之，这些发现表明个体宿主内的菌株组成决定了代谢能力并可能影响宿主的营养。此外，我们的研究揭示的生态位专业化可能会促进蜜蜂肠道微生物组的整体群落稳定性。
Significance Honey bees and other social bees harbor specialized gut microbiota dominated by 5 coevolved bacterial clusters. Bees eat pollen, which contains diverse polysaccharides, energy-rich substrates potentially digested by gut bacteria. Polysaccharide degradation genes were identified in genome sequences of cultured bacteria and in metagenomic data, revealing that Bifidobacterium and Gilliamella digest polysaccharides in the honey bee gut. In both, individual strains vary in these abilities. Polysaccharide-degrading genes are clustered within Bifidobacterium genomes and are expressed in response to specific substrates. Other bee gut bacterial species cannot degrade polysaccharides, and some species rely on others for amino acids. This work provides insight into how bacterial species diverge into different ecological niches within the gut of their hosts. Bees acquire carbohydrates from nectar and lipids; and amino acids from pollen, which also contains polysaccharides including cellulose, hemicellulose, and pectin. These potential energy sources could be degraded and fermented through microbial enzymatic activity, resulting in short chain fatty acids available to hosts. However, the contributions of individual microbiota members to polysaccharide digestion have remained unclear. Through analysis of bacterial isolate genomes and a metagenome of the honey bee gut microbiota, we identify that Bifidobacterium and Gilliamella are the principal degraders of hemicellulose and pectin. Both Bifidobacterium and Gilliamella show extensive strain-level diversity in gene repertoires linked to polysaccharide digestion. Strains from honey bees possess more such genes than strains from bumble bees. In Bifidobacterium, genes encoding carbohydrate-active enzymes are colocated within loci devoted to polysaccharide utilization, as in Bacteroides from the human gut. Carbohydrate-active enzyme-encoding gene expressions are up-regulated in response to particular hemicelluloses both in vitro and in vivo. Metabolomic analyses document that bees experimentally colonized by different strains generate distinctive gut metabolomic profiles, with enrichment for specific monosaccharides, corresponding to predictions from genomic data. The other 3 core gut species clusters (Snodgrassella and 2 Lactobacillus clusters) possess few or no genes for polysaccharide digestion. Together, these findings indicate that strain composition within individual hosts determines the metabolic capabilities and potentially affects host nutrition. Furthermore, the niche specialization revealed by our study may promote overall community stability in the gut microbiomes of bees.