Ricigliano Vincent A, Anderson Kirk E
USDA-ARS, Honey Bee Breeding, Genetics, and Physiology Laboratory, Baton Rouge, LA 70820, USA.
USDA-ARS, Carl Hayden Bee Research Center, Tucson, AZ 85719, USA.
Insects. 2020 May 9;11(5):291. doi: 10.3390/insects11050291.
Microbial metabolites are considered important drivers of diet-based microbiota influence on the host, however, mechanistic models are confounded by interactions between diet, microbiota function, and host physiology. The honey bee harbors a simple microbiota that produces organic acids as fermentation products of dietary nectar and pollen, making it a model for gut microbiota research. Herein, we demonstrate that bacterial abundance in the honey bee gut is partially associated with the anterior rectum epithelium. We used dietary pollen restriction and organic acid feeding treatments to obtain information about the role of undigested pollen as a microbiota growth substrate and the impact of bacterial fermentation products on honey bee enteroendocrine signaling. Pollen restriction markedly reduced total and specific bacterial 16S rRNA abundance in the anterior rectum but not in the ileum. Anterior rectum expression levels of bacterial fermentative enzyme gene transcripts (acetate kinase, lactate dehydrogenase, and hydroxybutyryl-CoA dehydrogenase) were reduced in association with diet-induced microbiota shifts. To evaluate the effects of fermentative metabolites on host enteroendocrine function, pollen-restricted bees were fed an equimolar mixture of organic acid sodium salts (acetate, lactate, butyrate, formate, and succinate). Organic acid feeding significantly impacted hindgut enteroendocrine signaling gene expression, rescuing some effects of pollen restriction. This was specifically manifested by tissue-dependent expression patterns of neuropeptide F and allatostatin pathways, which are implicated in energy metabolism and feeding behaviors. Our findings provide new insights into the diet-microbiota-host axis in honey bees and may inform future efforts to improve bee health through diet-based microbiota manipulations.
微生物代谢产物被认为是基于饮食的微生物群影响宿主的重要驱动因素，然而，机制模型因饮食、微生物群功能和宿主生理学之间的相互作用而变得复杂。蜜蜂拥有一个简单的微生物群，该微生物群可产生有机酸作为饮食中花蜜和花粉的发酵产物，这使其成为肠道微生物群研究的一个模型。在此，我们证明蜜蜂肠道中的细菌丰度部分与直肠前部上皮相关。我们使用饮食花粉限制和有机酸喂养处理来获取有关未消化花粉作为微生物群生长底物的作用以及细菌发酵产物对蜜蜂肠内分泌信号传导影响的信息。花粉限制显著降低了直肠前部而非回肠中总的和特定细菌16S rRNA的丰度。与饮食诱导的微生物群变化相关，直肠前部细菌发酵酶基因转录本（乙酸激酶、乳酸脱氢酶和羟丁酰辅酶A脱氢酶）的表达水平降低。为了评估发酵代谢产物对宿主肠内分泌功能的影响，给花粉受限的蜜蜂喂食了一种等摩尔混合的有机酸钠盐（乙酸盐、乳酸盐、丁酸盐、甲酸盐和琥珀酸盐）。有机酸喂养显著影响后肠肠内分泌信号基因的表达，挽救了花粉限制的一些影响。这具体表现为神经肽F和咽侧体抑制素途径的组织依赖性表达模式，这些途径与能量代谢和摄食行为有关。我们的研究结果为蜜蜂的饮食-微生物群-宿主轴提供了新的见解，并可能为未来通过基于饮食的微生物群操纵来改善蜜蜂健康的努力提供参考。
