Department of Natural Capital and Plant Health, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, UK.
Department of Natural Capital and Plant Health, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, UK; Department of Biology and Biochemistry, University of Bath, Bath, Somerset BA2 7AX, UK.
Curr Biol. 2019 Oct 21;29(20):3494-3500.e5. doi: 10.1016/j.cub.2019.08.037. Epub 2019 Oct 10.
Plant phytochemicals can act as natural "medicines" for animals against parasites [1-3]. Some nectar metabolites, for example, reduce parasite infections in bees [4-7]. Declining plant diversity through anthropogenic landscape change [8-11] could reduce the availability of medicinal nectar plants for pollinators, exacerbating their decline [12]. Existing studies are, however, limited by (1) a lack of mechanistic insights into how phytochemicals affect pollinator diseases and (2) the restriction to few, commercially available chemicals, thereby potentially neglecting plants with the biggest antiparasitic effects. To rapidly identify plants with the greatest potential as natural bee medicines, we developed a bioactivity-directed fractionation assay for nectar metabolites. We evaluated 17 important nectar plants against the bumblebee pathogen Crithidia bombi (Trypanosomatidae) [13-17]. The most bioactive species was heather (Calluna vulgaris), the second most productive UK nectar plant [10]. We identified 4-(3-oxobut-1-enylidene)-3,5,5-trimethylcyclohex-2-en-1-one (callunene) from heather nectar as a potent inhibitor of C. bombi. Wild bumblebees (Bombus terrestris) foraging on heather ingest callunene at concentrations causing complete C. bombi inhibition. Feeding on callunene was prophylactic against infections. We show that C. bombi establishes infections by flagellar anchoring to the ileum epithelium. Short-term callunene exposure induced flagellum loss in C. bombi choanomastigotes, resulting in a loss of infectivity. We conclude that plant secondary metabolites can disrupt parasite flagellum attachment, revealing a mechanism behind their prophylactic effects. The decline of heathlands [18-21] reduces the availability of natural bee "medicine" and could exacerbate the contribution of diseases to pollinator declines. VIDEO ABSTRACT.
植物次生代谢物可以作为动物对抗寄生虫的天然“药物”[1-3]。例如，一些花蜜代谢物可以降低蜜蜂的寄生虫感染[4-7]。人为景观变化导致植物多样性下降[8-11]，可能会减少传粉媒介可用的药用花蜜植物，从而加剧它们的衰落[12]。然而，现有研究受到以下两个方面的限制：（1）缺乏关于次生代谢物如何影响传粉媒介疾病的机制见解；（2）限制于少数几种商业可用的化学物质，从而可能忽略了具有最大抗寄生虫效果的植物。为了快速确定最具潜力的植物作为天然蜜蜂药物，我们开发了一种针对花蜜代谢物的生物活性导向的分级分离测定法。我们评估了 17 种重要的花蜜植物对熊蜂病原体布氏锥虫（Trypanosomatidae）[13-17]的作用。最具生物活性的物种是石楠花（Calluna vulgaris），是英国第二大生产花蜜的植物[10]。我们从石楠花蜜中鉴定出 4-(3-氧代丁烯基亚基)-3,5,5-三甲基环己-2-烯-1-酮（石楠烯），它是一种有效的 C. bombi 抑制剂。在石楠花上觅食的野生熊蜂（Bombus terrestris）摄入的石楠烯浓度足以完全抑制 C. bombi。摄入石楠烯具有预防感染的作用。我们表明，C. bombi 通过鞭毛固定在回肠上皮来建立感染。短时间暴露于石楠烯会导致 C. bombi 的鞭毛丧失，从而丧失感染力。我们得出结论，植物次生代谢物可以破坏寄生虫鞭毛的附着，揭示了它们预防作用的机制。石南荒地的减少[18-21]降低了天然蜜蜂“药物”的可获得性，并可能加剧疾病对传粉媒介减少的贡献。视频摘要。
