Flagellum Removal by a Nectar Metabolite Inhibits Infectivity of a Bumblebee Parasite

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. [Display omitted] •Callunene from heather nectar inhibits the bumblebee parasite Crithidia bombi•C. bombi anchors to the ileum epithelium using its flagellum•Callunene removes the flagellum, resulting in reduced infectivity of C. bombi•Heathland declines could reduce access to this natural antimicrobial for bumblebees Koch et al. elucidate the first mechanism that explains how nectar secondary metabolites reduce infection by the common bumblebee parasite Crithidia bombi; exposure to callunene, a megastigmene from heather nectar, results in the loss of the parasite flagellum, leading to reduced infectivity.