Host and gut microbiome modulate the antiparasitic activity of nectar metabolites in a bumblebee pollinator

Hauke Koch, Vita Welcome, Amy Kendal-Smith, Lucy Thursfield, Iain W Farrell, Moses K Langat, Mark J F Brown, Philip C. Stevenson

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Antimicrobial nectar secondary metabolites can support pollinator health by preventing or reducing parasite infections. To better understand the outcome of nectar metabolite-parasite interactions in pollinators, we determined whether the antiparasitic activity was altered through chemical modification by the host or resident microbiome during gut passage. We investigated this interaction with linden (Tilia spp.) and strawberry tree (Arbutus unedo) nectar compounds. Unedone from A. unedo nectar inhibited the common bumblebee gut parasite Crithidia bombi in vitro and in Bombus terrestris gynes. A compound in Tilia nectar, 1-[4-(1-hydroxy-1-methylethyl)-1,3-cyclohexadiene-1-carboxylate]-6-O-β-D-glucopyranosyl-β-D-glucopyranose (tiliaside) showed no inhibition in vitro at naturally occurring concentrations, but reduced C. bombi infections of B. terrestris workers. Independent of microbiome status, tiliaside was deglycosylated during gut passage, thereby increasing its antiparasitic activity in the hindgut, the site of C. bombi infections. Conversely, unedone was first glycosylated in the midgut without influence of the microbiome to unedone-8-O-β-D-glucoside, rendering it inactive against C. bombi, but subsequently deglycosylated by the microbiome in the hindgut, restoring its activity. We therefore show that conversion of nectar metabolites by either the host or the microbiome modulates antiparasitic activity.

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