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

Host and gut microbiome modulate the antiparasitic activity of nectar metabolites in a bumblebee pollinator.
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DOI:
10.1098/rstb.2021.0162
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发表时间:
2022-06-20
影响因子:
6.3
通讯作者:
Stevenson, Philip C.
Stevenson, Philip C.
中科院分区:
生物学1区
文献类型:
--
作者:
Koch, Hauke;Welcome, Vita;Kendal-Smith, Amy;Thursfield, Lucy;Farrell, Iain W.;Langat, Moses K.;Brown, Mark J. F.;Stevenson, Philip C.

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抗菌花蜜次生代谢物可以通过预防或减少寄生虫感染来支持传粉者的健康。为了更好地了解传粉媒介中花蜜代谢物-寄生虫相互作用的结果,我们确定了宿主或常驻微生物群在肠道通道中是否通过化学修饰改变了抗寄生虫活性。我们研究了椴树(Tilia spp.)和草莓树(Arbutus unedo)花蜜化合物的相互作用。在体外和在地大黄蜂体内对普通大黄蜂肠道寄生虫炸弹蚜有抑制作用。天莲花蜜中的一种化合物,1-[4-(1-羟基-1-甲基乙基)-1,3-环己二烯-1-羧酸盐]-6- o -β-d- glucopyranoyl -β-d-glucopyranose(天莲皂苷),在体外自然浓度下没有抑制作用,但可以减少B. terrestris工人的bombi感染。与微生物组状态无关,tiliaside在肠道通道中被去糖基化,从而增加了其在后肠(C. bombi感染部位)的抗寄生虫活性。相反,unedone首先在中肠中糖基化,而不受微生物组对unedone-8- o -β-d-葡糖苷的影响,使其对C. bombi无活性,但随后在后肠的微生物组中去糖基化,恢复其活性。因此,我们表明宿主或微生物组对花蜜代谢物的转化调节了花蜜代谢物的抗寄生活性。本文是主题“影响传粉媒介健康的自然过程:从化学到景观”的一部分。
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 of nectar metabolites. This article is part of the theme issue ‘Natural processes influencing pollinator health: from chemistry to landscapes’.
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