Cooperative host-microbe metabolism of a plant toxin in bees

Abstract

During pollination, bees are exposed to a myriad of xenobiotics, including plant metabolites, which may exert a wide range of effects on their health. Although bees encode enzymes that help in the metabolism of xenobiotics, they still have reduced detoxification gene diversity when compared to other insects, and may rely on other components of their physiology, such as the microbiota, to degrade potentially toxic molecules. In this study, we show that amygdalin, a cyanogenic glycoside found in honey bee-pollinated almond trees, can be metabolized by both bees and members of the gut microbiota. In microbiota-deprived bees, amygdalin is degraded into prunasin, leading to prunasin accumulation in the midgut and hindgut. In microbiota-colonized bees, on the other hand, amygdalin is degraded even further, and prunasin does not accumulate in the gut, suggesting that the microbiota contribute to the full degradation of amygdalin into hydrogen cyanide. In vitro experiments demonstrated that amygdalin degradation by bee gut bacteria is strain-specific and not characteristic of a particular genus or species. We found strains of Bifidobacterium, Bombilactobacillus and Gilliamella that can degrade amygdalin, and the degradation mechanism appears to vary since only some strains produce prunasin as an intermediate. Finally, we investigated the basis of degradation in Bifidobacterium wkB204, a strain that fully degrades amygdalin. We found overexpression and secretion of several carbohydrate-degrading enzymes, including one in glycoside hydrolase family 3 (GH3). We expressed this GH3 in Escherichia coli and detected prunasin as a byproduct when cell lysates were cultured with amygdalin, supporting its contribution to amygdalin degradation. These findings demonstrate that both host and microbiota can act together to metabolize dietary plant metabolites. How amygdalin degradation into hydrogen cyanide affects bee health remains to be elucidated.

Host trees partially explain the complex bacterial communities of two threatened saproxylic beetles

“…Most studies dealing with the dynamics and functions of bacterial symbionts in insects focus on a few model species, such as Drosophila flies (Douglas, 2018) , or on some aphids and bees (McLean et al, 2019, Motta andMoran, 2024). However, knowledge of the diversity and roles of symbionts in the vast majority of insects, a group that makes up most of the world's diversity, is extremely limited (Salem et al, 2023).…”

Bumble bee microbiota shows temporal succession and increase of lactic acid bacteria when exposed to outdoor environments

“…Microbes play an essential role for bee health and resistance, as they help not only with digestion and nutrient uptake (Zheng et al, 2017;Bonilla-Rosso and Engel, 2018), but provide protection against stressors like pathogens, parasites and toxins (Engel et al, 2012;Cariveau et al, 2014;Daisley et al, 2020;Motta et al, 2022). For the large earth bumble bee (B. terrestris) as well as the common eastern bumble bee (B. impatiens), the microbiota is an important driver for the resistance against infections with the parasite Crithidia bombi Schmid-Hempel, 2011b, 2012;Mockler et al, 2018).…”