Colony-Level Effects of Amygdalin on Honeybees and Their Microbes

Tauber, James P.; Tozkar, Cansu Özge; Schwarz, Ryan S.; Lopez, Dawn; Irwin, Rebecca E.; Adler, Lynn S.; Evans, Jay D.

doi:10.3390/insects11110783

Cited by 9 publications

(17 citation statements)

References 89 publications

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“…Microbe counting using NGS reads essentially followed (Tauber et al, 2020), which contains a detailed workflow and command lines: demultiplexed and trimmed files were run in fastp for quality control (Chen et al, 2018), Hisat2 to remove honeybee reads (Kim et al, 2019), files manipulated using samtools (Li et al, 2009), Kraken2 to count microbe‐derived reads (using only paired reads) (Wood et al, 2019), and correction of counts with Bracken (Lu et al, 2017). The Confidence score for the Kraken2 algorithm was increased to 0.1 for this work.…”

Section: Methodsmentioning

confidence: 99%

Honeybee intestines retain low yeast titers, but no bacterial mutualists, at emergence

Tauber

McMahon

Ryabov

et al. 2021

Yeast

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Honeybee symbionts, predominantly bacteria, play important roles in honeybee health, nutrition, and pathogen protection, thereby supporting colony health. On the other hand, fungi are often considered indicators of poor bee health, and honeybee microbiome studies generally exclude fungi and yeasts. We hypothesized that yeasts may be an important aspect of early honeybee biology, and if yeasts provide a mutual benefit to their hosts, then honeybees could provide a refuge during metamorphosis to ensure the presence of yeasts at emergence. We surveyed for yeast and fungi during pupal development and metamorphosis in worker bees using fungal‐specific quantitative polymerase chain reaction (qPCR), next‐generation sequencing, and standard microbiological culturing. On the basis of yeast presence in three distinct apiaries and multiple developmental stages, we conclude that yeasts can survive through metamorphosis and in naïve worker bees, albeit at relatively low levels. In comparison, known bacterial mutualists, like Gilliamella and Snodgrassella, were generally not found in pre‐eclosed adult bees. Whether yeasts are actively retained as an important part of the bee microbiota or are passively propagating in the colony remains unknown. Our demonstration of the constancy of yeasts throughout development provides a framework to further understand the honeybee microbiota.

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Section: Methodsmentioning

confidence: 99%

Honeybee intestines retain low yeast titers, but no bacterial mutualists, at emergence

Tauber

McMahon

Ryabov

et al. 2021

Yeast

Self Cite

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“…Although bees and their native microbiota seem to tolerate relatively high doses of amygdalin, parasites that commonly inhabit the bee gut may not fare as well. There is increasing evidence that metabolites in nectar and pollen, even those considered toxic in some cases, can improve pollinator health at specific concentrations by controlling or reducing parasite loads (16,29,(50)(51)(52). Indeed, bees tend to forage on specific plants as a means of reducing colony pathogen loads (51).…”

Section: Discussionmentioning

confidence: 99%

“…Indeed, bees tend to forage on specific plants as a means of reducing colony pathogen loads (51). For example, honey bees from hives treated with amygdalin exhibited decreased levels of infection by the parasite Lotmaria passim and some viruses (29). In contrast, this does not seem to be the case for Crithidia infection in bumble bees, whose loads are not reduced after amygdalin exposure (53), as the parasite is not susceptible to amygdalin (54).…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, amygdalin itself does not show antibacterial effects in vitro , and the honey bee gut microbiota appears not to be significantly affected by amygdalin exposure (29). In fact, colony-level exposure to amygdalin may protect bees against some parasites, such as Lotmaria passim (29), and reduce the titer of pathogenic viruses (29, 30), suggesting a potential trade-off in metabolizing amygdalin.…”

Section: Introductionmentioning

confidence: 99%

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Cooperative host-microbe metabolism of a plant toxin in bees

Motta

Gage

Smith

et al. 2022

Preprint

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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.

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“…Studies that have looked for effects of phytochemicals on immune gene expression have generally found them, though nearly all such studies have used the western honey bee ( Boncristiani et al, 2012 ; Lu et al, 2020 ; Mao et al, 2013 ; Palmer-Young et al, 2017c ). Compound classes that influence immune gene regulation include alkaloids ( Lu et al, 2020 ; Palmer-Young et al, 2017c ), terpenoids ( Boncristiani et al, 2012 ; Palmer-Young et al, 2017c ), phenolic acids ( Mao et al, 2013 ; Palmer-Young et al, 2017c ), and iridoid glycosides ( Palmer-Young et al, 2017c ), with two studies finding no effect of the cyanogenic glycoside amygdalin on AMP expression ( Palmer-Young et al, 2017c ; Tauber et al, 2020 ). Most studies document a positive relationship between phytochemical consumption and immune gene expression ( Lu et al, 2020 ; Mao et al, 2013 ; Palmer-Young et al, 2017c ), suggesting an immune-boosting effect of phytochemical consumption, but Boncristiani et al (2012) found that thymol exposure downregulated immune recognition and signaling, although AMP production was unaffected.…”

Section: Host-mediated Effectsmentioning

confidence: 99%