Host-microbiome metabolism of a plant toxin in bees

  1. Erick VS Motta  Is a corresponding author
  2. Alejandra Gage
  3. Thomas E Smith
  4. Kristin J Blake
  5. Waldan K Kwong
  6. Ian M Riddington
  7. Nancy Moran  Is a corresponding author
  1. The University of Texas at Austin, United States
  2. Instituto Gulbenkian de Ciência, Portugal

Abstract

While foraging for nectar and pollen, bees are exposed to a myriad of xenobiotics, including plant metabolites, which may exert a wide range of effects on their health. Although the bee genome encodes enzymes that help in the metabolism of xenobiotics, it has lower detoxification gene diversity than the genomes of other insects. Therefore, bees may rely on other components that shape 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. 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.

Data availability

Bacterial strains are available by request from the Moran Lab. The complete genome sequence of strain BI-2.5 has been deposited at DDBJ/ENA/GenBank under the accession CP031513. The genome assemblies for strains BI-1.1, LV-8.1, BI-4G, L5-31, OCC3 and wkB204 have been deposited at DDBJ/ENA/GenBank under the accessions QOCR00000000, QOCS00000000, QOCU00000000, QOCT00000000, QOCV00000000 and JAFMNU020000000, respectively. 16S rRNA amplicon sequencing data are available at NCBI BioProject PRJNA865802.

The following data sets were generated

Article and author information

Author details

  1. Erick VS Motta

    Department of Integrative Biology, The University of Texas at Austin, Austin, United States
    For correspondence
    erickvsm@utexas.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9360-4353
  2. Alejandra Gage

    Department of Integrative Biology, The University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Thomas E Smith

    Department of Integrative Biology, The University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Kristin J Blake

    Department of Chemistry, The University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Waldan K Kwong

    Instituto Gulbenkian de Ciência, Oeiras, Portugal
    Competing interests
    The authors declare that no competing interests exist.
  6. Ian M Riddington

    Department of Integrative Biology, The University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Nancy Moran

    Department of Integrative Biology, The University of Texas at Austin, Austin, United States
    For correspondence
    nancy.moran@austin.utexas.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2983-9769

Funding

National Institute of Food and Agriculture (2018-67013-27540)

  • Nancy Moran

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Hauke Koch, Royal Botanic Gardens, Kew, United Kingdom

Publication history

  1. Received: August 10, 2022
  2. Preprint posted: August 27, 2022 (view preprint)
  3. Accepted: December 5, 2022
  4. Accepted Manuscript published: December 6, 2022 (version 1)

Copyright

© 2022, Motta et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Erick VS Motta
  2. Alejandra Gage
  3. Thomas E Smith
  4. Kristin J Blake
  5. Waldan K Kwong
  6. Ian M Riddington
  7. Nancy Moran
(2022)
Host-microbiome metabolism of a plant toxin in bees
eLife 11:e82595.
https://doi.org/10.7554/eLife.82595
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