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.

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.

Metrics

  • 2,732
    views
  • 474
    downloads
  • 29
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

https://doi.org/10.7554/eLife.82595

Further reading

  1. Honeybees use microbes to break down the toxins found in pollen and nectar

    1. Ecology
    Luis Abdala-Roberts, Adriana Puentes ... Kailen A Mooney
    Review Article

    Global change is causing unprecedented degradation of the Earth’s biological systems and thus undermining human prosperity. Past practices have focused either on monitoring biodiversity decline or mitigating ecosystem services degradation. Missing, but critically needed, are management approaches that monitor and restore species interaction networks, thus bridging existing practices. Our overall aim here is to lay the foundations of a framework for developing network management, defined here as the study, monitoring, and management of species interaction networks. We review theory and empirical evidence demonstrating the importance of species interaction networks for the provisioning of ecosystem services, how human impacts on those networks lead to network rewiring that underlies ecosystem service degradation, and then turn to case studies showing how network management has effectively mitigated such effects or aided in network restoration. We also examine how emerging technologies for data acquisition and analysis are providing new opportunities for monitoring species interactions and discuss the opportunities and challenges of developing effective network management. In summary, we propose that network management provides key mechanistic knowledge on ecosystem degradation that links species- to ecosystem-level responses to global change, and that emerging technological tools offer the opportunity to accelerate its widespread adoption.