1. Ecology
  2. Microbiology and Infectious Disease

Gut Bacteria: Synergy in symbiosis

Honeybees rely on their microbial gut symbionts to overcome a potent toxin found in pollen and nectar.
https://doi.org/10.7554/eLife.85565
Share this article
Cite this article
  1. Aileen Berasategui
  2. Hassan Salem
(2023)
Gut Bacteria: Synergy in symbiosis
eLife 12:e85565.
https://doi.org/10.7554/eLife.85565
  2. Download BibTeX
  3. Download .RIS
  1. Aileen Berasategui
  2. Hassan Salem  Is a corresponding author
  1. Mutualisms Research Group, Max Planck Institute for Biology, Germany

Plants deploy a remarkable range of mechanical structures (such as thorns) and chemical weapons (such as toxins) to protect themselves against herbivores. Secondary metabolites from plants can harm herbivores by disrupting the transport of nutrients or the production of hormones. However, herbivores fight back by detoxifying, isolating or deactivating these metabolites (Mithöfer and Boland, 2012).

Gut microbes in herbivores are also involved in breaking down toxins into less dangerous chemicals (Dearing et al., 2022). Now, in eLife, Nancy Moran and colleagues at the University of Texas at Austin and the Gulbenkian Institute in Portugal – including Eric Motta as first author – report how symbiotic microbes can upgrade the detoxifying capacity of the Western honeybee against amygdalin, a widespread plant toxin (Motta et al., 2022).

Amygdalin is a cyanogenic compound that is found in the nectar and pollen of many of the plant species that bees frequent, including almond, apple and cherry trees. Although bees can fully degrade amygdalin, the mechanism behind this metabolism remained elusive.

Herbivores typically encode specific enzymes that help to break down plant toxins (Erb and Reymond, 2019). However, compared to other insects, bees encode relatively few of these genes, suggesting that the gut microbiome may be involved in degrading plant toxins, including amygdalin.

To test this hypothesis, Motta et al. compared the effects of amygdalin consumption in bees with and without their native gut microbes. They found that honeybees without their microbes can only partially degrade amygdalin into an intermediate, called prunasin. In honeybees harbouring gut microbes, on the other hand, amygdalin is fully broken down into hydrogen cyanide and other derivatives without apparent harmful effects on the bees (Figure 1).

Figure 1
Download asset Open asset
Metabolising plant toxins in the honeybee gut.

Amygdalin is a toxin found in the nectar and pollen of several plants, and it can be harmful if ingested in large quantities. Motta et al. found that bees with gut bacteria (left) were able to fully degrade amygdalin into hydrogen cyanide (HCN) and other metabolites. However, bees without gut bacteria (right) were only able to degrade the chemical to an intermediate compound, called prunasin. This confirmed that enzymes secreted by gut bacteria are essential to fully degrade amygdalin.

Image created with BioRender.com.

Motta et al. then examined the different types of gut bacteria and their ability to cope with varying concentrations of amygdalin, and quantified the metabolic by-products. This revealed that only a few types of bacteria, including a strain of the genus Bifidobacterium, can break down amygdalin. Introducing this bacterial strain into honeybees without gut bacteria enabled them to fully degrade amygdalin, mirroring what happens in bees that harbour a native community of microbes.

Motta et al. then set out to identify the enzymes secreted by Bifidobacterium that are responsible for the break down. When grown in cultures containing amygdalin, the bacterium upregulated the expression of a gene encoding for glycoside hydrolase (GH) family 3, which belongs to a class of enzymes that is known to degrade amygdalin. Expressing the gene encoding GH3 in E. coli, which cannot normally degrade amygdalin, enabled it to break down the metabolite. This confirms the importance of GH3 for the metabolism of amygdalin.

Microbial symbionts are increasingly recognized for their role in reducing the toxicity of plant metabolites in insects. Local environments with a high abundance of toxins may exert a strong selection on microbes in these locations to degrade plant metabolites (Hammer and Bowers, 2015). Herbivores may leverage this metabolic diversity by acquiring new symbionts directly from the environment, or through the exchange of genetic material (e.g., horizontal gene transfer) between gut bacteria (Berasategui et al., 2017; Ceja-Navarro et al., 2015).

Gut symbionts in bees modulate a remarkable range of functions in their hosts, from fermenting complex sugars to fighting off parasites (Kwong et al., 2017; Kwong and Moran, 2016). Motta et al. show that these froles extend to metabolizing plant toxins. Characterizing amygdalin metabolism across different bee species would help clarify if the ability to fully degrade the toxin is a fixed feature of the gut microbiome, or if it is shaped by the environment and the distribution of amygdalin-producing plants. Ultimately, a better understanding of how hosts and gut symbionts interact to degrade toxins, may shed light on the effect of various plant metabolites on bee health, and the different strategies to counteract them.

References

Article and author information

Author details

  1. Aileen Berasategui

    Aileen Berasategui is in the Mutualisms Research Group, Max Planck Institute for Biology, Tuebingen, Germany
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7317-8139

  2. Hassan Salem

    Hassan Salem is in the Mutualisms Research Group, Max Planck Institute for Biology, Tuebingen, Germany
    For correspondence
    hassan.salem@tuebingen.mpg.de
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4135-7407

Publication history

  1. Version of Record published: February 3, 2023 (version 1)

Copyright

© 2023, Berasategui and Salem

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

Metrics

  • 1,026
    Page views
  • 107
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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. Aileen Berasategui
  2. Hassan Salem
(2023)
Gut Bacteria: Synergy in symbiosis
eLife 12:e85565.
https://doi.org/10.7554/eLife.85565

Categories and tags

    1. Related to

    Host-microbiome metabolism of a plant toxin in bees

    Erick VS Motta, Alejandra Gage ... Nancy Moran
  2. Further reading

Further reading

    1. Ecology
    2. Microbiology and Infectious Disease

    Host-microbiome metabolism of a plant toxin in bees

    Erick VS Motta, Alejandra Gage ... Nancy Moran
    Research Article Updated

    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.

  2. Listen to Erick Motta describe how honeybees defend themselves against toxins.

    Podcast

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

    1. Ecology

    The push–pull intercrop Desmodium does not repel, but intercepts and kills pests

    Anna L Erdei, Aneth B David ... Teun Dekker
    Research Article Updated

    Over two decades ago, an intercropping strategy was developed that received critical acclaim for synergizing food security with ecosystem resilience in smallholder farming. The push–pull strategy reportedly suppresses lepidopteran pests in maize through a combination of a repellent intercrop (push), commonly Desmodium spp., and an attractive, border crop (pull). Key in the system is the intercrop’s constitutive release of volatile terpenoids that repel herbivores. However, the earlier described volatile terpenoids were not detectable in the headspace of Desmodium, and only minimally upon herbivory. This was independent of soil type, microbiome composition, and whether collections were made in the laboratory or in the field. Furthermore, in oviposition choice tests in a wind tunnel, maize with or without an odor background of Desmodium was equally attractive for the invasive pest Spodoptera frugiperda. In search of an alternative mechanism, we found that neonate larvae strongly preferred Desmodium over maize. However, their development stagnated and no larva survived. In addition, older larvae were frequently seen impaled and immobilized by the dense network of silica-fortified, non-glandular trichomes. Thus, our data suggest that Desmodium may act through intercepting and decimating dispersing larval offspring rather than adult deterrence. As a hallmark of sustainable pest control, maize–Desmodium push–pull intercropping has inspired countless efforts to emulate stimulo-deterrent diversion in other cropping systems. However, detailed knowledge of the actual mechanisms is required to rationally improve the strategy, and translate the concept to other cropping systems.