1. Ecology
  2. Microbiology and Infectious Disease
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Niche partitioning facilitates coexistence of closely related honey bee gut bacteria

  1. Silvia Brochet
  2. Andrew Quinn
  3. Ruben AT Mars
  4. Nicolas Neuschwander
  5. Uwe Sauer
  6. Philipp Engel  Is a corresponding author
  1. University of Lausanne, Switzerland
  2. ETH Zürich, Switzerland
  3. ETH Zurich, Switzerland
Research Article
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Cite this article as: eLife 2021;10:e68583 doi: 10.7554/eLife.68583

Abstract

Ecological processes underlying bacterial coexistence in the gut are not well understood. Here, we disentangled the effect of the host and the diet on the coexistence of four closely related Lactobacillus species colonizing the honey bee gut. We serially passaged the four species through gnotobiotic bees and in liquid cultures in the presence of either pollen (bee diet) or simple sugars. Although the four species engaged in negative interactions, they were able to stably coexist, both in vivo and in vitro. However, coexistence was only possible in the presence of pollen, and not in simple sugars, independent of the environment. Using metatranscriptomics and metabolomics, we found that the four species utilize different pollen-derived carbohydrate substrates indicating resource partitioning as the basis of coexistence. Our results show that despite longstanding host association, gut bacterial interactions can be recapitulated in vitro providing insights about bacterial coexistence when combined with in vivo experiments.

Data availability

The amplicon sequencing data and the RNA sequencing data are available under the NCBI Bioproject PRJNA700984 and the GEO record GSE166724 respectively.All data generated or analysed during this study are included in the manuscript and supporting files. Bacterial abundance data (CFUs) are included into Supplementary File 3, amplicon sequencing processed data are included into Supplementary File 4, RNA sequencing processed data, statistical analysis results (enrichment tests) and transcript per million data are included into Supplementary File 5-9, metabolomics analysis data are included into Supplementary File 10. All differential expression analysis results of this study are included in Supplementary File 11.

The following data sets were generated

Article and author information

Author details

  1. Silvia Brochet

    Department of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6443-185X
  2. Andrew Quinn

    Department of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1401-1053
  3. Ruben AT Mars

    Institute of Molecular Systems Biology, ETH Zürich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  4. Nicolas Neuschwander

    Department of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  5. Uwe Sauer

    Institute of Molecular Systems Biology, ETH Zurich, Zürich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5923-0770
  6. Philipp Engel

    Department of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
    For correspondence
    philipp.engel@unil.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4678-6200

Funding

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (31003A_160345)

  • Philipp Engel

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (31003A_179487)

  • Andrew Quinn
  • Nicolas Neuschwander
  • Philipp Engel

H2020 European Research Council (714804)

  • Silvia Brochet
  • Philipp Engel

NCCR Microbiomes (51NF40_180575)

  • Philipp Engel

Human Frontier Science Program (RGY0077/2016)

  • Philipp Engel

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

Reviewing Editor

  1. Karina B Xavier, Instituto Gulbenkian de Ciência, Portugal

Publication history

  1. Received: March 19, 2021
  2. Accepted: July 14, 2021
  3. Accepted Manuscript published: July 19, 2021 (version 1)
  4. Accepted Manuscript updated: July 22, 2021 (version 2)

Copyright

© 2021, Brochet 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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Further reading

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    The Varroa destructor mite is a devastating parasite of Apis mellifera honeybees. They can cause colonies to collapse by spreading viruses and feeding on the fat reserves of adults and larvae. Amitraz is used to control mites due to its low toxicity to bees; however, the mechanism of bee resistance to amitraz remains unknown. In this study, we found that amitraz and its major metabolite potently activated all four mite octopamine receptors. Behavioral assays using Drosophila null mutants of octopamine receptors identified one receptor subtype Octβ2R as the sole target of amitraz in vivo. We found that thermogenetic activation of octβ2R-expressing neurons mimics amitraz poisoning symptoms in target pests. We next confirmed that the mite Octβ2R was more sensitive to amitraz and its metabolite than the bee Octβ2R in pharmacological assays and transgenic flies. Furthermore, replacement of three bee-specific residues with the counterparts in the mite receptor increased amitraz sensitivity of the bee Octβ2R, indicating that the relative insensitivity of their receptor is the major mechanism for honeybees to resist amitraz. The present findings have important implications for resistance management and the design of safer insecticides that selectively target pests while maintaining low toxicity to non-target pollinators.

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