Niche partitioning facilitates coexistence of closely related honey bee gut bacteria
- University of Lausanne, Switzerland
- ETH Zürich, Switzerland
- ETH Zurich, Switzerland
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.
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Lactobacillus Firm5 amplicon sequencingNCBI Sequence Read Archive PRJNA700984.
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Lactobacillus Firm5 in vivo and in vitro RNA sequencingNCBI Gene Expression Omnibus GSE166724.
Article and author information
Author details
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.
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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Niche partitioning facilitates coexistence of closely related honey bee gut bacteria
eLife 10:e68583.
https://doi.org/10.7554/eLife.68583
Further reading
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- Ecology
Behavioral strategies for foraging and reproduction in the oriental fruit fly (Bactrocera dorsalis) are alternative options for resource allocation and are controlled by neuropeptides. Here, we show that the behavioral switch between foraging and reproduction is associated with changes in antennal sensitivity. Starved flies became more sensitive to food odors while suppressing their response to opposite-sex pheromones. The gene encoding sulfakinin receptor 1 (SkR1) was significantly upregulated in the antennae of starved flies, so we tested the behavioral phenotypes of null mutants for the genes encoding the receptor (skr1–/–) and its ligand sulfakinin (sk–/–). In both knockout lines, the antennal responses shifted to mating mode even when flies were starved. This suggests that sulfakinin signaling via SkR1 promotes foraging while suppressing mating. Further analysis of the mutant flies revealed that sets of odorant receptor (OR) genes were differentially expressed. Functional characterization of the differentially expressed ORs suggested that sulfakinin directly suppresses the expression of ORs that respond to opposite-sex hormones while enhancing the expression of ORs that detect food volatiles. We conclude that sulfakinin signaling via SkR1, modulating OR expressions and leading to altered antenna sensitivities, is an important component in starvation-dependent behavioral change.
