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
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Understanding the origins of novel, complex phenotypes is a major goal in evolutionary biology. Poison frogs of the family Dendrobatidae have evolved the novel ability to acquire alkaloids from their diet for chemical defense at least three times. However, taxon sampling for alkaloids has been biased towards colorful species, without similar attention paid to inconspicuous ones that are often assumed to be undefended. As a result, our understanding of how chemical defense evolved in this group is incomplete. Here, we provide new data showing that, in contrast to previous studies, species from each undefended poison frog clade have measurable yet low amounts of alkaloids. We confirm that undefended dendrobatids regularly consume mites and ants, which are known sources of alkaloids. Thus, our data suggest that diet is insufficient to explain the defended phenotype. Our data support the existence of a phenotypic intermediate between toxin consumption and sequestration — passive accumulation — that differs from sequestration in that it involves no derived forms of transport and storage mechanisms yet results in low levels of toxin accumulation. We discuss the concept of passive accumulation and its potential role in the origin of chemical defenses in poison frogs and other toxin-sequestering organisms. In light of ideas from pharmacokinetics, we incorporate new and old data from poison frogs into an evolutionary model that could help explain the origins of acquired chemical defenses in animals and provide insight into the molecular processes that govern the fate of ingested toxins.
