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.
-
Lactobacillus Firm5 amplicon sequencingNCBI Sequence Read Archive PRJNA700984.
-
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.
Metrics
-
- 4,029
- views
-
- 610
- downloads
-
- 74
- 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)
Niche partitioning facilitates coexistence of closely related honey bee gut bacteria
eLife 10:e68583.
https://doi.org/10.7554/eLife.68583
Further reading
-
- Ecology
- Microbiology and Infectious Disease
Predicting how species diversity changes along environmental gradients is an enduring problem in ecology. In microbes, current theories tend to invoke energy availability and enzyme kinetics as the main drivers of temperature-richness relationships. Here, we derive a general empirically-grounded theory that can explain this phenomenon by linking microbial species richness in competitive communities to variation in the temperature-dependence of their interaction and growth rates. Specifically, the shape of the microbial community temperature-richness relationship depends on how rapidly the strength of effective competition between species pairs changes with temperature relative to the variance of their growth rates. Furthermore, it predicts that a thermal specialist-generalist tradeoff in growth rates alters coexistence by shifting this balance, causing richness to peak at relatively higher temperatures. Finally, we show that the observed patterns of variation in thermal performance curves of metabolic traits across extant bacterial taxa is indeed sufficient to generate the variety of community-level temperature-richness responses observed in the real world. Our results provide a new and general mechanism that can help explain temperature-diversity gradients in microbial communities, and provide a quantitative framework for interlinking variation in the thermal physiology of microbial species to their community-level diversity.
