Probabilistic Invasion Underlies Natural Gut Microbiome Stability
Abstract
Species compositions of gut microbiomes impact host health, but the processes determining these compositions are largely unknown. An unexplained observation is that gut species composition varies widely between individuals but is largely stable over time within individuals. Stochastic factors during establishment may drive these alternative stable states (colonized versus non-colonized), which can influence susceptibility to pathogens, such as Clostridium difficile. Here, in this study, we sought to quantify and model the dose response, dynamics, and stability of bacterial colonization in the fruit fly (Drosophila melanogaster) gut. Our precise, high-throughput technique revealed stable between-host variation in colonization when individual germ-free flies were fed their own natural commensals (including the probiotic Lactobacillus plantarum). Some flies were colonized while others remained germ-free even at extremely high bacterial doses. Thus, alternative stable states of colonization exist even in this low-complexity model of host-microbe interactions. These alternative states are driven by a fundamental asymmetry between the inoculum population and the stably colonized population that is mediated by spatial localization and a population bottleneck, which makes stochastic effects important by lowering the effective population size. Prior colonization with other bacteria reduced the chances of subsequent colonization, thus increasing the stability of higher-diversity guts. Lastly, stable gutmore »
- Authors:
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1459717
- Alternate Identifier(s):
- OSTI ID: 1426730
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- Current Biology
- Additional Journal Information:
- Journal Name: Current Biology Journal Volume: 27 Journal Issue: 13; Journal ID: ISSN 0960-9822
- Publisher:
- Elsevier
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; microbiome; gut bacteria; Drosophila; Lactobacillus; invasion; colonization; population bottleneck; lottery model; stochastic assembly; bacterial community
Citation Formats
Obadia, Benjamin, Güvener, Z. T., Zhang, Vivian, Ceja-Navarro, Javier A., Brodie, Eoin L., Ja, William W., and Ludington, William B. Probabilistic Invasion Underlies Natural Gut Microbiome Stability. United Kingdom: N. p., 2017.
Web. doi:10.1016/j.cub.2017.05.034.
Obadia, Benjamin, Güvener, Z. T., Zhang, Vivian, Ceja-Navarro, Javier A., Brodie, Eoin L., Ja, William W., & Ludington, William B. Probabilistic Invasion Underlies Natural Gut Microbiome Stability. United Kingdom. https://doi.org/10.1016/j.cub.2017.05.034
Obadia, Benjamin, Güvener, Z. T., Zhang, Vivian, Ceja-Navarro, Javier A., Brodie, Eoin L., Ja, William W., and Ludington, William B. Sat .
"Probabilistic Invasion Underlies Natural Gut Microbiome Stability". United Kingdom. https://doi.org/10.1016/j.cub.2017.05.034.
@article{osti_1459717,
title = {Probabilistic Invasion Underlies Natural Gut Microbiome Stability},
author = {Obadia, Benjamin and Güvener, Z. T. and Zhang, Vivian and Ceja-Navarro, Javier A. and Brodie, Eoin L. and Ja, William W. and Ludington, William B.},
abstractNote = {Species compositions of gut microbiomes impact host health, but the processes determining these compositions are largely unknown. An unexplained observation is that gut species composition varies widely between individuals but is largely stable over time within individuals. Stochastic factors during establishment may drive these alternative stable states (colonized versus non-colonized), which can influence susceptibility to pathogens, such as Clostridium difficile. Here, in this study, we sought to quantify and model the dose response, dynamics, and stability of bacterial colonization in the fruit fly (Drosophila melanogaster) gut. Our precise, high-throughput technique revealed stable between-host variation in colonization when individual germ-free flies were fed their own natural commensals (including the probiotic Lactobacillus plantarum). Some flies were colonized while others remained germ-free even at extremely high bacterial doses. Thus, alternative stable states of colonization exist even in this low-complexity model of host-microbe interactions. These alternative states are driven by a fundamental asymmetry between the inoculum population and the stably colonized population that is mediated by spatial localization and a population bottleneck, which makes stochastic effects important by lowering the effective population size. Prior colonization with other bacteria reduced the chances of subsequent colonization, thus increasing the stability of higher-diversity guts. Lastly, stable gut diversity may be driven by inherently stochastic processes, which has important implications for combatting infectious diseases and for stably establishing probiotics in the gut.},
doi = {10.1016/j.cub.2017.05.034},
journal = {Current Biology},
number = 13,
volume = 27,
place = {United Kingdom},
year = {Sat Jul 01 00:00:00 EDT 2017},
month = {Sat Jul 01 00:00:00 EDT 2017}
}
https://doi.org/10.1016/j.cub.2017.05.034
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