Probabilistic Invasion Underlies Natural Gut Microbiome Stability

Species compositions of gut microbiomes impact host health [1–3], 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 [4, 5]. Stochastic f...

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Bibliographic Details
Published in:	Current biology Vol. 27; no. 13; pp. 1999 - 2006.e8
Main Authors:	Obadia, Benjamin, Güvener, Z.T., Zhang, Vivian, Ceja-Navarro, Javier A., Brodie, Eoin L., Ja, William W., Ludington, William B.
Format:	Journal Article
Language:	English
Published:	England Elsevier Ltd 10-07-2017 Elsevier
Subjects:	Animals bacterial community colonization Drosophila Drosophila melanogaster - microbiology Drosophila melanogaster - physiology Female Gastrointestinal Microbiome Gastrointestinal Tract - microbiology gut bacteria invasion Lactobacillus lottery model microbiome population bottleneck Probability stochastic assembly Symbiosis stochastic assembly invasion colonization Drosophila population bottleneck gut bacteria bacterial community microbiome lottery model Lactobacillus
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Summary:	Species compositions of gut microbiomes impact host health [1–3], 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 [4, 5]. Stochastic factors during establishment may drive these alternative stable states (colonized versus non-colonized) [6, 7], which can influence susceptibility to pathogens, such as Clostridium difficile. Here 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. Therefore, 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. [Display omitted] •Establishment of commensal bacteria in the gut works like a lottery•Stochastic factors generate alternate stable states of gut colonization•Distinct spatial habitats within the gut regulate the maximal chance of colonization•Resident species reduce the odds of subsequent colonization, promoting stability Each person has a unique microbiome, like a fingerprint. Obadia et al. use a fruit fly microbiome model to show how this unique fingerprint could become established by stochastic processes. The results suggest strategies to engineer microbiome diversity.
Bibliography:	USDOE AC02-05CH11231 Lead Contact
ISSN:	0960-9822 1879-0445
DOI:	10.1016/j.cub.2017.05.034