Dataset Information

Probabilistic Invasion Underlies Natural Gut Microbiome Stability.

ABSTRACT: 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.

SUBMITTER: Obadia B

PROVIDER: S-EPMC5555957 | biostudies-literature | 2017 Jul

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Probabilistic Invasion Underlies Natural Gut Microbiome Stability.

Obadia Benjamin B Güvener Z T ZT Zhang Vivian V Ceja-Navarro Javier A JA Brodie Eoin L EL Ja William W WW Ludington William B WB

Current biology : CB 20170615 13

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 s ...[more]

PMID: 28625783

Similar Datasets

Project description:BackgroundThe gut microbiome (GM) can influence many biological processes in the host, impacting its health and survival, but the GM can also be influenced by the host's traits. In vertebrates, Major Histocompatibility Complex (MHC) genes play a pivotal role in combatting pathogens and are thought to shape the host's GM. Despite this-and the documented importance of both GM and MHC variation to individual fitness-few studies have investigated the association between the GM and MHC in the wild.ResultsWe characterised MHC class I (MHC-I), MHC class II (MHC-II) and GM variation in individuals within a natural population of the Seychelles warbler (Acrocephalus sechellensis). We determined how the diversity and composition of the GM varied with MHC characteristics, in addition to environmental factors and other host traits. Our results show that the presence of specific MHC alleles, but not MHC diversity, influences both the diversity and composition of the GM in this population. MHC-I alleles, rather than MHC-II alleles, had the greatest impact on the GM. GM diversity was negatively associated with the presence of three MHC-I alleles (Ase-ua3, Ase-ua4, Ase-ua5), and one MHC-II allele (Ase-dab4), while changes in GM composition were associated with the presence of four different MHC-I alleles (Ase-ua1, Ase-ua7, Ase-ua10, Ase-ua11). There were no associations between GM diversity and TLR3 genotype, but GM diversity was positively correlated with genome-wide heterozygosity and varied with host age and field period.ConclusionsThese results suggest that components of the host's immune system play a role in shaping the GM of wild animals. Host genotype-specifically MHC-I and to a lesser degree MHC-II variation-can modulate the GM, although whether this occurs directly, or indirectly through effects on host health, is unclear. Importantly, if immune genes can regulate host health through modulation of the microbiome, then it is plausible that the microbiome could also influence selection on immune genes. As such, host-microbiome coevolution may play a role in maintaining functional immunogenetic variation within natural vertebrate populations. Video abstract.

Project description:The human gut microbiome harbors substantial ecological diversity at the species level as well as at the strain level within species. In healthy hosts, species abundance fluctuations in the microbiome are thought to be stable, and these fluctuations can be described by macroecological laws. However, it is less clear how strain abundances change over time. An open question is whether individual strains behave like species themselves, exhibiting stability and following the macroecological relationships known to hold at the species level, or whether strains have different dynamics, perhaps due to the relatively close phylogenetic relatedness of cocolonizing lineages. Here, we analyze the daily dynamics of intraspecific genetic variation in the gut microbiomes of four healthy, densely longitudinally sampled hosts. First, we find that the overall genetic diversity of a large majority of species is stationary over time despite short-term fluctuations. Next, we show that fluctuations in abundances in approximately 80% of strains analyzed can be predicted with a stochastic logistic model (SLM), an ecological model of a population experiencing environmental fluctuations around a fixed carrying capacity, which has previously been shown to capture statistical properties of species abundance fluctuations. The success of this model indicates that strain abundances typically fluctuate around a fixed carrying capacity, suggesting that most strains are dynamically stable. Finally, we find that the strain abundances follow several empirical macroecological laws known to hold at the species level. Together, our results suggest that macroecological properties of the human gut microbiome, including its stability, emerge at the level of strains. IMPORTANCE To date, there has been an intense focus on the ecological dynamics of the human gut microbiome at the species level. However, there is considerable genetic diversity within species at the strain level, and these intraspecific differences can have important phenotypic effects on the host, impacting the ability to digest certain foods and metabolize drugs. Thus, to fully understand how the gut microbiome operates in times of health and sickness, its ecological dynamics may need to be quantified at the level of strains. Here, we show that a large majority of strains maintain stable abundances for periods of months to years, exhibiting fluctuations in abundance that can be well described by macroecological laws known to hold at the species level, while a smaller percentage of strains undergo rapid, directional changes in abundance. Overall, our work indicates that strains are an important unit of ecological organization in the human gut microbiome.

Dataset Information

Probabilistic Invasion Underlies Natural Gut Microbiome Stability.

Publications

Probabilistic Invasion Underlies Natural Gut Microbiome Stability.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets