Ecological Stability Emerges at the Level of Strains in the Human Gut Microbiome

Wolff, Richard; Shoemaker, William R.; Garud, Nandita R.

doi:10.1128/mbio.02502-22

Cited by 27 publications

(40 citation statements)

References 55 publications

(127 reference statements)

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“…S1). Combined with the overwhelming stationarity of microbial abundance trajectories within healthy individuals not undergoing major lifestyle changes 15,32,33 , these results support our assertion that dietary patterns are largely stable over weeks-to-months and stool samples provide stable, steady-state population abundance estimates of abundant gut commensal bacteria.…”

Section: Characterizing the Relationships Between Gut Commensal Popul...supporting

confidence: 77%

“…1-2). Thus, as prior work has indicated 15,32 , bacterial taxa in the gut have stable average population sizes, which likely represent steady-state endpoints of internal dynamics (Figs. 1-2).…”

Section: Discussionmentioning

confidence: 74%

“…Early experiments by Jaques Monod 24 identified distinct growth phases for bacterial populations in culture, which can be captured by the stochastic logistic growth equation (sLGE) 25 . The sLGE has been shown to be a good fit for bacterial population growth in vitro and in realworld, steady-state ecosystems [26][27][28][29][30][31][32] . We used the sLGE to study statistical relationships between population sizes and growth rates across the various phases of growth (i.e., acceleration, mid-log, deceleration, stationary phases) to see if we could extract in situ growth phase information.…”

Section: Introductionmentioning

confidence: 99%

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Growth phase estimation for abundant bacterial populations sampled longitudinally from human stool metagenomes

Lim

Diener

Gibbons

2022

Preprint

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Longitudinal sampling of the stool has yielded important insights into the ecological dynamics of the human gut microbiome. However, due to practical limitations, the most densely sampled time series from the human gut are collected at a frequency of about once per day, while the population doubling times for gut commensals are on the order of minutes-to-hours. Despite this, much of the prior work on human gut microbiome time series modeling has, implicitly or explicitly, assumed that day-to-day fluctuations in taxon abundances are related to population growth or death rates, which is likely not the case. Here, we propose an alternative model of the human gut as a continuous flow ecosystem at a dynamical steady state, where population dynamics occur internally and the bacterial population sizes measured in stool represent an endpoint of these internal dynamics. We formalize this idea as stochastic logistic growth of a population held at a constant dilution rate. We show how this model provides a path toward estimating the growth phases of gut bacterial populations in situ. We assess our model predictions against densely-sampled human stool metagenomic time series data. Consistent with our model, donors with slower defecation rates tended to harbor a larger proportion of taxa in later growth phases, while faster defecation rates were associated with more taxa in earlier growth phases. We discuss how these growth phase estimates may be used to better inform metabolic modeling in flow-through ecosystems, like animal guts or industrial bioreactors.

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Section: Characterizing the Relationships Between Gut Commensal Popul...supporting

confidence: 77%

Section: Discussionmentioning

confidence: 74%

Section: Introductionmentioning

confidence: 99%

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Growth phase estimation for abundant bacterial populations sampled longitudinally from human stool metagenomes

Lim

Diener

Gibbons

2022

Preprint

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“…Recent results suggest that ecological dynamics starts to decouple at much finer phylogenetic resolutions [54]. Moreover, strains seem to still obey the three macroecological laws of variation and diversity valid at species level [55]. These results leave open the question of how ecological forces shape the variation of community composition at finer phylogenetic scales.…”

Section: Discussionmentioning

confidence: 99%

Environmental fluctuations explain the universal decay of species-abundance correlations with phylogenetic distance

Sireci

Muñoz

Grilli

2022

Preprint

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Multiple ecological forces act together in shaping the composition of microbial communities. Phyloecology approaches ---which combine phylogenetic relationships with community ecology--- have the potential to disentangle such forces, but are often hard to connect with quantitative predictions from theoretical models. On the other hand, macroecology, which focuses on statistical patterns of abundance and diversity, provides natural connections with theoretical models but often neglects inter-speficic correlations and interactions. Here, we propose a unified framework combining both such approaches to microbial communities. In particular, by using both cross-sectional and longitudinal abundance metagenomic data, we reveal the existence of a novel empirical macroecological law establishing that correlations in species-abundance fluctuations across communities decay from positive to null values as a function of phylogenetic similarity in a consistent manner across ecologically distinct microbiomes. We formulate three mechanistic models ---relying on alternative ecological forces--- that produce distinct predictions. We conclude that the empirically observed macroecological pattern can be quantitatively explained as a result of fluctuating shared resources, i.e. environmental filtering and not e.g. as a result of species competition. Finally, we also show that the macroecological law is also valid for temporal data of a single community, and that the properties of delayed temporal correlations are reproduced by our model.

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“…With our coarse-graining procedures established, we begin our macroecological investigation. Recent efforts have found that the distribution of abundances of a given taxon maintains a consistent statistically similar form across independent sites and time, a pattern known as the Abundance Fluctuation Distribution [37–39, 43, 44]. By coarse-graining empirical AFDs and rescaling them by their mean and variance (i.e., standard score), we see that AFDs from the human gut microbiome retain their shape across phylogenetic scales (Fig.…”

Section: Resultsmentioning

confidence: 81%

Investigating macroecological patterns in coarse-grained microbial communities using the stochastic logistic model of growth

Shoemaker

Grilli

2023

Preprint

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Microbial communities are intrinsically hierarchical due to the shared evolutionary history of community members. This history is primarily captured through taxonomic assignment and phylogenetic reconstruction, sources of information that are frequently used to group microbes into higher levels of organization in experimental and natural communities. However, our understanding of how community diversity depends on one’s scale of observation has yet to be systematically examined. This omission is not simply a methodological detail, as the shared history of community members captured by taxonomic and phylogenetic information provides an opportunity to investigate how patterns of diversity and abundance (i.e., macroecology) are altered across scales of organization. Here, we evaluate the extent that macroecological laws endure across taxonomic and phylogenetic scales among disparate environments using data from the Earth Microbiome Project. We found that measures of biodiversity at a given scale can be consistently predicted using predictions derived from a minimal model containing zero free parameters, the Stochastic Logistic Model of growth (SLM). Extending these within-scale results, we examine the relationship between measures of biodiversity calculated at different scales (e.g., genus vs. family), an empirical prediction known as the Diversity Begets Diversity (DBD) hypothesis. We found that the relationship between richness estimates at different scales can be quantitatively predicted assuming Independence among community members. Contrastingly, only by including correlations between species (i.e., interactions) can we predict the relationship between estimates of diversity at different scales. The results of this study characterize novel microbial patterns across scales of organization and establish a sharp demarcation between recently proposed macroecological patterns that can and cannot be captured by a minimal model of biodiversity.

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Ecological Stability Emerges at the Level of Strains in the Human Gut Microbiome

Cited by 27 publications

References 55 publications

Growth phase estimation for abundant bacterial populations sampled longitudinally from human stool metagenomes

Growth phase estimation for abundant bacterial populations sampled longitudinally from human stool metagenomes

Environmental fluctuations explain the universal decay of species-abundance correlations with phylogenetic distance

Investigating macroecological patterns in coarse-grained microbial communities using the stochastic logistic model of growth

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