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Metabolic resource allocation in individual microbes determines ecosystem interactions and spatial dynamics.

ABSTRACT: The interspecies exchange of metabolites plays a key role in the spatiotemporal dynamics of microbial communities. This raises the question of whether ecosystem-level behavior of structured communities can be predicted using genome-scale metabolic models for multiple organisms. We developed a modeling framework that integrates dynamic flux balance analysis with diffusion on a lattice and applied it to engineered communities. First, we predicted and experimentally confirmed the species ratio to which a two-species mutualistic consortium converges and the equilibrium composition of a newly engineered three-member community. We next identified a specific spatial arrangement of colonies, which gives rise to what we term the "eclipse dilemma": does a competitor placed between a colony and its cross-feeding partner benefit or hurt growth of the original colony? Our experimentally validated finding that the net outcome is beneficial highlights the complex nature of metabolic interactions in microbial communities while at the same time demonstrating their predictability.

SUBMITTER: Harcombe WR

PROVIDER: S-EPMC4097880 | biostudies-literature | 2014 May

REPOSITORIES: biostudies-literature

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Metabolic resource allocation in individual microbes determines ecosystem interactions and spatial dynamics.

Harcombe William R WR Riehl William J WJ Dukovski Ilija I Granger Brian R BR Betts Alex A Lang Alex H AH Bonilla Gracia G Kar Amrita A Leiby Nicholas N Mehta Pankaj P Marx Christopher J CJ Segrè Daniel D

Cell reports 20140501 4

The interspecies exchange of metabolites plays a key role in the spatiotemporal dynamics of microbial communities. This raises the question of whether ecosystem-level behavior of structured communities can be predicted using genome-scale metabolic models for multiple organisms. We developed a modeling framework that integrates dynamic flux balance analysis with diffusion on a lattice and applied it to engineered communities. First, we predicted and experimentally confirmed the species ratio to w ...[more]

PMID: 24794435

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Project description:BackgroundThe dominant paradigm for modeling the complexities of interacting populations and food webs is a system of coupled ordinary differential equations in which the state of each species, population, or functional trophic group is represented by an aggregated numbers-density or biomass-density variable. Here, using the metaphysiological approach to model consumer-resource interactions, we formulate a two-state paradigm that represents each population or group in a food web in terms of both its quantity and quality.Methodology and principal findingsThe formulation includes an allocation function controlling the relative proportion of extracted resources to increasing quantity versus elevating quality. Since lower quality individuals senescence more rapidly than higher quality individuals, an optimal allocation proportion exists and we derive an expression for how this proportion depends on population parameters that determine the senescence rate, the per-capita mortality rate, and the effects of these rates on the dynamics of the quality variable. We demonstrate that oscillations do not arise in our model from quantity-quality interactions alone, but require consumer-resource interactions across trophic levels that can be stabilized through judicious resource allocation strategies. Analysis and simulations provide compelling arguments for the necessity of populations to evolve quality-related dynamics in the form of maternal effects, storage or other appropriate structures. They also indicate that resource allocation switching between investments in abundance versus quality provide a powerful mechanism for promoting the stability of consumer-resource interactions in seasonally forcing environments.Conclusions/significanceOur simulations show that physiological inefficiencies associated with this switching can be favored by selection due to the diminished exposure of inefficient consumers to strong oscillations associated with the well-known paradox of enrichment. Also our results demonstrate how allocation switching can explain observed growth patterns in experimental microbial cultures and discuss how our formulation can address questions that cannot be answered using the quantity-only paradigms that currently predominate.

Dataset Information

Metabolic resource allocation in individual microbes determines ecosystem interactions and spatial dynamics.

Publications

Metabolic resource allocation in individual microbes determines ecosystem interactions and spatial dynamics.

Similar Datasets

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