Constraints on microbial metabolism drive evolutionary diversification in homogeneous environments

Gudelj, Ivana; Beardmore, Robert; Arkin, Sinan Sadi; MacLean, R. Craig

doi:10.1111/j.1420-9101.2007.01376.x

Cited by 65 publications

(81 citation statements)

References 47 publications

(70 reference statements)

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“…However, if more than two processes are involved (Doebeli and Ispolatov, 2010) or if ecological or genetic aspects are considered (Gudelj et al, 2007), then verbal arguments are insufficient, and mathematical modeling offers a rigorous and objective way to predict evolutionary outcomes.…”

Section: The Consequences Of Biochemical Conflictsmentioning

confidence: 99%

“…If the shape of the constraint function is known for a set of metabolic processes, then simple evolutionary models can be used to predict whether specialization is likely to evolve (Doebeli, 2002;Gudelj et al, 2007;Figure 2). For the models discussed in Figure 2, metabolic generalists evolve for concave constraint functions (weak conflicts between processes) whereas metabolic specialists evolve for convex constraint functions (strong conflicts between processes).…”

Section: The Consequences Of Biochemical Conflictsmentioning

confidence: 99%

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Metabolic specialization and the assembly of microbial communities

et al. 2012

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Metabolic specialization is a general biological principle that shapes the assembly of microbial communities. Individual cell types rarely metabolize a wide range of substrates within their environment. Instead, different cell types often specialize at metabolizing only subsets of the available substrates. What is the advantage of metabolizing subsets of the available substrates rather than all of them? In this perspective piece, we argue that biochemical conflicts between different metabolic processes can promote metabolic specialization and that a better understanding of these conflicts is therefore important for revealing the general principles and rules that govern the assembly of microbial communities. We first discuss three types of biochemical conflicts that could promote metabolic specialization. Next, we demonstrate how knowledge about the consequences of biochemical conflicts can be used to predict whether different metabolic processes are likely to be performed by the same cell type or by different cell types. We then discuss the major challenges in identifying and assessing biochemical conflicts between different metabolic processes and propose several approaches for their measurement. Finally, we argue that a deeper understanding of the biochemical causes of metabolic specialization could serve as a foundation for the field of synthetic ecology, where the objective would be to rationally engineer the assembly of a microbial community to perform a desired biotransformation.

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Section: The Consequences Of Biochemical Conflictsmentioning

confidence: 99%

Section: The Consequences Of Biochemical Conflictsmentioning

confidence: 99%

Metabolic specialization and the assembly of microbial communities

et al. 2012

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“…The growth rate (i.e. absolute fitness) at a given resource concentration S is denoted G(x,S) and defined by [3] where c(x) is cell yield per unit resource (for further details see supplement 1--7). Equations [2] and [3] can capture two trade--offs.…”

mentioning

confidence: 99%

Metabolic trade-offs and the maintenance of the fittest and the flattest

Beardmore

Gudelj

Lipson

et al. 2011

Nature

119

138

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How is diversity maintained? While environmental heterogeneity is considered important 1 , diversity in seemingly homogeneous environments is nonetheless observed 2 . This, it is assumed, must either be owing to weak selection, mutational input or a fitness advantage to genotypes when rare 1 .Here we demonstrate the possibility of a new general mechanism of stable diversity maintenance, one that stems from metabolic and physiological trade--offs 3 . The model requires that such trade--offs translate into a fitness landscape in which the most fit has unfit near--mutational neighbours, while a lower fitness peak exists that is more mutationally robust. The "survival of the fittest" applies at low mutation rates, giving way to "survival of the flattest 4,5,6 " at high mutation rates. However, as a consequence of quasispecies--level negative frequency--dependent selection and differences in mutational robustness we observe a transition zone in which both fittest and flattest co--exist. While diversity maintenance is possible for simple organisms in simple environments, the more trade--offs the wider the maintenance zone. The principle may be applied to lineages within a species or species within a community, potentially explaining why competitive exclusion need not be observed in homogeneous environments. This principle predicts the enigmatic richness of metabolic strategies in clonal bacteria 7 and questions the safety of lethal mutagenesis 8,9 as an antimicrobial treatment.

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“…The simplest method to test for a rateyield trade-off is to measure the yield of microbial cultures grown at different resource uptake rates. Such experiments consistently find evidence of a trade-off between the rate and yield of entire metabolic pathways (Weusthuis et al, 1994;Kreft, 2004;Gudelj et al, 2007). For example, a very convincing trade-off between the rate and yield of glucose metabolism has been demonstrated in the yeast Saccharomyces cerevisiae (Figure 1b).…”

Section: Metabolic Constraints Generate Social Conflictsmentioning

confidence: 85%

“…Early theoretical studies addressed this question by modeling pairwise competition between hypothetical strains of microbe that consume resources rapidly or efficiently. The outcome of these models is simple: under competition for a common resource, the selfish strain with a high rate of ATP production always displaces the prudent strain with a high yield of ATP production, revealing the potential for metabolic trade-offs to generate a tragedy of the commons (Pfeiffer et al, 2001;Frick and Schuster, 2003;Kreft, 2004;Gudelj et al, 2007). This outcome changes when individuals compete for local pools of resources with their neighbors, as occurs in structured populations such as a bacterial biofilm (Kreft, 2004).…”

Section: Theoretical Modelsmentioning

confidence: 98%

The tragedy of the commons in microbial populations: insights from theoretical, comparative and experimental studies

2007

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First principles of thermodynamics imply that metabolic pathways are faced with a trade-off between the rate and yield of ATP production. Simple evolutionary models argue that this trade-off generates a fundamental social conflict in microbial populations: average fitness in a population is highest if all individuals exploit common resources efficiently, but individual reproductive rate is maximized by consuming common resources at the highest possible rate, a scenario known as the tragedy of the commons. In this paper, I review studies that have addressed two key questions: What is the evidence that the rate-yield trade-off is an evolutionary constraint on metabolic pathways? And, if so, what determines evolutionary outcome of the conflicts generated by this trade-off? Comparative studies and microbial experiments provide evidence that the rate-yield trade-off is an evolutionary constraint that is driven by thermodynamic constraints that are common to all metabolic pathways and pathway-specific constraints that reflect the evolutionary history of populations. Microbial selection experiments show that the evolutionary consequences of this trade-off depend on both kin selection and biochemical constraints. In wellmixed populations with low relatedness, genotypes with rapid and efficient metabolism can coexist as a result of negative frequency-dependent selection generated by density-dependent biochemical costs of rapid metabolism. Kin selection can promote the maintenance of efficient metabolism in structured populations with high relatedness by ensuring that genotypes with efficient metabolic pathways gain an indirect fitness benefit from their competitive restraint. I conclude by suggesting avenues for future research and by discussing the broader implications of this work for microbial social evolution.

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Constraints on microbial metabolism drive evolutionary diversification in homogeneous environments

Cited by 65 publications

References 47 publications

Metabolic specialization and the assembly of microbial communities

Metabolic specialization and the assembly of microbial communities

Metabolic trade-offs and the maintenance of the fittest and the flattest

The tragedy of the commons in microbial populations: insights from theoretical, comparative and experimental studies

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