Dataset Information

The evolutionary dynamics of metabolic protocells.

ABSTRACT: Protocell multilevel selection models have been proposed to study the evolutionary dynamics of vesicles encapsulating a set of replicating, competing and mutating sequences. The frequency of the different sequence types determines protocell survival through a fitness function. One of the defining features of these models is the genetic load generated when the protocell divides and its sequences are assorted between the offspring vesicles. However, these stochastic assortment effects disappear when the redundancy of each sequence type is sufficiently high. The fitness dependence of the vesicle with its sequence content is usually defined without considering a realistic account on how the lower level dynamics would specify the protocell fitness. Here, we present a protocell model with a fitness function determined by the output flux of a simple metabolic network with the aim of understanding how the evolution of both kinetic and topological features of metabolism would have been constrained by the particularities of the protocell evolutionary dynamics. In our model, the sequences inside the vesicle are both the carriers of information and Michaelis-Menten catalysts exhibiting saturation. We found that the saturation of the catalysts controlling the metabolic fluxes, achievable by modifying the kinetic or stoichiometric parameters, provides a mechanism to ameliorate the assortment load by increasing the redundancy of the catalytic sequences required to achieve the maximum flux. Regarding the network architecture, we conclude that combinations of parallel network motifs and bimolecular catalysts are a robust way to increase the complexity of the metabolism enclosed by the protocell.

SUBMITTER: Pechuan X

PROVIDER: S-EPMC6070278 | biostudies-literature | 2018 Jul

REPOSITORIES: biostudies-literature

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The evolutionary dynamics of metabolic protocells.

Pechuan Ximo X Puzio Raymond R Bergman Aviv A

PLoS computational biology 20180720 7

Protocell multilevel selection models have been proposed to study the evolutionary dynamics of vesicles encapsulating a set of replicating, competing and mutating sequences. The frequency of the different sequence types determines protocell survival through a fitness function. One of the defining features of these models is the genetic load generated when the protocell divides and its sequences are assorted between the offspring vesicles. However, these stochastic assortment effects disappear wh ...[more]

PMID: 30028838

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Project description:Escherichia coli arbitrarily encompasses facultative anaerobic, rod-shaped bacteria with defined respiratory and fermentative types of metabolism. The species diversification has been further advanced by atypical strains whose features deviate from the essential species-specific morphological and metabolic cutoff. The morphological cutoff is exemplified by bacterial filamentation. E. coli filamentation has been studied from two different perspectives: the first considers filamentation as a result of adaptive strategies and response to stress, while the second is based on findings from the cell division of E. coli's conditional mutants. Another cutoff is represented by E. coli's inability to use citrate as a sole carbon and energy source. In this study, we compared two atypical E. coli strains that belong to the same neuroinvasive ecovar but exhibit either of the two phenotypes that deviate from the species' features. While E. coli RS218 exists in the form of filaments incapable of growth on citrate, strain IHE3034 is represented as normal-sized bacteria able to ferment citrate under oxic conditions in the presence of glucose; in this paper, we show that these two phenotypes result from a bona fide trade-off. With the help of comparative proteomics and metabolomics, we discovered the proteome required for the upkeep of these phenotypes. The metabolic profiles of both strains reveal that under aerobic conditions, RS218 undergoes oxidative metabolism, while IHE3034 undergoes anaerobic respiration. Finally, we show that the use of citrate and filament formation are both linked in a trade-off occurring via a c-di-GMP-dependent phase variation event. IMPORTANCE Aerobic use of citrate and filamentous growth are arbitrary cutoffs for the Escherichia coli species. The strains that exhibit them as stable phenotypes are called atypical. In this study, we compare two atypical neuroinvasive E. coli strains, which alternatively display either of these phenotypes. We present the proteome and metabolome required for the maintenance of filamentous growth and show that anaerobic nitrate respiration is the main requirement for the use of citrate. The fact that the two phenotypes are differentially expressed by each strain prompted us to check if they are part of a trade-off. Indeed, these atypical characters are reversible and result from a c-di-GMP phase variation event. Thus, we revealed hidden links between stable morphological and metabolic phenotypes and provided information about alternative evolutionary pathways for the survival of E. coli strains in various host niches.

Dataset Information

The evolutionary dynamics of metabolic protocells.

Publications

The evolutionary dynamics of metabolic protocells.

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