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Historical contingency and the gradual evolution of metabolic properties in central carbon and genome-scale metabolisms


Barve, Aditya; Hosseini, Sayed-Rzgar; Martin, Olivier C; Wagner, Andreas (2014). Historical contingency and the gradual evolution of metabolic properties in central carbon and genome-scale metabolisms. BMC Systems Biology, 8:48.

Abstract

BACKGROUND A metabolism can evolve through changes in its biochemical reactions that are caused by processes such as horizontal gene transfer and gene deletion. While such changes need to preserve an organism's viability in its environment, they can modify other important properties, such as a metabolism's maximal biomass synthesis rate and its robustness to genetic and environmental change. Whether such properties can be modulated in evolution depends on whether all or most viable metabolisms - those that can synthesize all essential biomass precursors - are connected in a space of all possible metabolisms. Connectedness means that any two viable metabolisms can be converted into one another through a sequence of single reaction changes that leave viability intact. If the set of viable metabolisms is disconnected and highly fragmented, then historical contingency becomes important and restricts the alteration of metabolic properties, as well as the number of novel metabolic phenotypes accessible in evolution. RESULTS We here computationally explore two vast spaces of possible metabolisms to ask whether viable metabolisms are connected. We find that for all but the simplest metabolisms, most viable metabolisms can be transformed into one another by single viability-preserving reaction changes. Where this is not the case, alternative essential metabolic pathways consisting of multiple reactions are responsible, but such pathways are not common. CONCLUSIONS Metabolism is thus highly evolvable, in the sense that its properties could be fine-tuned by successively altering individual reactions. Historical contingency does not strongly restrict the origin of novel metabolic phenotypes.

BACKGROUND A metabolism can evolve through changes in its biochemical reactions that are caused by processes such as horizontal gene transfer and gene deletion. While such changes need to preserve an organism's viability in its environment, they can modify other important properties, such as a metabolism's maximal biomass synthesis rate and its robustness to genetic and environmental change. Whether such properties can be modulated in evolution depends on whether all or most viable metabolisms - those that can synthesize all essential biomass precursors - are connected in a space of all possible metabolisms. Connectedness means that any two viable metabolisms can be converted into one another through a sequence of single reaction changes that leave viability intact. If the set of viable metabolisms is disconnected and highly fragmented, then historical contingency becomes important and restricts the alteration of metabolic properties, as well as the number of novel metabolic phenotypes accessible in evolution. RESULTS We here computationally explore two vast spaces of possible metabolisms to ask whether viable metabolisms are connected. We find that for all but the simplest metabolisms, most viable metabolisms can be transformed into one another by single viability-preserving reaction changes. Where this is not the case, alternative essential metabolic pathways consisting of multiple reactions are responsible, but such pathways are not common. CONCLUSIONS Metabolism is thus highly evolvable, in the sense that its properties could be fine-tuned by successively altering individual reactions. Historical contingency does not strongly restrict the origin of novel metabolic phenotypes.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
Dewey Decimal Classification:570 Life sciences; biology
590 Animals (Zoology)
Language:English
Date:23 April 2014
Deposited On:05 Feb 2015 12:29
Last Modified:31 Oct 2016 08:21
Publisher:BioMed Central
ISSN:1752-0509
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1186/1752-0509-8-48
PubMed ID:24758311
Permanent URL: https://doi.org/10.5167/uzh-107386

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