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Constraint and Contingency Pervade the Emergence of Novel Phenotypes in Complex Metabolic Systems


Hosseini, Sayed-Rzgar; Wagner, Andreas (2017). Constraint and Contingency Pervade the Emergence of Novel Phenotypes in Complex Metabolic Systems. Biophysical Journal, 113(3):690-701.

Abstract

An evolutionary constraint is a bias or limitation in phenotypic variation that a biological system produces. We know examples of such constraints, but we have no systematic understanding about their extent and causes for any one biological system. We here study metabolisms, genomically encoded complex networks of enzyme-catalyzed biochemical reactions, and the constraints they experience in bringing forth novel phenotypes that allow survival on novel carbon sources. Our computational approach does not limit us to analyzing constrained variation in any one organism, but allows us to quantify constraints experienced by any metabolism. Specifically, we study metabolisms that are viable on one of 50 different carbon sources, and quantify how readily alterations of their chemical reactions create the ability to survive on a novel carbon source. We find that some metabolic phenotypes are much less likely to originate than others. For example, metabolisms viable on D-glucose are 1835 times more likely to give rise to metabolisms viable on D-fructose than on acetate. Likewise, we observe that some novel metabolic phenotypes are more contingent on parental phenotypes than others. Biochemical similarities among carbon sources can help explain the causes of these constraints. In addition, we study metabolisms that can be produced by recombination among 55 metabolisms of different bacterial strains or species, and show that their novel phenotypes are also contingent on and constrained by parental genotypes. To our knowledge, our analysis is the first to systematically quantify the incidence of constrained evolution in a broad class of biological system that is central to life and its evolution.

Abstract

An evolutionary constraint is a bias or limitation in phenotypic variation that a biological system produces. We know examples of such constraints, but we have no systematic understanding about their extent and causes for any one biological system. We here study metabolisms, genomically encoded complex networks of enzyme-catalyzed biochemical reactions, and the constraints they experience in bringing forth novel phenotypes that allow survival on novel carbon sources. Our computational approach does not limit us to analyzing constrained variation in any one organism, but allows us to quantify constraints experienced by any metabolism. Specifically, we study metabolisms that are viable on one of 50 different carbon sources, and quantify how readily alterations of their chemical reactions create the ability to survive on a novel carbon source. We find that some metabolic phenotypes are much less likely to originate than others. For example, metabolisms viable on D-glucose are 1835 times more likely to give rise to metabolisms viable on D-fructose than on acetate. Likewise, we observe that some novel metabolic phenotypes are more contingent on parental phenotypes than others. Biochemical similarities among carbon sources can help explain the causes of these constraints. In addition, we study metabolisms that can be produced by recombination among 55 metabolisms of different bacterial strains or species, and show that their novel phenotypes are also contingent on and constrained by parental genotypes. To our knowledge, our analysis is the first to systematically quantify the incidence of constrained evolution in a broad class of biological system that is central to life and its evolution.

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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:8 August 2017
Deposited On:01 Mar 2018 10:22
Last Modified:14 Mar 2018 18:03
Publisher:Elsevier
ISSN:0006-3495
OA Status:Closed
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1016/j.bpj.2017.06.034

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