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Environmental versatility promotes modularity in genome-scale metabolic networks

BACKGROUND: The ubiquity of modules in biological networks may result from an evolutionary benefit of a modular organization. For instance, modularity may increase the rate of adaptive evolution, because modules can be easily combined into new arrangements that may benefit their carrier. Conversely,...

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Autores principales: Samal, Areejit, Wagner, Andreas, Martin, Olivier C
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3184077/
https://www.ncbi.nlm.nih.gov/pubmed/21864340
http://dx.doi.org/10.1186/1752-0509-5-135
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author Samal, Areejit
Wagner, Andreas
Martin, Olivier C
author_facet Samal, Areejit
Wagner, Andreas
Martin, Olivier C
author_sort Samal, Areejit
collection PubMed
description BACKGROUND: The ubiquity of modules in biological networks may result from an evolutionary benefit of a modular organization. For instance, modularity may increase the rate of adaptive evolution, because modules can be easily combined into new arrangements that may benefit their carrier. Conversely, modularity may emerge as a by-product of some trait. We here ask whether this last scenario may play a role in genome-scale metabolic networks that need to sustain life in one or more chemical environments. For such networks, we define a network module as a maximal set of reactions that are fully coupled, i.e., whose fluxes can only vary in fixed proportions. This definition overcomes limitations of purely graph based analyses of metabolism by exploiting the functional links between reactions. We call a metabolic network viable in a given chemical environment if it can synthesize all of an organism's biomass compounds from nutrients in this environment. An organism's metabolism is highly versatile if it can sustain life in many different chemical environments. We here ask whether versatility affects the modularity of metabolic networks. RESULTS: Using recently developed techniques to randomly sample large numbers of viable metabolic networks from a vast space of metabolic networks, we use flux balance analysis to study in silico metabolic networks that differ in their versatility. We find that highly versatile networks are also highly modular. They contain more modules and more reactions that are organized into modules. Most or all reactions in a module are associated with the same biochemical pathways. Modules that arise in highly versatile networks generally involve reactions that process nutrients or closely related chemicals. We also observe that the metabolism of E. coli is significantly more modular than even our most versatile networks. CONCLUSIONS: Our work shows that modularity in metabolic networks can be a by-product of functional constraints, e.g., the need to sustain life in multiple environments. This organizational principle is insensitive to the environments we consider and to the number of reactions in a metabolic network. Because we observe this principle not just in one or few biological networks, but in large random samples of networks, we propose that it may be a generic principle of metabolic network organization.
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spelling pubmed-31840772011-10-03 Environmental versatility promotes modularity in genome-scale metabolic networks Samal, Areejit Wagner, Andreas Martin, Olivier C BMC Syst Biol Research Article BACKGROUND: The ubiquity of modules in biological networks may result from an evolutionary benefit of a modular organization. For instance, modularity may increase the rate of adaptive evolution, because modules can be easily combined into new arrangements that may benefit their carrier. Conversely, modularity may emerge as a by-product of some trait. We here ask whether this last scenario may play a role in genome-scale metabolic networks that need to sustain life in one or more chemical environments. For such networks, we define a network module as a maximal set of reactions that are fully coupled, i.e., whose fluxes can only vary in fixed proportions. This definition overcomes limitations of purely graph based analyses of metabolism by exploiting the functional links between reactions. We call a metabolic network viable in a given chemical environment if it can synthesize all of an organism's biomass compounds from nutrients in this environment. An organism's metabolism is highly versatile if it can sustain life in many different chemical environments. We here ask whether versatility affects the modularity of metabolic networks. RESULTS: Using recently developed techniques to randomly sample large numbers of viable metabolic networks from a vast space of metabolic networks, we use flux balance analysis to study in silico metabolic networks that differ in their versatility. We find that highly versatile networks are also highly modular. They contain more modules and more reactions that are organized into modules. Most or all reactions in a module are associated with the same biochemical pathways. Modules that arise in highly versatile networks generally involve reactions that process nutrients or closely related chemicals. We also observe that the metabolism of E. coli is significantly more modular than even our most versatile networks. CONCLUSIONS: Our work shows that modularity in metabolic networks can be a by-product of functional constraints, e.g., the need to sustain life in multiple environments. This organizational principle is insensitive to the environments we consider and to the number of reactions in a metabolic network. Because we observe this principle not just in one or few biological networks, but in large random samples of networks, we propose that it may be a generic principle of metabolic network organization. BioMed Central 2011-08-24 /pmc/articles/PMC3184077/ /pubmed/21864340 http://dx.doi.org/10.1186/1752-0509-5-135 Text en Copyright ©2011 Samal et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Samal, Areejit
Wagner, Andreas
Martin, Olivier C
Environmental versatility promotes modularity in genome-scale metabolic networks
title Environmental versatility promotes modularity in genome-scale metabolic networks
title_full Environmental versatility promotes modularity in genome-scale metabolic networks
title_fullStr Environmental versatility promotes modularity in genome-scale metabolic networks
title_full_unstemmed Environmental versatility promotes modularity in genome-scale metabolic networks
title_short Environmental versatility promotes modularity in genome-scale metabolic networks
title_sort environmental versatility promotes modularity in genome-scale metabolic networks
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3184077/
https://www.ncbi.nlm.nih.gov/pubmed/21864340
http://dx.doi.org/10.1186/1752-0509-5-135
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