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Genome Biology and Evolution Advance Access published online on April 30, 2009

Genome Biology and Evolution, doi:10.1093/gbe/evp002
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© 2009 The Authors
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abundant indispensable redundancies in cellular metabolic networks

Zhi Wang and Jianzhi Zhang*

Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, 48109, USA

* Correspondence to: Jianzhi Zhang, Department of Ecology and Evolutionary Biology, University of Michigan, 1075 Natural Science Building, 830 North University Avenue, Ann Arbor, MI 48109, Phone: 734-763-0527, Fax: 734-763-0544, Email: jianzhi{at}umich.edu


   Abstract

Cellular life is a highly redundant complex system, yet the evolutionary maintenance of the redundancy remains unexplained. Using a systems biology approach, we infer that 37-47% of metabolic reactions in E. coli and yeast can be individually removed without blocking the production of any biomass component under any nutritional condition. However, the majority of these redundant reactions are preserved, because they have differential maximal efficiencies at different conditions or their loss causes an immediate fitness reduction that can only be regained via mutation, drift, and selection in evolution. The remaining redundancies are attributable to pleiotropic effects or recent horizontal gene transfers. We find that E. coli and yeast exhibit opposite relationships between the functional importance and redundancy level of a reaction, which is inconsistent with the conjecture that redundancies are preserved as an adaptation to backup important parts in the system. Interestingly, the opposite relationships can both be recapitulated by a simple model in which the natural environments of the organisms change frequently. Thus, adaptive backup is neither necessary nor sufficient to explain the high redundancy of cellular metabolic networks. Taken together, our results strongly suggest that redundant reactions are not kept as backups and that the genetic robustness of metabolic networks is an evolutionary byproduct.

Received January 15, 2009; Revised March 13, 2009; Accepted March 19, 2009


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