Abstract
A high level of robustness against gene deletion is observed in many organisms. However, it is still not clear which biochemical features underline this robustness and how these are acquired during evolution. One hypothesis, specific to metabolic networks, is that robustness emerges as a byproduct of selection for biomass production in different environments. To test this hypothesis we performed evolutionary simulations of metabolic networks under stable and fluctuating environments. We find that networks evolved under the latter scenario can better tolerate single gene deletion in specific environments. Such robustness is underlined by an increased number of independent fluxes and multifunctional enzymes in the evolved networks. Observed robustness in networks evolved under fluctuating environments was “apparent,” in the sense that it decreased significantly as we tested effects of gene deletions under all environments experienced during evolution. Furthermore, when we continued evolution of these networks under a stable environment, we found that any robustness they had acquired was completely lost. These findings provide evidence that evolution under fluctuating environments can account for the observed robustness in metabolic networks. Further, they suggest that organisms living under stable environments should display lower robustness in their metabolic networks, and that robustness should decrease upon switching to more stable environments.
Highlights
High-throughput single gene deletion studies in several organisms revealed that a large fraction of genes have little or no detectable fitness effects when compromised [1,2,3,4,5]
Using mathematical models capturing the structure and dynamics of metabolic networks, we simulate their evolution under stable and fluctuating environments. We find that the latter scenario leads to evolution of metabolic networks that display high robustness against gene loss
This robustness of in silico evolved networks is underlined by an increased number of multifunctional enzymes and independent paths leading from initial metabolites to biomass
Summary
High-throughput single gene deletion studies in several organisms revealed that a large fraction of genes have little or no detectable fitness effects when compromised [1,2,3,4,5]. These observations raise the question of how biological systems can acquire and maintain such robustness against gene loss. As for any biological trait, robustness could be adaptive, resulting from direct selection for it, or non-adaptive, resulting as a byproduct of other selective pressures [6]. Robustness against small mutations is shown to evolve in gene regulatory networks selected for dynamic stability [19,20] and robustness against gene deletions is shown to evolve in signaling networks under parasite interference [21]
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