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Abstract
BackgroundThe growth and development of a biological organism is reflected by its metabolic network, the evolution of which relies on the essential gene duplication mechanism. There are two current views about the evolution of metabolic networks. The retrograde model hypothesizes that a pathway evolves by recruiting novel enzymes in a direction opposite to the metabolic flow. The patchwork model is instead based on the assumption that the evolution is based on the exploitation of broad-specificity enzymes capable of catalysing a variety of metabolic reactions.ResultsWe analysed a well-studied unicellular eukaryotic organism, S. cerevisiae, and studied the effect of the removal of paralogous gene products on its metabolic network. Our results, obtained using different paralog and network definitions, show that, after an initial period when gene duplication was indeed instrumental in expanding the metabolic space, the latter reached an equilibrium and subsequent gene duplications were used as a source of more specialized enzymes rather than as a source of novel reactions. We also show that the switch between the two evolutionary strategies in S. cerevisiae can be dated to about 350 million years ago.ConclusionsOur data, obtained through a novel analysis methodology, strongly supports the hypothesis that the patchwork model better explains the more recent evolution of the S. cerevisiae metabolic network. Interestingly, the effects of a patchwork strategy acting before the Euascomycete-Hemiascomycete divergence are still detectable today.
Highlights
The growth and development of a biological organism is reflected by its metabolic network, the evolution of which relies on the essential gene duplication mechanism
The results of the analysis reported here show that the S. cerevisiae metabolic network has evolved in a discontinuous manner: the first growing moves increased the number of metabolites
These pioneering studies interestingly converge on assigning a high likelihood to the patchwork model, they have some limitations: both analyse E. coli, a prokaryotic organism in which the widespread phenomenon of lateral gene transfer, affecting proteins involved in metabolism [42], can compromise the reliability of the homology inference
Summary
The growth and development of a biological organism is reflected by its metabolic network, the evolution of which relies on the essential gene duplication mechanism. There are two current views about the evolution of metabolic networks. The patchwork model is instead based on the assumption that the evolution is based on the exploitation of broad-specificity enzymes capable of catalysing a variety of metabolic reactions. Metabolism defines the reactions that provide energy and constituents for cells and organisms. The modular units of the metabolism are the metabolic pathways, sets of chemical reactions by which a metabolite is transformed into another through a series of steps catalysed by enzymes. The metabolic networks provide a global view of the metabolic pathways of an organism and can be represented in two alternative ways. In enzyme-centric networks, proteins are defined as nodes, connected by the metabolites they process, whilst metabolite-centric
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