Abstract
Complex networks have been successfully employed to represent different levels of biological systems, ranging from gene regulation to protein–protein interactions and metabolism. Network-based research has mainly focused on identifying unifying structural properties, such as small average path length, large clustering coefficient, heavy-tail degree distribution and hierarchical organization, viewed as requirements for efficient and robust system architectures. However, for biological networks, it is unclear to what extent these properties reflect the evolutionary history of the represented systems. Here, we show that the salient structural properties of six metabolic networks from all kingdoms of life may be inherently related to the evolution and functional organization of metabolism by employing network randomization under mass balance constraints. Contrary to the results from the common Markov-chain switching algorithm, our findings suggest the evolutionary importance of the small-world hypothesis as a fundamental design principle of complex networks. The approach may help us to determine the biologically meaningful properties that result from evolutionary pressure imposed on metabolism, such as the global impact of local reaction knockouts. Moreover, the approach can be applied to test to what extent novel structural properties can be used to draw biologically meaningful hypothesis or predictions from structure alone.
Highlights
The central findings in network-based research suggest that there exist simple mechanisms directing the evolution of both engineered and natural networks [1 – 10]
To identify the properties that originate from evolutionary pressure, a network should be compared with random networks that evolved free of evolutionary pressure, but persistently satisfy all relevant physical constraints
We proposed a novel method to reveal the relation between network properties and their evolutionary background by preserving the universal physical principles that constrain the design of metabolic networks
Summary
The central findings in network-based research suggest that there exist simple mechanisms directing the evolution of both engineered and natural networks [1 – 10]. The relation between the functions of a biological system and its network properties is hardly understood. Properties of biological systems arise from two fundamental origins: physical principles, universally constraining the feasibility of biochemical processes, and evolutionary pressure, bearing the specific functional abilities required for an organism’s vitality [12]. The former comprise well-understood physical laws, such as mass balance and thermodynamics, which constitute the basic requirements imposed on all living systems.
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