The Symbiontic Nature of Metabolic Evolution

Abstract

We discuss evolutionary aspects of metabolism, right from the beginning of life to the present day at various levels of organization, thereby including quantitative aspects on the basis of the Dynamic Energy Budget (DEB) theory. We propose a scheme for the evolution of the central metabolism with archaeal as well as eubacterial roots. After an extended initial phase of prokaryotic diversification, cycles of exchange of metabolites between partners in a symbiosis, integration of partners into new individuals and new specializations led to forms of symbiosis of various intensity ranging from loosely living together in species aggregates to several forms of endosymbiosis. While the prokaryotic metabolism evolved into a considerable chemical diversity, the eukaryotic metabolic design remained qualitatively the same but shows a large organizational diversity. Homeostasis of biomass evolved, introducing stoichiometric constraints on production and excretion of products that can be re-utilized; carbohydrates and inorganic nitrogen being the most important ones. This stimulates the formation of symbioses, since most are based on syntrophy, which is probably the basis of the huge biodiversity. A remarkable property of DEB theory for metabolic organization is that organisms of two species that exchange products, and thereby follow the DEB rules, can together follow a symbiogenic route such that the symbiosis behaves as a new organism that itself follows the DEB rules. This property of the reserve dynamics in the DEB theory also explains a possible evolutionary route to homeostasis. The reserve dynamics in DEB theory also plays a key role in linking the kinetics of metabolic pathways to needs of metabolites at the cellular level. Moreover, reserve kinetics, in combination with other DEB elements, explains how metabolic performance depends on body size and why such relationships work out differently within and between species. Apart from the key role of reserves, the dynamic interaction between surface areas and volumes is a basic feature of the DEB theory at all levels of organization (molecules, individuals, ecosystems). The explicit mass and energy balances of the DEB theory facilitates ecosystem modelling as it depends on nutrient exchange. The theoretical interest in this topic concerns the huge range in space-time scales that is involved in understanding the significance of the actions of life within the context of metabolic organization.