Suitable energetic conditions for dynamic chemical complexity and the living state
© Pascal; licensee Chemistry Central Ltd. 2012
Received: 2 April 2012
Accepted: 3 May 2012
Published: 17 May 2012
Any living organism can be considered as a component of a dissipative process coupling an irreversible consumption of energy to the growth, reproduction and evolution of living things. Close interactions between metabolism and reproduction are thus required, which means that metabolism has two main functions. The first one, which is the most easily perceptible, corresponds to the synthesis of the components of living beings that are not found in the environment (anabolism). The second one, which is usually associated with the former, is the dissipative process coupling the consumption of energy to self-organization and reproduction and introducing irreversibility in the process. Considering the origin of life, the formation of at least some of the building blocks constituting a living organism can be envisaged in a close to equilibrium situation under reducing conditions (for instance in hydrothermal vents). However, coupling irreversibly self-organization with the dissipation of an energy flux implies far from equilibrium conditions that are shown in this work to raise quantitative requirements on the height of kinetic barriers protecting metabolites from a spontaneous evolution into deactivated species through a quantitative relationship with the time scale of the progress of the overall process and the absolute temperature. The thermodynamic potential of physical sources of energy capable of feeding the emergence of this capacity can be inferred, which leads to the identification of photochemistry at the wavelength of visible light or processes capable of generating activated species by heating transiently a chemical environment above several thousand Kelvin as the only processes capable of fulfilling this requirement.
The main features of the living state can be identified even though a comprehensive definition of what is life may be difficult to reach or actually would require an agreement of the scientific community that has not been met yet. It has been proposed that life could be characterized as a kinetic state of matter, in which systems that are capable of reproducing themselves can become persistent and evolve owing to the concept of dynamic kinetic stability[3, 4]. This description provides a rational basis to the attempt to express natural selection as a physical principle stated almost a century ago by Lotka. The chemical processes capable of initiating life have been recognized decades ago through the analyses of Eigen and coworkers[6, 7] as related to the specific behavior of reaction networks behaving as autocatalysts or more generally hypercycles. These systems correspond in fact to reaction cycles involving multiple feedback processes so that the overall system present unique properties. Although it is possible to understand the emergence of life as that of a genetic replicator, and that of the exponential growth needed for these systems to develop[9, 10], a metabolic contribution to this process remains unavoidable since autocatalysis does not result in growth for systems close to equilibrium, which means that the systems requires the availability of energy-rich building blocks that are used up irreversibly. The metabolic features of living systems have been analyzed by Schrödinger as the need of an association with processes generating an increase in entropy to compensate for the local decrease associated with self-organization. The involvement of processes in which a flux of energy (or matter in an activated state) is irreversibly transformed through a dissipative process, producing entropy in the environment in a way that is coupled to a local decrease within the self-organizing system, is then crucial for living organisms. With regard to the origin of life, the formation of an organized system coupling the use of this irreversible energy flux with self-organization must have required the spontaneous decay of chemical species involved in the process to be slow enough so that features of organization can develop. Eschenmoser considered indeed that the complexity of a reaction network involving metabolic cycles or autocatalytic networks associated with the first developments of life must have emerged from systems evolving in a chemical environment held far from equilibrium by kinetic barriers[12–14]. This idea simply means that chemical self-organization cannot emerge when species decay with fast rates toward the equilibrium state. In this essay, this idea is developed in a quantitative way to demonstrate that it can actually lead to valuable conclusions on the thermodynamic potential needed to bring about the living state of matter and on the nature of the corresponding processes. This does not mean that life and evolution can be understood in a deterministic way, but simply that having a probability different from zero for life to emerge requires specific chemical conditions. These requirements must be taken into account when tackling the questions of the origin of living systems on the early Earth or of its possible occurrence on extrasolar planetary systems, but also when considering the evolution of artificial chemical systems based on dynamic kinetic stability[3, 4], which constitutes one of the goals of systems chemistry[15, 16].
The driver process delivering energy and enabling the formation of an activated carrier in the first step of Figure1 may be physical (for instance photochemical and not being subject to microscopic reversibility as proposed in an analysis of autocatalytic models on the emergence of homochirality) or chemical. However, its actual nature does not matter. The condition that the proto-metabolisms must work irreversibly (as a one-way flux of reactants) for coupling self-organization with an entropy producing process implies that this driver process is capable of bringing the system into an excited state with a free energy exceeding the level of the transition state of the reaction reverting the energy carrier into its precursors. As a result, this short-lived activated state either reverts back to the reactants or proceeds downhill in the forward direction until a free energy well is reached yielding a chemical carrier conserving a significant part of the free energy of the source. Irreversibility in the proto-metabolic process thus emerges from the kinetic barrier of a reverse reaction. This discussion helps in identifying processes enabling the formation of the energy carriers. Photochemical processes able to deliver the corresponding amount of energy (ca. 150 kJ mol–1) correspond to wavelength of ca. 0.8 μm meaning that light in the visible spectrum is needed. Few other physical processes are capable of driving such systems in a spontaneous way. Using the black body emission as a typical example of irreversible transformation of thermal energy, heating a solid to 3600 K enables the emission of electromagnetic radiations with a maximum at the wavelength of 0.8 μm. This can be a measurement of the temperature needed for thermal energy to generate activated chemical intermediates, though the system needs a quenching step to preserve the corresponding species from evolving back to equilibrium. The only obvious processes compatible with the effect of heat are lightning, as mimicked in the Miller experiment, and impact-shock syntheses. These processes are capable of heating locally and transiently the atmosphere at temperatures exceeding several thousand of K needed to generate radicals and ions that have enough time to recombine after cooling within a fraction of second at the lower temperature of the high atmosphere. By contrast, finding means by which geothermal energy could directly play a similar role is more problematic.
In principle, having a chemical environment in which species are held far from equilibrium by kinetic barriers may enable certain catalysts to be amplified provided that the reaction network is additionally capable of producing them. These protometabolic cycles involving catalysts that are themselves reproduced by the system are likely to increase the rate of consumption of energy carriers so that they will tend to predominate in the environment–they are selected–, corresponding to the definition of dynamic kinetic stability, which is the main feature of living systems.
In summary, an analysis starting by considering the fate of any single metabolite shows that the lifetime corresponding to the evolution of the whole chemical system (related to that of its major intermediates) and the absolute temperature determine the heights of the free energy barriers required for protecting metabolites with a significant lifetime from a spontaneous breakdown. At moderate temperatures corresponding to that of the surface of the Earth, these barriers represent a significant part of the dissociation energies of simple covalent bonds signifying that scaffolds based on this kind of linkages are the easiest solution to sustain life under these conditions. This analysis establishes that not all forms of energy are capable of sustaining the origin of life and predicts photochemistry or transient heating to temperatures beyond several thousands of Kelvin (by lightning or impacts) as likely sources. Therefore, photochemistry may have been directly involved in the emergence of living organisms or may have been introduced very early in their metabolism long before photosynthesis brought about the possibility of generating both chemical energy under the form of ATP and reducing power used for the biosynthesis of their organics components. As life tend to occupy every ecological niche in which energy is available, further biochemical machineries evolved that use complex mechanisms to extract energy from diluted sources, which may even include syntrophic cooperation of different forms of life that develop different kinds of metabolisms. But, life must have initially be based on much simpler systems so that the requirements defined here introduce new limits for the habitability of the early Earth environments or of extrasolar planets as factors conditioning the origin of life. Chemical principles are thus essential for understanding how life can emerge and introduce independent conditions for habitability that are more strict than those coming from the possibility of the persistence of evolved living beings deduced by analogy to extant life on Earth. The analysis of these principles is also useful in building a theoretical framework for systems chemistry.
The author thanks the interdisciplinary program of the CNRS Planetary Environments and Origins of Life (EPOV) for support and the COST Action CM070 “Systems chemistry” for providing a fruitful context for scientific exchanges during the realization of this work.
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