Towards an evolutionary theory of the origin of life based on kinetics and thermodynamics

Abstract

A sudden transition in a system from an inanimate state to the living state-defined on the basis of present day living organisms-would constitute a highly unlikely event hardly predictable from physical laws. From this uncontroversial idea, a self-consistent representation of the origin of life process is built up, which is based on the possibility of a series of intermediate stages. This approach requires a particular kind of stability for these stages-dynamic kinetic stability (DKS)-which is not usually observed in regular chemistry, and which is reflected in the persistence of entities capable of self-reproduction. The necessary connection of this kinetic behaviour with far-from-equilibrium thermodynamic conditions is emphasized and this leads to an evolutionary view for the origin of life in which multiplying entities must be associated with the dissipation of free energy. Any kind of entity involved in this process has to pay the energetic cost of irreversibility, but, by doing so, the contingent emergence of new functions is made feasible. The consequences of these views on the studies of processes by which life can emerge are inferred.

Keywords: abiogenesis; dynamic kinetic stability; irreversibility; metabolism; origin of life; systems chemistry.

Scheme 1.

The emergence of life considered as a transition to a highly improbable system. (a) Abrupt transition induced by a highly improbable random event in contradiction with the 2nd Law; (b) Stepwise process in which intermediate steps (there is in principle no limitation to the number of steps) allow further evolution towards greater degrees of organization on the basis of entities that are capable of reproducing themselves and, therefore, that exhibit a significant persistence before reverting to the unorganized state (right arrow). The choice of a logarithmic scale of improbability for characterizing ‘aliveness’ as the ordinate is purely arbitrary, but in line with the characterization of the emergence of life as an event of low probability.

Scheme 2.

Close to equilibrium, the kinetics of replicator growth levels off and the composition is ruled by the equilibrium constant K. As both the forward and reverse reactions are dependent on the concentration of the replicating entity, it can be neglected at equilibrium, meaning that close to equilibrium a replicating system does not behave differently to regular chemical systems. In the exponential growth domain, however, the reverse reaction remains negligible, the irreversibility condition is fulfilled and replication growth becomes unsustainable so that the process is usually limited by the availability of resources.

Scheme 3.

Representation of catalytic cycles (a) the usual representation of enzymatic catalysis; (b) any reaction cycle with an increased size also gives rise to catalysis with respect to the conversion of substrate S into product P; (c) a simple example of autocatalysis; (d) autocatalysis can for instance result from the generation of a component (Mⁿ) of a catalytic cycle from a downstream process.

Scheme 4.

Driving a catalytic cycle (R, reactant; C, catalyst; I, intermediate; M, downstream metabolite) to proceed unidirectionally by coupling with an energy source. Irreversibility requires the waste of an amount of free energy corresponding to the kinetic barrier of the reverse reaction (ΔG^≠). A significant part of the free energy (typically an amount of ca 100 kJ mol^–1 at 300 K for systems with time scales of seconds to years [42,43]) is dissipated so that the loop proceeds unidirectionally, provided that subsequent kinetic barriers remain below that of the activation process. Useful chemical work can be produced from further reactions of intermediate I through its conversion into metabolites (M) but in limited amount (≤ΔG(I)) compared with the free energy introduced in the system.

Scheme 5.

Free energy source requirements in living systems (inspired from the figure introduced by Lineweaver & Chopra [45] with a different perspective). Comparison of different sources of energy available in planetary environments: electromagnetic radiations (correspondence with frequency and wavelength in abscissa), thermal energy (black body radiation curves displaying spectral radiance in ordinate: at 647 K, the critical point of water, blue line; 1600 K, representing typical Hadean magma temperatures red line; and 3500 or 6000 K, dark and light orange lines, surface temperatures of examples of M-stars or G-stars as the Sun, respectively) and lightning (T ≥10⁴ K). A much higher potential (ca 150 kJ mol^–1 [42,43]) than the free energy potential of usual biochemicals (green rectangle 30–70 kJ mol^–1, including ATP) was required to trigger the self-organization of life after taking into account the cost of irreversibility (yellow arrows). Photochemistry induced by UV or visible light (emitted by many stars including a significant part of highly abundant M-stars) complies with the requirement as well as lightning. At higher stages of evolution of life on Earth, the development of metabolic engines allowed the concentration of free energy from less potent transmembrane potentials through chemiosmosis [46]. The development of membrane bioenergetics thanks to rotary ATP synthases and of membranes impermeable to ions made the colonization of new environments possible as well as the use of new energy sources through the exploitation of pH gradients [47]. Overall, these molecular motors operating as energy concentration engines allowed the use of free energy potential of ca 15–20 kJ mol^–1 to drive cell metabolism instead of the almost 10-fold higher potential required to drive early self-organization. By contrast, thermal energy in hydrothermal systems with temperature close to the critical point of water (647 K) fails to comply with the irreversibility requirement for the origin of life.