Chemical roots of biological evolution: the origins of life as a process of development of autonomous functional systems

Abstract

In recent years, an extension of the Darwinian framework is being considered for the study of prebiotic chemical evolution, shifting the attention from homogeneous populations of naked molecular species to populations of heterogeneous, compartmentalized and functionally integrated assemblies of molecules. Several implications of this shift of perspective are analysed in this critical review, both in terms of the individual units, which require an adequate characterization as self-maintaining systems with an internal organization, and also in relation to their collective and long-term evolutionary dynamics, based on competition, collaboration and selection processes among those complex individuals. On these lines, a concrete proposal for the set of molecular control mechanisms that must be coupled to bring about autonomous functional systems, at the interface between chemistry and biology, is provided.

Keywords: autonomous functional systems; chemical evolution; natural selection; origins of life; prebiotic systems chemistry.

Figure 1.

Scheme of the different stages and bottlenecks that could have occurred during the transition from chemical to biological evolution. Among the complex and interacting chemical mixtures present on early Earth, only those that developed the first functional couplings were available for the next step of the overall process. Further diversification of those coupled systems made stronger functional integration mechanisms possible, leading to—at least—one type of system in the population with sufficient dynamic/structural stability to overcome the bottleneck imposed by the need for reliable reproduction (including molecular template mechanisms). This stage corresponded to systems in which compartment, metabolism and replication (CMR) were tightly coupled. In turn, only those CMR systems that became capable of open-ended biological evolution (see explanation in the text) would show the long-term robustness required to follow the pathway to LUCA and its further diversification into the three domains of life.

Figure 2.

Schematic of the minimal set of control mechanisms that should operate, in a highly interdependent manner, to support the development of the first autonomous functional systems in the context of heterogeneous prebiotic chemistries. These mechanisms involve: (i) kinetic control, to coordinate the different reaction processes in time and enable transformations that reinforce the incipient chemistry but would otherwise be kinetically hindered; (ii) spatial control, to establish a clear inside/outside distinction and preserve minimal concentration thresholds of the relevant chemical species; (iii) energetic control, to facilitate the thermodynamically uphill but necessary reactions; and (iv) variability control, for these systems to have a minimal chance to evolve, through NS, into more complex forms. These four types of control mechanisms are represented as the vertices of a tetrahedron (with candidate molecular and supramolecular components suggested in red) and connected to each other by integrative and cooperative chemical couplings (black edges). Individuals with such an irreducible heterogeneity in their composition (and complexity in their dynamic behaviour) would constitute proper candidates as units of selection in this extended framework to conceive prebiotic chemical evolution. As a result of that evolutionary process, one could envision further functional diversification and more efficient integration (through new coupling processes), which would confer higher dynamic robustness to increasingly complex individuals in the population (a stage that is schematically illustrated by the multiple tetrahedron within the initial, elementary one).

Figure 3.

Scheme showing the main evolutionary transitions proposed for prebiotic chemistry and the overall process of origins of life. The notion of protocell populations employed here is remarkably wide, understood as heterogeneous, compartmented and functionally integrated assemblies of molecules that could implement, in successive stages, the different processes, capacities and mechanisms shown at the lower part of the figure.