Protometabolism as out-of-equilibrium chemistry

Abstract

It is common to compare life with machines. Both consume fuel and release waste to run. In biology, the engine that drives the living system is referred to as metabolism. However, attempts at deciphering the origins of metabolism do not focus on this energetic relationship that sustains life but rather concentrate on nonenzymatic reactions that produce all the intermediates of an extant metabolic pathway. Such an approach is akin to studying the molecules produced from the burning of coal instead of deciphering how the released energy drives the movement of pistons and ultimately the train when investigating the mechanisms behind locomotion. Theories that do explicitly invoke geological chemical gradients to drive metabolism most frequently feature hydrothermal vent conditions, but hydrothermal vents are not the only regions of the early Earth that could have provided the fuel necessary to sustain the Earth's first (proto)cells. Here, we give examples of prior reports on protometabolism and highlight how more recent investigations of out-of-equilibrium systems may point to alternative scenarios more consistent with the majority of prebiotic chemistry data accumulated thus far. This article is part of the theme issue 'Emergent phenomena in complex physical and socio-technical systems: from cells to societies'.

Keywords: dissipative systems; origins of life; out-of-equilibrium; prebiotic chemistry; protometabolism.

Figure 1.

Extant metabolism works, in part, by funnelling the energy released from the oxidative degradation of varied fuel sources into common currencies, which are then used to drive the energetically costly reductive synthetic processes needed to sustain the cell.

Figure 2.

Comparing timelines of early life innovations. (a) A generic representation of hydrothermal vent scenarios where a constant influx of energy and matter through porous rock sustains prebiotic analogues of metabolism. Over time, the system evolves, generating biopolymers and other molecular machinery before an escape event that leads to encapsulation within a lipid vesicle. (b) A generic representation of the surface of the early Earth where building blocks assemble preferentially within lipid vesicles. This spatial isolation imposes a selective pressure that gives rise to protocells supported by an internal chemistry. (Online version in colour.)

Figure 3.

Living systems use metabolism to exploit the free energy released from the degradation of fuel to maintain their out-of-equilibrium state. As life is a chemical unit capable of catalysing the degradation of fuel and is capable of proliferation, a feedback loop is established between the fuel containing environment and the living organism. (Online version in colour.)

Figure 4.

Self-assembly pulls systems out-of-equilibrium. (a) Autocatalysis. Building blocks (1), e.g. thiol containing peptides, react with a fuel molecule or oxidant (2) to form a dynamic combinatorial library (3). One molecular member of the library can self-assemble (4), thus pulling the system out-of-equilibrium. The self-assembled state (4) itself, or after mechanical breakage, can catalyse the formation of more of the self-assembled state. Further, new properties of the self-assembled state, either intrinsically or by uptake of cofactors from the environment, may emerge which facilitate the productive consumption of building blocks (5). (b) Differential formation and degradation pathways. A mixture of soluble building blocks (1), e.g. fatty acids, react with fuel molecules (2), such as a carbodiimide, to generate products of decreased solubility (3) that can be degraded back to the building block through hydrolysis. The self-assembly of a subset of products (4) inhibits the back reaction, thereby pulling the system away from equilibrium and sustaining an assembly of unstable molecules over time. (Online version in colour.)