Generating minimal living systems from non-living materials and increasing their evolutionary abilities

Abstract

We review lessons learned about evolutionary transitions from a bottom-up construction of minimal life. We use a particular systemic protocell design process as a starting point for exploring two fundamental questions: (i) how may minimal living systems emerge from non-living materials? and (ii) how may minimal living systems support increasingly more evolutionary richness? Under (i), we present what has been accomplished so far and discuss the remaining open challenges and their possible solutions. Under (ii), we present a design principle we have used successfully both for our computational and experimental protocellular investigations, and we conjecture how this design principle can be extended for enhancing the evolutionary potential for a wide range of systems.This article is part of the themed issue 'The major synthetic evolutionary transitions'.

Keywords: minimal life; open-ended evolution; origins of life; protocells; self-assembly; self-organization.

Figure 1.

(inner triangle) A system of three interconnected components, a container that connects a metabolism and an informational system, which in a given environment, can transform resources into building blocks, grow, divide and undergo evolution (outer circle). Detailed discussions follow in §§2 and 3.

Figure 2.

Obtaining organizational and functional closure is a key issue to construct a protocell bottom up. Resources and free energy are provided from the right side and are part of the environment. The free energy is used to process or ‘digest’ the resources and turn them into building blocks (dG > 0), which defines the primitive metabolism. The metabolism can be light-driven or fuelled by chemical redox energy. One set of building blocks self-assemble into a container (dG < 0), which, for example, can be a vesicle or a droplet. Another set of the building blocks is used to construct new informational molecules. One function of the container is to keep the metabolism and the informational system in close proximity, which is done through self-assembly as the metabolic and informational components, for example, have hydrophobic anchors so they attach to the container (surface of a vesicle) or through container encapsulation (inside a vesicle). The informational system facilitates the chemical production of the building blocks, which means the system increases the metabolic rate kinetics through catalysis. Further, the information complex can make copies of itself from the building blocks produced in the metabolic process, such that catalytic capabilities can be inherited from one generation to the next.

Figure 3.

Metabolism at the centre of the protocell design. (a) Production of amphiphiles. (b) Ligation of the DNA between a 3′-phosphoimidazole phosphate and a 5′-picolyl protected 5′-amino oligomers. Step I: in both cases, the photocleavage of a picolyl group by the ruthenium complex [box: 8-oxoG-Ru(bpy)₃ complex] delivers the protocell building blocks. In (b), two subsequent steps take place: steps II: decarboxylation and III: formation of the phophorimidate bond. (c) Scheme of the photochemistry. Upon irradiation, a Ru MLCT is formed that alone cannot perform the photoclevage. Upon transfer of an electron from the information molecule (8-oxoG), a functional reductant is formed that converts the amphiphile precursor (pL) into an amphiphile (L⁻). A sacrificial H-atom donor is used to regenerate the 8-oxoG and scavenge the radical. (d) Impact of the information-photocatalyst on the conversion rates. Red and black, 8-oxoG-Ru(bpy)₃ with a hydrocarbon moiety and without it (aqueous complex), respectively. In blue, the catalysis by a guanine Ru complex. All samples were the same except for the catalyst. For more details and references, see text.

Figure 4.

Overview of the implementation of our experimental systems together with envisioned systems integration. Enumerated subsystems 1–5 are implemented and published. The open challenges for implementing subsystem 6 are explored in the following §3. A more thorough discussion of minimal life together with different kinds of evolution is presented in §4.

Figure 5.

Template-directed ligation and product inhibition replication where X and O denote the template strand and oligomers, respectively.

Figure 6.

Effective overall replication rate constant k as a function of strand length and temperature. In (a), the template-directed replication mechanism is subjected to product inhibition and slow (i.e. rate-limiting) ligation reaction (see Eq. (3.11)) [36]. In (b), the replication mechanism is also subjected to product inhibition but exposed to a fast (i.e. not rate-limiting) ligation reaction (see Eq. (3.12)] [42].

Figure 7.

Connection between the details included in the simulations and the ability of the simulations to generate targeted observables. Left side of table summarizes the included physical model (each row). Right side of table indicates the higher order observable phenomena/functionalities generated by the simulation. Top of table depicts the qualitative information details needed in a molecular model representation (the data structure) of the simulation (columns). Simulations with more detailed and thus complex molecular components are able to generate increasingly more complex dynamics and functionalities. As an example, data structure D₃ has included enough molecular interaction details to allow the simulation to generate molecular self-assembly and, for example, micellar and vesicle formation. The last row is left open as we conjecture that to obtain a higher evolutionary potential we need to add more components and resources to the system. More detailed discussion in §4a,b.

Figure 8.

For a fixed environment an increased environmental richness through more available building blocks and energy sources will eventually be necessary to open up for more evolutionary possibilities. We conjecture that increasing environmental richness is a necessary condition for eventually obtaining open-ended evolution.