The origin of replicators and reproducers

Abstract

Replicators are fundamental to the origin of life and evolvability. Their survival depends on the accuracy of replication and the efficiency of growth relative to spontaneous decay. Infrabiological systems are built of two coupled autocatalytic systems, in contrast to minimal living systems that must comprise at least a metabolic subsystem, a hereditary subsystem and a boundary, serving respective functions. Some scenarios prefer to unite all these functions into one primordial system, as illustrated in the lipid world scenario, which is considered as a didactic example in detail. Experimentally produced chemical replicators grow parabolically owing to product inhibition. A selection consequence is survival of everybody. The chromatographized replicator model predicts that such replicators spreading on surfaces can be selected for higher replication rate because double strands are washed away slower than single strands from the surface. Analysis of real ribozymes suggests that the error threshold of replication is less severe by about one order of magnitude than thought previously. Surface-bound dynamics is predicted to play a crucial role also for exponential replicators: unlinked genes belonging to the same genome do not displace each other by competition, and efficient and accurate replicases can spread. The most efficient form of such useful population structure is encapsulation by reproducing vesicles. The stochastic corrector model shows how such a bag of genes can survive, and what the role of chromosome formation and intragenic recombination could be. Prebiotic and early evolution cannot be understood without the models of dynamics.

Figure 1

The autocatalytic core or seed of the formose reaction (Fernando et al. 2005). Each circle represents a chemical group including one carbon atom.

Figure 2

Elementary combinatorics of infrabiological systems (Fernando et al. 2005). The chemoton is a biological minimal system comprising three qualitatively different subsystems (metabolism, membrane and template).

Figure 3

The graded autocatalytic replication domain or composome model: catalysed micelle growth and fission (Segré et al. 2001a,b). L_i and L_j molecules are different amphiphilic compounds, k_i and k_−i are rate constants for spontaneous insertion and emigration of amphiphile L_i, and β_ij is the rate enhancement of getting in and out of this molecule from the micelle, catalysed by L_j. Note that the model does not deal with the primary origin of L_i molecules per se.

Figure 4

Stoichiometric scheme of the simplified system with differential decay rates for the double and single strands (von Kiedrowski & Szathma´ry 2000). The resource R is fed into the system at a constant rate ρ. The assumption d≫δ corresponds to that of the more complicated case when the double strand is retained much more strongly than the single strand by the chromatography column.

Figure 5

Secondary structures of (a) Neurospora VS ribozyme and (b) hairpin ribozyme indicating different regions (Kun et al. 2005a,b). Position numbering follows standard convention. Capitalized nucleotides specify those sites that have been subjected to mutagenesis experiments, and enzymatic activities of mutants are available. A total of 183 mutants for the VS ribozyme affecting 83 out of 144 positions, excluding insertions and deletions, were considered. For the hairpin ribozyme, the survey was based on 142 mutants affecting 39 out of 50 positions of the ribozyme and some part of the substrate region. Nucleotides marked in bold are the critical sites.

Figure 6

The hypercycle with translation. R_i is a replicase protein enzyme coded for by gene I_i.

Figure 7

The stochastic corrector model. Different templates (labelled by open and closed circles) contribute to the well being of the compartments (protocells) in that they catalyse steps of metabolism, for example. During protocell growth, templates replicate at differential expected rates stochastically. Upon division, there is chance assortment of templates into offspring compartments. Stochastic replication and reassortment generate variation among protocells on which natural selection at the compartment level can act and oppose to (correct) internal deterioration owing to within-cell competition.