Evolutionary advantage of directional symmetry breaking in self-replicating polymers

Abstract

Due to the asymmetric nature of the nucleotides, the extant informational biomolecule, DNA, is constrained to replicate unidirectionally on a template. As a product of molecular evolution that sought to maximize replicative potential, DNA's unidirectional replication poses a mystery since symmetric bidirectional self-replicators obviously would replicate faster than unidirectional self-replicators and hence would have been evolutionarily more successful. Here we carefully examine the physico-chemical requirements for evolutionarily successful primordial self-replicators and theoretically show that at low monomer concentrations that possibly prevailed in the primordial oceans, asymmetric unidirectional self-replicators would have an evolutionary advantage over bidirectional self-replicators. The competing requirements of low and high kinetic barriers for formation and long lifetime of inter-strand bonds respectively are simultaneously satisfied through asymmetric kinetic influence of inter-strand bonds, resulting in evolutionarily successful unidirectional self-replicators. Within our model, circular strands, the configuration prefered by primitive life forms, have higher replicative potential compared to linear strands.

Evolutionary advantage of anti-parallel strand orientation of duplex DNA

“…In an earlier article 12 , we showed that maximization of the replicative potential of a generic primordial self-replicating polymer leads to the property of asymmetric cooperativity. We recapitulate the same here for completeness.…”

“…The central concept of this article is asymmetric cooperativity, a new property of self-replicating heteropolymers that we introduced in our earlier article 12 . In that article, we have quantitatively evaluated, using a Marko Chain model, the self-replicative potential of heteropolymers with asymmetric and symmetric cooperativities.…”

“…The current article examines the evolutionary consequences of asymmetric cooperativity to the replicative organization of DNA. We begin below by recapitulating, from our earlier article 12 , what asymmetric cooperativity is and why it is useful for self-replication. In the next "Model and its Premises" section, we decompose asymmetric cooperativity into two parts, namely, sequence-independent and sequence-dependent asymmetric cooperativities, and elaborate on and illustrate them with a number of diagrams.…”

“…Within the premise that DNA is a product of molecular evolution, it would be natural to expect that asymmetric cooperativity is present in DNA as well. In our previous publication 12 , we have suggested an experiment to verify the existence of asymmetric cooperativity in DNA, and cited numerous experiments suggesting its presence in DNA.…”

“…This premise is borne from the observation that DNA daughter strand construction is unidirectional and proceeds from its 5′ end. Illustration of replica strand construction process of a circular autocatalytic polymer in the presence of (a) asymmetric and (b) symmetric nearest-neighbor hydrogen bond cooperativities (reprinted from 12 with permission from Elsevier). The circles represent monomers and the thick vertical lines connecting a pair represent the inter-strand hydrogen bonds.…”