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Evolutionary advantage of directional symmetry breaking in self-replicating polymers

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 Publication date 2017
  fields Biology
and research's language is English




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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, DNAs 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.

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The macromolecules that encode and translate information in living systems, DNA and RNA, exhibit distinctive structural asymmetries, including homochirality or mirror image asymmetry and $3 - 5$ directionality, that are invariant across all life forms. The evolutionary advantages of these broken symmetries remain unknown. Here we utilize a very simple model of hypothetical self-replicating polymers to show that asymmetric autocatalytic polymers are more successful in self-replication compared to their symmetric counterparts in the Darwinian competition for space and common substrates. This broken-symmetry property, called asymmetric cooperativity, arises with the maximization of a replication potential, where the catalytic influence of inter-strand bonds on their left and right neighbors is unequal. Asymmetric cooperativity also leads to tentative, qualitative and simple evolution-based explanations for a number of other properties of DNA that include four nucleotide alphabet, three nucleotide codons, circular genomes, helicity, anti-parallel double-strand orientation, heteromolecular base-pairing, asymmetric base compositions, and palindromic instability, apart from the structural asymmetries mentioned above. Our model results and tentative explanations are consistent with multiple lines of experimental evidence, which include evidence for the presence of asymmetric cooperativity in DNA.
Directed polymers on 1+1 dimensional lattices coupled to a heat bath at temperature $T$ are studied numerically for three ensembles of the site disorder. In particular correlations of the disorder as well as fractal patterning are considered. Configurations are directly sampled in perfect thermal equilibrium for very large system sizes with up to $N=L^2= 32768 times 32768 approx 10^{9}$ sites. The phase-space structure is studied via the distribution of overlaps and hierarchical clustering of configurations. One ensemble shows a simple behavior like a ferromagnet. The other two ensembles exhibit indications for complex behavior reminiscent of multiple replica-symmetry breaking. Also results for the ultrametricity of the phase space and the phase transition behavior of $P(q)$ when varying the temperature $T$ are studied. In total, the present model ensembles offer convenient numerical accesses to comprehensively studying complex behavior.
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