The origin of a primordial genome through spontaneous symmetry breaking

Nobuto Takeuchi,Paulien Hogeweg,Kunihiko Kaneko

doi:10.1038/s41467-017-00243-x

Nobuto Takeuchi, Paulien Hogeweg + Show 1 more

Open Access

https://doi.org/10.1038/s41467-017-00243-x

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Abstract

The heredity of a cell is provided by a small number of non-catalytic templates—the genome. How did genomes originate? Here, we demonstrate the possibility that genome-like molecules arise from symmetry breaking between complementary strands of self-replicating molecules. Our model assumes a population of protocells, each containing a population of self-replicating catalytic molecules. The protocells evolve towards maximising the catalytic activities of the molecules to increase their growth rates. Conversely, the molecules evolve towards minimising their catalytic activities to increase their intracellular relative fitness. These conflicting tendencies induce the symmetry breaking, whereby one strand of the molecules remains catalytic and increases its copy number (enzyme-like molecules), whereas the other becomes non-catalytic and decreases its copy number (genome-like molecules). This asymmetry increases the equilibrium cellular fitness by decreasing mutation pressure and increasing intracellular genetic drift. These results implicate conflicting multilevel evolution as a key cause of the origin of genetic complexity.

Highlights

The heredity of a cell is provided by a small number of non-catalytic templates—the genome
First of all, is the resemblance between such genome-like molecules and the genome as we know it more than purely formal? In other words, do such genome-like molecules have any special quality related to heredity, besides having the two features of a genome mentioned above? Second, what evolutionary mechanism can account for the postulated functional asymmetry? This mechanism has to allow for the fact that both complementary strands could in principle have catalytic activity[4]
Functional and kinetic asymmetry between complementary strands has been suggested as the first, primordial form of differentiation between templates and catalysts in an RNA world[1]

Summary

Introduction

The heredity of a cell is provided by a small number of non-catalytic templates—the genome. The RNA world hypothesis posits that the heredity of the first, primitive cell (protocell, for short) was provided by a population of dualfunctional molecules serving as both templates and catalysts This hypothesis raises a question: how did ‘non-catalytic, small-copynumber templates providing information for producing catalysts’ evolve? The first, primordial form of genomes arose from functional asymmetry between complementary strands of replicating molecules, whereby one strand served as both a template and a catalyst, whereas the other served only as a template Because it pays to produce more catalysts than templates, evolution would increase the copy number of the catalytic strand[3], commensurately decreasing that of the non-catalytic strand, the evolution of non-catalytic, small-copy-number templates, i.e., genome-like molecules.

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