Lack of evolvability in self-sustaining autocatalytic networks constraints metabolism-first scenarios for the origin of life

Abstract

A basic property of life is its capacity to experience Darwinian evolution. The replicator concept is at the core of genetics-first theories of the origin of life, which suggest that self-replicating oligonucleotides or their similar ancestors may have been the first "living" systems and may have led to the evolution of an RNA world. But problems with the nonenzymatic synthesis of biopolymers and the origin of template replication have spurred the alternative metabolism-first scenario, where self-reproducing and evolving proto-metabolic networks are assumed to have predated self-replicating genes. Recent theoretical work shows that "compositional genomes" (i.e., the counts of different molecular species in an assembly) are able to propagate compositional information and can provide a setup on which natural selection acts. Accordingly, if we stick to the notion of replicator as an entity that passes on its structure largely intact in successive replications, those macromolecular aggregates could be dubbed "ensemble replicators" (composomes) and quite different from the more familiar genes and memes. In sharp contrast with templatedependent replication dynamics, we demonstrate here that replication of compositional information is so inaccurate that fitter compositional genomes cannot be maintained by selection and, therefore, the system lacks evolvability (i.e., it cannot substantially depart from the asymptotic steady-state solution already built-in in the dynamical equations). We conclude that this fundamental limitation of ensemble replicators cautions against metabolismfirst theories of the origin of life, although ancient metabolic systems could have provided a stable habitat within which polymer replicators later evolved.autocatalysis | graded autocatalysis replication domain model | units of evolution O nce beyond the abiogenic synthesis and accumulation of a variety of complex organic compounds on Earth took place (1), the conceivable paths toward life's emergence have been dominated by two fundamentally different views in origin-of-life research: the genetics-or replication-first approach (2), and the metabolism-first scenario (3). Both schools acknowledge that a critical requirement for primitive evolvable systems (in the Darwinian sense) is to solve the problems of information storage and reliable information transmission (4, 5). Disagreement starts, however, in the way information was first stored. All present life is based on digitally encoded information in polynucleotide strings, but difficulties with the de novo appearance of oligonucleotides and clear-cut routes to an RNA world (but see ref. 6), wherein RNA molecules had the dual role of catalysts and information storage systems (7,8), have provided continuous fuel for objections to the genetics-first scenario (9, 10).As emphasized by Kauffman (11), metabolism-first theories suggest that life, in a deep sense, crystallized as a collective selfreproducing metabolism in a space of possible organic reactions. A critical property of such systems must ...

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