Abstract
Theories of the origin of the genetic code typically appeal to natural selection and/or mutation of hereditable traits to explain its regularities and error robustness, yet the present translation system presupposes high-fidelity replication. Woese’s solution to this bootstrapping problem was to assume that code optimization had played a key role in reducing the effect of errors caused by the early translation system. He further conjectured that initially evolution was dominated by horizontal exchange of cellular components among loosely organized protocells (“progenotes”), rather than by vertical transmission of genes. Here we simulated such communal evolution based on horizontal transfer of code fragments, possibly involving pairs of tRNAs and their cognate aminoacyl tRNA synthetases or a precursor tRNA ribozyme capable of catalysing its own aminoacylation, by using an iterated learning model. This is the first model to confirm Woese’s conjecture that regularity, optimality, and (near) universality could have emerged via horizontal interactions alone.
Highlights
Explaining the origins of life remains one of the biggest challenges of science, and one essential aspect of this challenge is to explain the origin of the standard genetic code
This theory sits uneasily with the finding that standard genetic code is not that optimal, at least according to some measures, and that better codes can be found when selected for robustness[3]. This sub-optimality has been interpreted as a combination of adaptation and frozen accident, whereby selection was constrained by initial conditions and subsequently by deleterious consequences of code changes. Another possibility is suggested by the existence of simplified genetic codes[4]: if codes started with few amino acids, optimality could be an emergent consequence of code expansion from early simple ones to the standard genetic code, whereby new amino acids were assigned to codons that had previously encoded chemically similar amino acids[5]
Crick’s frozen accident hypothesis[5] helps to explain universality because all extant species share a last universal common ancestor, and inherited its genetic code. This last universal common ancestor must have already been a highly optimised organism, which leaves us with a circular problem that is somewhat similar to Eigen’s paradox: it is difficult to conceive of the evolutionary origins of its complex translation system before there were a number of functional proteins capable of maintaining the integrity of the system to minimize the translational error along with functional RNAs, but such proteins could not have evolved without a high-fidelity translation system[8]
Summary
Explaining the origins of life remains one of the biggest challenges of science, and one essential aspect of this challenge is to explain the origin of the standard genetic code. Previous computer models have confirmed that adding horizontal gene transfer to the evolution of a population of genetic codes selected for error robustness has the effect of facilitating convergence on optimal and universal codes compared to vertical descent alone[20,21,22].
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