Abstract
The standard genetic code (SGC) is central to molecular biology and its origin and evolution is a fundamental problem in evolutionary biology, the elucidation of which promises to reveal much about the origins of life. In addition, we propose that study of its origin can also reveal some fundamental and generalizable insights into mechanisms of molecular evolution, utilizing concepts from complexity theory. The first is that beneficial traits may arise by non-adaptive processes, via a process of “neutral emergence”. The structure of the SGC is optimized for the property of error minimization, which reduces the deleterious impact of point mutations. Via simulation, it can be shown that genetic codes with error minimization superior to the SGC can emerge in a neutral fashion simply by a process of genetic code expansion via tRNA and aminoacyl-tRNA synthetase duplication, whereby similar amino acids are added to codons related to that of the parent amino acid. This process of neutral emergence has implications beyond that of the genetic code, as it suggests that not all beneficial traits have arisen by the direct action of natural selection; we term these “pseudaptations”, and discuss a range of potential examples. Secondly, consideration of genetic code deviations (codon reassignments) reveals that these are mostly associated with a reduction in proteome size. This code malleability implies the existence of a proteomic constraint on the genetic code, proportional to the size of the proteome (P), and that its reduction in size leads to an “unfreezing” of the codon – amino acid mapping that defines the genetic code, consistent with Crick’s Frozen Accident theory. The concept of a proteomic constraint may be extended to propose a general informational constraint on genetic fidelity, which may be used to explain variously, differences in mutation rates in genomes with differing proteome sizes, differences in DNA repair capacity and genome GC content between organisms, a selective pressure in the evolution of sexual reproduction, and differences in translational fidelity. Lastly, the utility of the concept of an informational constraint to other diverse fields of research is explored.
Highlights
The standard genetic code (SGC) is central to molecular biology and its origin and evolution is a fundamental problem in evolutionary biology, the elucidation of which promises to reveal much about the origins of life
The arrangement of codons to amino acids in the SGC is such that the deleterious effects of point mutations are minimized, compared to randomly generated codes; this error minimization is a form of mutational robustness
The relative frequency of these are affected by the structure of the genetic code itself, because amino acids encoded by codons that differ by one nucleotide will be substituted more frequently than those that differ by two nucleotides
Summary
Near Optimal and Near Universal “Theory space” has been well covered when it comes to the potential pathways that may have led to the present day standard genetic code (SGC) [1]. While it is largely accepted that the genetic code underwent expansion during its evolution, there is no consensus regarding the specific route that led its development, which may be unknowable [2] The reason why these considerations are important relates to a central concern in biology, that of “genotype—phenotype mapping”. A central problem is that of Crick’s Frozen Accident [26], which asserts that the reason for the widespread distribution of the SGC (only a minority of genomes use deviant genetic codes), is that any changes to the genetic code would be catastrophic to the organism This is because reassigning a codon to a new amino acid effectively involves mutating every single occurrence of that codon in the genome, which is expected to lead to a massive deleterious mutational load. We examine how genomic information content may act as an evolutionary constraint on other elements of the genetic information system responsible for fidelity, providing indirect evidence for its role in influencing genetic code malleability
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