The dynamics of the RNA world: insights and challenges

Abstract

The problem of the origin of life is not only one of structure but also that of dynamics. Ever since the seminal result of Manfred Eigen in 1971 showing that early template replication suffers from an error threshold, research has tackled the issue of how early genomes could have been dynamically stable without highly evolved mechanisms such as accurate replication and chromosomes. We review the theory of the origin, maintenance and enhancement of the RNA world as an evolving population of dynamical systems. Investigation of sequence space has revealed how structures are allocated in sequence space and how this affects the nature of the error threshold that sets the selectively maintainable genome length. New applications of old dynamical theory are still possible: the application of Gause's principle of competitive exclusion, based on resource utilisation, to RNA replication predicts that at most four pairs (plus and minus strands) can stably be maintained on four nucleotides. Other mechanisms of early template coexistence should be regarded as additional means to raise the number of coexisting species above the number set by the competitive exclusion principle. One such example is the hypercycle in which templates were postulated to help replication of the next member in a cycle superimposed on individual replication cycles. Although the hypercycle is ecologically unstable it is evolutionarily unstable because it cannot efficiently compete against emerging parasites. Population structure can modify this conclusion but not without further qualification. The simplest form of population structure is limited diffusion on a surface. This simple mechanism can ensure the coexistence of competing ribozymes contributing to surface metabolism as well as the spread of efficient replicases despite the parasite problem. Hypercyclescan only be saved by active compartmentalization when replicators are enclosed in reproducing protocells. Once there are protocells there is no need for internal hypercyclic organization, however. Finally we review two crucial adaptations that enhanced the RNA world: chromosomes and enzymatic metabolism. Interestingly, it was shown that these two have been presumably coevolutionarily linked because protocells harbouring unlinked, competing ribozymes are better off if the ribozymes remain inefficient but generalists. The appearance of chromosomes alleviates intragenomic conflict and is enabling constraint for the emergence of specific and efficient enzymes.The possibility of an RNA world, a period in the origin of life on Earth, when RNA molecules acted both as enzymes and as genetic material, was suggested well before the name was coined by Gilbert in 1986 1 . The history of the research on the origin of life 2 tells us that the potential prebiotic importance of RNA was suggested as early as in the late 50's. When it became established that living cells harbour much more RNA than DNA some biologist have proposed that RNA preceded DNA during evolution 3,4 . The discovery of the details of protein ...

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