The dawn of the RNA World: Toward functional complexity through ligation of random RNA oligomers

Briones, Carlos; Stich, Michael; Manrubia, Susanna C.

doi:10.1261/rna.1488609

Cited by 99 publications

(101 citation statements)

References 61 publications

(67 reference statements)

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“…Most abundant structural motifs are topologically simple and occur frequently in natural RNAs (Gan et al, 2003;Cowperthwaite et al, 2008). They could have also played a relevant role in prebiotic scenarios where random polymerization was likely, by constituting simple building blocks able to combine into more complex structures (Briones et al, 2009). …”

Section: Introductionmentioning

confidence: 99%

Motif frequency and evolutionary search times in RNA populations

Stich

Manrubia

2011

Journal of Theoretical Biology

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RNA molecules, through their dual identity as sequence and structure, are an appropriate experimental and theoretical model to study the genotype-phenotype map and evolutionary processes taking place in simple replicator populations. In this computational study, we relate properties of the sequence-structure map, in particular the abundance of a given secondary structure in a random pool, with the number of replicative events that an initially random population of sequences needs to find that structure through mutation and selection. For common structures, this search process turns out to be much faster than for rare structures. Furthermore, search and fixation processes are more efficient in a wider range of mutation rates for common structures, thus indicating that evolvability of RNA populations is not simply determined by abundance. We also find significant differences in the search and fixation processes for structures of same abundance, and relate them with the number of base pairs forming the structure. Moreover, the influence of the nucleotide content of the RNA sequences on the search process is studied. Our results advance in the understanding of the distribution and attainability of RNA secondary structures. They hint at the fact that, beyond sequence length and sequence-to-function redundancy, the mutation rate that permits localization and fixation of a given phenotype strongly depends on its relative abundance and global, in general nonuniform, distribution in sequence space.

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Section: Introductionmentioning

confidence: 99%

Motif frequency and evolutionary search times in RNA populations

Stich

Manrubia

2011

Journal of Theoretical Biology

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“…has recently been suggested that the spontaneous emergence of RNA polymerases even without previous nonenzymatic replication could be promoted by a significant increase of functional complexity in a pool of random RNA due to the likely appearance of ligase activity [13].…”

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Escalation of error catastrophe for enzymatic self-replicators

Obermayer

Frey

2009

Europhys. Lett.

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Abstract. -It is a long-standing question in origin-of-life research whether the information content of replicating molecules can be maintained in the presence of replication errors. Extending standard quasispecies models of non-enzymatic replication, we analyze highly specific enzymatic self-replication mediated through an otherwise neutral recognition region, which leads to frequency-dependent replication rates. We find a significant reduction of the maximally tolerable error rate, because the replication rate of the fittest molecules decreases with the fraction of functional enzymes. Our analysis is extended to hypercyclic couplings as an example for catalytic networks.Introduction. -According to the RNA world hypothesis [1], prebiotic biochemical life is thought to have emerged through four steps: starting from the primordial non-enzymatic synthesis of nucleotides and their subsequent non-enzymatic polymerization into random RNA, which in a third step would non-enzymatically replicate, natural selection would finally produce a set of functional RNA enzymes (ribozymes), establishing exponential growth and initiating RNA evolution. Despite considerable experimental progress [2,3], as of today no truely self-replicating system has been evolved according to this hypothetic schedule. To assess its intrinsic plausibility, theory has mainly focused on the third step, usually based on the Eigen model [4] for prebiotic evolution: here, autocatalytic self-replication of L-nucleotide sequences proceeds non-enzymatically via stepwise template-directed polymerization, with a non-negligible error probability µ per single nucleotide. Assuming that one specific "master" template replicates with the highest rate α > 1, while all other sequences have unit replication rate, it is found that faithful replication of the master is possible only for error probabilities smaller than a critical value µ c ≈ ln α/L. In this regime, the population in sequence space is concentrated about the master in a rather broad distribution, giving rise to the notion of a "quasispecies". Larger values µ > µ c lead to a delocalized state with completely random sequences in the population. Many aspects of the

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“…The similarities between the populations evolved here and RNAs evolved previously in vitro and in vivo do, however, suggest the possibility of a smooth evolutionary transition from biomolecules evolving in association with mineral surfaces to evolving in mineralfree protocellular environments. These similarities also increase the confidence with which insights derived from in vitro evolution studies performed without minerals, can be applied to origin of life scenarios involving mineral surfaces (Hanczyc et al 2003;Briones et al 2009;Konnyu et al 2015;Shay et al 2015). While the presence of montmorillonite had surprisingly little impact on the evolution of ribozymes that catalyze self-cleavage, it remains to be seen if intermolecular functions such as ligand binding or RNA ligation are more strongly impacted by the presence of this mineral surface.…”

Section: Discussionmentioning

confidence: 90%

Evolution of ribozymes in the presence of a mineral surface

Stephenson

Popovic

Bristow

et al. 2016

RNA

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Mineral surfaces are often proposed as the sites of critical processes in the emergence of life. Clay minerals in particular are thought to play significant roles in the origin of life including polymerizing, concentrating, organizing, and protecting biopolymers. In these scenarios, the impact of minerals on biopolymer folding is expected to influence evolutionary processes. These processes include both the initial emergence of functional structures in the presence of the mineral and the subsequent transition away from the mineral-associated niche. The initial evolution of function depends upon the number and distribution of sequences capable of functioning in the presence of the mineral, and the transition to new environments depends upon the overlap between sequences that evolve on the mineral surface and sequences that can perform the same functions in the mineral's absence. To examine these processes, we evolved self-cleaving ribozymes in vitro in the presence or absence of Na-saturated montmorillonite clay mineral particles. Starting from a shared population of random sequences, RNA populations were evolved in parallel, along separate evolutionary trajectories. Comparative sequence analysis and activity assays show that the impact of this clay mineral on functional structure selection was minimal; it neither prevented common structures from emerging, nor did it promote the emergence of new structures. This suggests that montmorillonite does not improve RNA's ability to evolve functional structures; however, it also suggests that RNAs that do evolve in contact with montmorillonite retain the same structures in mineral-free environments, potentially facilitating an evolutionary transition away from a mineralassociated niche.

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The dawn of the RNA World: Toward functional complexity through ligation of random RNA oligomers

Cited by 99 publications

References 61 publications

Motif frequency and evolutionary search times in RNA populations

Motif frequency and evolutionary search times in RNA populations

Escalation of error catastrophe for enzymatic self-replicators

Evolution of ribozymes in the presence of a mineral surface

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