Selfishness versus functional cooperation in a stochastic protocell model

Ζιντζαράς, Ηλίας; Santos, Mauro; Szathmáry, Eörs

doi:10.1016/j.jtbi.2010.09.011

Cited by 19 publications

(18 citation statements)

References 49 publications

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“…This shows a sense of “group selection”, but does not involve the “correcting” mechanism described in SCM; as mentioned above, a lower rate of protocell division would favor the co-spread of the ribozymes (to prevent “gene loss”). It was recently shown that if competition of replicators with different replicating rates (in a sense as templates) were subjugated, the “correcting” mechanism at the level of the protocell may no longer be significantly important [66]. Additionally, another possible reason may deserve attention.…”

Section: Discussionmentioning

confidence: 99%

Computer Simulation on the Cooperation of Functional Molecules during the Early Stages of Evolution

2012

PLoS ONE

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It is very likely that life began with some RNA (or RNA-like) molecules, self-replicating by base-pairing and exhibiting enzyme-like functions that favored the self-replication. Different functional molecules may have emerged by favoring their own self-replication at different aspects. Then, a direct route towards complexity/efficiency may have been through the coexistence/cooperation of these molecules. However, the likelihood of this route remains quite unclear, especially because the molecules would be competing for limited common resources. By computer simulation using a Monte-Carlo model (with “micro-resolution” at the level of nucleotides and membrane components), we show that the coexistence/cooperation of these molecules can occur naturally, both in a naked form and in a protocell form. The results of the computer simulation also lead to quite a few deductions concerning the environment and history in the scenario. First, a naked stage (with functional molecules catalyzing template-replication and metabolism) may have occurred early in evolution but required high concentration and limited dispersal of the system (e.g., on some mineral surface); the emergence of protocells enabled a “habitat-shift” into bulk water. Second, the protocell stage started with a substage of “pseudo-protocells”, with functional molecules catalyzing template-replication and metabolism, but still missing the function involved in the synthesis of membrane components, the emergence of which would lead to a subsequent “true-protocell” substage. Third, the initial unstable membrane, composed of prebiotically available fatty acids, should have been superseded quite early by a more stable membrane (e.g., composed of phospholipids, like modern cells). Additionally, the membrane-takeover probably occurred at the transition of the two substages of the protocells. The scenario described in the present study should correspond to an episode in early evolution, after the emergence of single “genes”, but before the appearance of a “chromosome” with linked genes.

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Section: Discussionmentioning

confidence: 99%

Computer Simulation on the Cooperation of Functional Molecules during the Early Stages of Evolution

2012

PLoS ONE

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“…Zintzaras et al [48] investigated the consequence of the trade-off between catalytic activity and template affinity to RNA polymerase in ribozymes and proposed that the complete absence of competition between two species of ribozymes could lead to the evolutionary divergence where one species functions slightly more efficiently as a catalyst and the other functions more efficiently as a template. Despite the superficial similarity, this form of divergence crucially differs from the division of labor between template and catalyst discussed here.…”

Section: Discussionmentioning

confidence: 99%

On the Origin of DNA Genomes: Evolution of the Division of Labor between Template and Catalyst in Model Replicator Systems

2011

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The division of labor between template and catalyst is a fundamental property of all living systems: DNA stores genetic information whereas proteins function as catalysts. The RNA world hypothesis, however, posits that, at the earlier stages of evolution, RNA acted as both template and catalyst. Why would such division of labor evolve in the RNA world? We investigated the evolution of DNA-like molecules, i.e. molecules that can function only as template, in minimal computational models of RNA replicator systems. In the models, RNA can function as both template-directed polymerase and template, whereas DNA can function only as template. Two classes of models were explored. In the surface models, replicators are attached to surfaces with finite diffusion. In the compartment models, replicators are compartmentalized by vesicle-like boundaries. Both models displayed the evolution of DNA and the ensuing division of labor between templates and catalysts. In the surface model, DNA provides the advantage of greater resistance against parasitic templates. However, this advantage is at least partially offset by the disadvantage of slower multiplication due to the increased complexity of the replication cycle. In the compartment model, DNA can significantly delay the intra-compartment evolution of RNA towards catalytic deterioration. These results are explained in terms of the trade-off between template and catalyst that is inherent in RNA-only replication cycles: DNA releases RNA from this trade-off by making it unnecessary for RNA to serve as template and so rendering the system more resistant against evolving parasitism. Our analysis of these simple models suggests that the lack of catalytic activity in DNA by itself can generate a sufficient selective advantage for RNA replicator systems to produce DNA. Given the widespread notion that DNA evolved owing to its superior chemical properties as a template, this study offers a novel insight into the evolutionary origin of DNA.

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“…This process protects the population from extinction and results in evolutionary dynamics yielding a stable quasispecies at the level of compartments 162 . The SCM is inherently stable against parasites: it has the ability to select against inferior and select for superior mutants [163][164][165][166] . The cells of the SCM are individuals subject to selection and are thus evolutionary units.…”

Section: Ii/3 Active Compartmentalizationmentioning

confidence: 99%

“…It has the ability to select against inferior and for superior mutants. [173][174][175][176] The cells of the SCM are individuals subject to selection, and thus are evolutionary units. Selection at the level of compartments can be considered as group selection 177,178 because (1) the number of templates in protocells is much smaller than the number of compartments; (2) each protocell has only one parent; and (3) there is no migration among groups.…”

Section: Active Compartmentalizationmentioning

confidence: 99%

The dynamics of the RNA world: insights and challenges

Kun

Szilágyi

Könnyű

et al. 2015

Annals of the New York Academy of Sciences

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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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Selfishness versus functional cooperation in a stochastic protocell model

Cited by 19 publications

References 49 publications

Computer Simulation on the Cooperation of Functional Molecules during the Early Stages of Evolution

Computer Simulation on the Cooperation of Functional Molecules during the Early Stages of Evolution

On the Origin of DNA Genomes: Evolution of the Division of Labor between Template and Catalyst in Model Replicator Systems

The dynamics of the RNA world: insights and challenges

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