Emergence of Information Transmission in a Prebiotic RNA Reactor

Obermayer, Benedikt; Krammer, Hubert; Braun, Dieter; Gerland, Ulrich

doi:10.1103/physrevlett.107.018101

Cited by 27 publications

(36 citation statements)

References 20 publications

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“…For example, the possibility that stable folding could be protective against degradation, and therefore help select for structured molecules, has been studied theoretically in the context of non-templated ligation. 62 In that study, the simulated RNA pool showed a surprising degree of heritability even though ligation was not templated. One wonders how this effect would alter the evolutionary dynamics of prelife, perhaps by enhancing replication.…”

Section: Discussionmentioning

confidence: 93%

From Prelife to Life: How Chemical Kinetics Become Evolutionary Dynamics

Chen

Nowak

2012

Acc. Chem. Res.

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Conspectus Life is that which evolves. Living systems are the products of evolutionary processes and are capable of undergoing further evolution. A crucial question for the origin of life is the following: when do chemical kinetics become evolutionary dynamics? In this paper we review properties of ‘prelife’ and discuss the transition from prelife to life. We describe prelife as a chemical system where activated monomers can co-polymerize into macromolecules (such as RNA). These macromolecules are information carriers. Their physical and chemical properties depend to a certain extent on their particular sequence of monomers. We consider prelife as a logical precursor of life, where macromolecules are formed by copolymerization, but they are not capable of replication. Prelife can undergo ‘prevolutionary dynamics’. There can be mutation, selection and cooperation. Prelife selection, however, is blunt: small differences in rate constants lead to small differences in abundance. Life emerges with the ability of replication. In the resulting evolutionary dynamics selection is sharp: small differences in rate constants can lead to large differences in abundance. We also study the competition of different ‘prelives’ and find that there can be selection for those systems which ultimately give rise to replication. The transition from prelife to life can occur over an extended period of time. There may not have been a single moment which marks the origin of life. Instead prelife seeds many attempts for the origin of life. Eventually life takes over and destroys prelife.

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Section: Discussionmentioning

confidence: 93%

From Prelife to Life: How Chemical Kinetics Become Evolutionary Dynamics

Chen

Nowak

2012

Acc. Chem. Res.

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“…Interestingly, important steps in peptide synthesis can be catalyzed by simple RNA molecules under physiological conditions (37). In addition, it was recently shown theoretically by modeling RNA ligation in a thermophoretic trap that sequence information transmission can be initiated by differential degradation in a thermal oscillation (38). More generally, the framework of nonequilibrium statistical thermodynamics can be used as a unifying theoretical framework to describe the generation of sequence information, using chemical and physical nonequilibrium processes (39).…”

Section: Discussionmentioning

confidence: 99%

Escalation of polymerization in a thermal gradient

Mast

Schink

Gerland

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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149

159

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For the emergence of early life, the formation of biopolymers such as RNA is essential. However, the addition of nucleotide monomers to existing oligonucleotides requires millimolar concentrations. Even in such optimistic settings, no polymerization of RNA longer than about 20 bases could be demonstrated. How then could self-replicating ribozymes appear, for which recent experiments suggest a minimal length of 200 nt? Here, we demonstrate a mechanism to bridge this gap: the escalated polymerization of nucleotides by a spatially confined thermal gradient. The gradient accumulates monomers by thermophoresis and convection while retaining longer polymers exponentially better. Polymerization and accumulation become mutually self-enhancing and result in a hyperexponential escalation of polymer length. We describe this escalation theoretically under the conservative assumption of reversible polymerization. Taking into account the separately measured thermophoretic properties of RNA, we extrapolate the results for primordial RNA polymerization inside a temperature gradient in pores or fissures of rocks. With a dilute, nanomolar concentration of monomers the model predicts that a pore length of 5 cm and a temperature difference of 10 K suffice to polymerize 200-mers of RNA in micromolar concentrations. The probability to generate these long RNAs is raised by a factor of >10 600 compared with polymerization in a physical equilibrium. We experimentally validate the theory with the reversible polymerization of DNA blocks in a laser-driven thermal trap. The results confirm that a thermal gradient can significantly enlarge the available sequence space for the emergence of catalytically active polymers. molecular evolution | nonequilibrium | RNA world | (nonenzymatic) emergence of RNA | hydrothermal vents P olymers are the vital building blocks of all known life forms. According to the central dogma of molecular biology (1), DNA stores the information for how and when to build proteins, which for their part carry out catalytic tasks like the polymerization of DNA. How this self-perpetuating cycle has started is unknown. The RNA-world hypothesis posits that RNA molecules were the central players in prebiotic evolution, because they exhibit both a catalytic function similar to that of proteins and the information storage capabilities of DNA (2). However, how could such an RNA world have emerged from the prebiotic soup?A key element of the RNA world is a ribozyme that catalyzes RNA replication. Directed in vitro evolution and engineering have shown that such ribozymes exist, but require a length of 200 bases or more, even in favorable high-salt conditions (3). Starting from chemical nonequilibrium conditions with millimolar concentrations of energy-rich nucleotides (4-6) and with the help of catalytic surfaces (7), only the formation of much shorter polynucleotides on the order of 20 bases was demonstrated in the laboratory. Slow kinetics and cleavage due to hydrolysis limit the formation of long polynucleotides and finally lead...

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“…Pioneering reports of RNA recombination have appeared [7][8][9][10][11][12]. With the possible exception of the systems described in [13][14][15], the reactions reported so far are not simple and robust enough to be of likely prebiotic relevance.…”

Section: Introductionmentioning

confidence: 99%

Ribozyme Activity of RNA Nonenzymatically Polymerized from 3′,5′-Cyclic GMP

Pino

Costanzo

Giorgi

et al. 2013

Entropy

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3′,5′-Cyclic GMP spontaneously nonenzymatically polymerizes in a base-catalyzed reaction affording G oligonucleotides. When reacted with fully or partially sequence-complementary RNA (oligo C), the abiotically generated oligo G RNA displays a typical ribozyme activity consisting of terminal ligation accompanied by cleavage of an internal phosphate site of the donor oligonucleotide stem upon attack of the acceptor 3′ terminal OH. This reaction is dubbed Ligation following Intermolecular Cleavage (LIC). In a prebiotic perspective, the ability of oligo G polynucleotides to react with other sequences outlines a simple and possible evolutionary scenario based on the autocatalytic properties of RNA.

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Emergence of Information Transmission in a Prebiotic RNA Reactor

Cited by 27 publications

References 20 publications

From Prelife to Life: How Chemical Kinetics Become Evolutionary Dynamics

From Prelife to Life: How Chemical Kinetics Become Evolutionary Dynamics

Escalation of polymerization in a thermal gradient

Ribozyme Activity of RNA Nonenzymatically Polymerized from 3′,5′-Cyclic GMP

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