From Prelife to Life: How Chemical Kinetics Become Evolutionary Dynamics

Chen, Irene; Nowak, Martin A.

doi:10.1021/ar2002683

Cited by 45 publications

(52 citation statements)

References 66 publications

(119 reference statements)

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“…In our chemical system, there is no replication per se. It is more de novo synthesis (reproduction rather than replication) that could be described as prelife (13,14) in which the replicator equation does not apply. Here, Eq.…”

Section: Discussionmentioning

confidence: 99%

“…However, it can be sharply seen in the 20+-y effort aimed at developing a generalized RNA replicase ribozyme in the laboratory: new successes have taken advantage of a fragmentation of the best such artificial ribozyme and invoke a network of reactions to provide for its assembly (12). Our own laboratories have focused on a variety of "prelife" (13,14) and cooperative network (15,16) approaches to understand how evolving RNA systems could have arisen from abiotic sources of nucleotides and short oligomers. Many others have also stressed the need for distributed functionality at the onset of life, both chemically (17) and in space and time (18,19).…”

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confidence: 99%

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Dynamics of prebiotic RNA reproduction illuminated by chemical game theory

Yeates

Hilbe

Zwick

et al. 2016

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

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Many origins-of-life scenarios depict a situation in which there are common and potentially scarce resources needed by molecules that compete for survival and reproduction. The dynamics of RNA assembly in a complex mixture of sequences is a frequencydependent process and mimics such scenarios. By synthesizing Azoarcus ribozyme genotypes that differ in their single-nucleotide interactions with other genotypes, we can create molecules that interact among each other to reproduce. Pairwise interplays between RNAs involve both cooperation and selfishness, quantifiable in a 2 × 2 payoff matrix. We show that a simple model of differential equations based on chemical kinetics accurately predicts the outcomes of these molecular competitions using simple rate inputs into these matrices. In some cases, we find that mixtures of different RNAs reproduce much better than each RNA type alone, reflecting a molecular form of reciprocal cooperation. We also demonstrate that three RNA genotypes can stably coexist in a rock-paper-scissors analog. Our experiments suggest a new type of evolutionary game dynamics, called prelife game dynamics or chemical game dynamics. These operate without templatedirected replication, illustrating how small networks of RNAs could have developed and evolved in an RNA world.RNA | prebiotic chemistry | origins of life | game theory | ribozyme A plausible description of a sequence of events that could have led to the origins of life on the Earth from a purely chemical milieu has long been desirable, yet remains elusive. The RNA world hypothesis has helped sharpen our focus on what could have taken place 4 Gya, in that RNA serves as a powerful model for a self-sustaining chemical system capable of evolutionary change (1-6). Although this hypothesis has engendered much debate, both in its general applicability and in the details of its implementation (7-9), there are some clear emerging trends. Among the recent advances in prebiotic RNA studies is the concept of an evolving "network" of RNAs being required to kick-start life, rather than a single selfish entity. This idea dates back to the formative studies of Eigen and Schuster in the 1970s (10, 11). However, it can be sharply seen in the 20+-y effort aimed at developing a generalized RNA replicase ribozyme in the laboratory: new successes have taken advantage of a fragmentation of the best such artificial ribozyme and invoke a network of reactions to provide for its assembly (12). Our own laboratories have focused on a variety of "prelife" (13, 14) and cooperative network (15, 16) approaches to understand how evolving RNA systems could have arisen from abiotic sources of nucleotides and short oligomers. Many others have also stressed the need for distributed functionality at the onset of life, both chemically (17) and in space and time (18,19).To advance a network approach to the "single biomolecule problem" in the RNA world, what is needed now is an understanding of how prebiotic networks could have evolved. Auspiciously, the mechanisms of network evol...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Dynamics of prebiotic RNA reproduction illuminated by chemical game theory

Yeates

Hilbe

Zwick

et al. 2016

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

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“…In one such model, it is assumed that polymers serve as their own templates because of the ability of certain heteropolymers to concentrate their own precursors (16)(17)(18)(19). It supposes an ability of molecules to recognize "self," although without specifying exactly how.…”

Section: Ctb Requires An Autocatalytic Processmentioning

confidence: 99%

Foldamer hypothesis for the growth and sequence differentiation of prebiotic polymers

Guseva

Zuckermann

Dill

2017

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

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It is not known how life originated. It is thought that prebiotic processes were able to synthesize short random polymers. However, then, how do short-chain molecules spontaneously grow longer? Also, how would random chains grow more informational and become autocatalytic (i.e., increasing their own concentrations)? We study the folding and binding of random sequences of hydrophobic (H) and polar (P) monomers in a computational model. We find that even short hydrophobic polar (HP) chains can collapse into relatively compact structures, exposing hydrophobic surfaces. In this way, they act as primitive versions of today's protein catalysts, elongating other such HP polymers as ribosomes would now do. Such foldamer catalysts are shown to form an autocatalytic set, through which short chains grow into longer chains that have particular sequences. An attractive feature of this model is that it does not overconverge to a single solution; it gives ensembles that could further evolve under selection. This mechanism describes how specific sequences and conformations could contribute to the chemistry-to-biology (CTB) transition.origin of life | HP model | biopolymers | autocatalytic sets A mong the most mysterious processes in chemistry is how the spontaneous transition occurred more than 3 billion years ago from a soup of prebiotic molecules to living cells. What was the mechanism of the chemistry-to-biology (CTB) transition? In this paper, we develop a model to explore how prebiotic polymerization processes might have produced long chains of proteinlike or nucleic acid-like molecules (1, 2). What polymerization processes are autocatalytic? How could they have produced long chains? Also, how might random chain sequences have become informational and self-serving? Our questions here are about physical spontaneous mechanisms, not about specific monomer or polymer chemistries. CTB Requires an Autocatalytic ProcessEarly on, it was recognized that the transition from simple chemistry to self-supporting biological behavior requires autocatalysis (i.e., some form of positive feedback or bootstrapping, in which the concentrations of some molecules become amplified and selfsustaining relative to other molecules) (3-8). That work has led to the idea of an autocatalytic set, a collection of entities in which any one entity can catalyze another.We first review some of the key results. A class of models called Graded Autocatalysis Replication Domain (GARD) (9-11) predicts that artificial autocatalytic chemical kinetic networks can lead to self-replication, with a corresponding amplification of some chemicals over others. Such systems display some degree of inheritance and adaptability. GARD model is a subset of metabolism first models, which envision that small molecule chemical processes precede information transfer and precede the first biopolymers. Focusing on polymers, Wu and Higgs (12) developed a model of RNA chain-length autocatalysis. They envision that some of the RNA chains can spontaneously serve as polymerase ribozymes, l...

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“…[6][7][8] What was/were the RNA precursor/ s 9 that underwent chemical evolution and the "fittest" of them came to dominate the biotic landscape? 10 This would mean a longer list of "extinct" molecular species. A variety of organic moieties have been presented as RNA precursor/s i.e.…”

Section: Introductionmentioning

confidence: 99%

Achiral, acyclic nucleic acids: synthesis and biophysical studies of a possible prebiotic polymer

et al. 2015

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The search for prebiotic, nucleic acid precursors is, at its best, a speculative undertaking. Given the complex structure of RNA, it is not very likely that RNA was the first information system in the universe and thus finding possible precursor/s i.e. pre-RNA remains an open challenge. We, in this paper, have tried to construct nucleic acid polymers with a simple acyclic, achiral backbone. Such a linear, achiral backbone may have been formed from simple monomers that may have existed in the "prebiotic soup". We have shown that such polymers are capable of identifying the complementary "other self" and thus forming a potential system for information storage and transmission. This study thus involves investigation of nucleic acid analogues with a modified backbone that are likely to have formed in the prebiotic setting.

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From Prelife to Life: How Chemical Kinetics Become Evolutionary Dynamics

Cited by 45 publications

References 66 publications

Dynamics of prebiotic RNA reproduction illuminated by chemical game theory

Dynamics of prebiotic RNA reproduction illuminated by chemical game theory

Foldamer hypothesis for the growth and sequence differentiation of prebiotic polymers

Achiral, acyclic nucleic acids: synthesis and biophysical studies of a possible prebiotic polymer

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