A viscous solvent enables information transfer from gene-length nucleic acids in a model prebiotic replication cycle

He, Christine; Gállego, Isaac; Laughlin, Brandon Patrick; Grover, Martha A.; Hud, Nicholas V.

doi:10.1038/nchem.2628

Cited by 70 publications

(56 citation statements)

References 48 publications

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“…This demonstrates the emergence of individual sequence patterns without the need of compartmentalization. c), Control simulation without cooperative enhancement of the ligation from binding (KD, 20 = KD, 40 = KD, 60 = 150 nM). The initial concentration fluctuations disappeared and the system converged to a uniform state.…”

Section: Figure 6: Frequency-dependent Selection Of Cooperative Ligatmentioning

confidence: 99%

Cooperative Ligation Breaks Sequence Symmetry and Stabilizes Early Molecular Replication

Toyabe

Braun

2019

Phys. Rev. X

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Each living species carries a complex DNA sequence that determines their unique features and functionalities. It is generally assumed that life started from a random pool of oligonucleotides sequences, generated by a prebiotic polymerization of nucleotides. The mechanism that initially facilitated the emergence of sequences that code for the function of the first species from such a random pool of sequences remains unknown. It is a central problem of the origin of life. An interesting option would be a self-selection mechanism by spontaneous symmetry breaking. Initial concentration fluctuations of specific sequence motifs would have been amplified and outcompeted less abundant sequences, enhancing the signal to noise to replicate and select functional sequences. Here, we demonstrate with experimental and theoretical findings that templated ligation would provide such a self-selection. In templated ligation, two adjacent single sequences strands are chemically joined when a third complementary strand sequence brought them in close proximity. This simple mechanism was a likely side-product of a prebiotic polymerization chemistry once the strands reach the length to form double stranded species. As shown here, the ligation gave rise to a nonlinear replication process by the cooperative ligation of matching sequences which self-promoted their own elongation. This led to a cascade of enhanced template binding and faster ligation reactions. A requirement was the reshuffling of the strands by thermal cycling, enabled for example by microscale convection. By using a limited initial sequence space and performing long term ligations, we found that complementary sequences with an initially higher concentration prevailed over either non-complementary or less concentrated sequences. The latter died out by the molecular degradation that we simulated in the experiment by serial dilution. The experimental results are consistent with both explicit and abstract theory models that were generated considering the ligation rates determined experimentally. Previously, other nonlinear modes of replication such as Hypercycles have been discussed to overcome instabilities from first-order replication dynamics such as the error catastrophe and the dominance of structurally simple, but fast replicating sequences, known as the Spiegelman problem. Assuming that templated ligation was driven by the same chemical mechanism that generated prebiotic polymerization of oligonucleotides, the mechanism could function as a missing link between polymerization and the self-stabilized replication, offering a pathway to the autonomous emergence of Darwinian evolution for the origin of life.

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Section: Figure 6: Frequency-dependent Selection Of Cooperative Ligatmentioning

confidence: 99%

Cooperative Ligation Breaks Sequence Symmetry and Stabilizes Early Molecular Replication

Toyabe

Braun

2019

Phys. Rev. X

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“…Precursors have been shown to give rise to more complex structures through a variety of non-chemical processes (Ferris and Orgel 1966;Sanchez et al 1967Sanchez and Orgel 1970;Fuller et al 1972a,b;Orgel and Crick 1993;Ferris et al 1996;Orgel 2004;Powner et al 2009Powner et al , 2010Powner et al , 2011. Other efforts towards demonstrating the prebiotic synthesis of RNA have yielded promising results (Cafferty et al 2016;Yeates et al 2016;Costanzo et al 2017;He et al 2017;Mathis et al 2017;Szilagyi et al 2017;Taran et al 2017;Yeates et al 2017). A significant effort resulted in the robust production of enantiopure RNA precursors from racemic starting materials under potential prebiotic conditions (Hein et al 2011;Leu et al 2011;.…”

Section: Can a Primitive Rna World Or Rna-peptide World Generate Rapimentioning

confidence: 99%

The Emergence of Life

et al. 2019

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The aim of this article is to provide the reader with an overview of the different possible scenarios for the emergence of life, to critically assess them and, according to the conclusions we reach, to analyze whether similar processes could have been conducive to independent origins of life on the several icy moons of the Solar System. Instead of directly proposing a concrete and unequivocal cradle of life on Earth, we focus on describing the different requirements that are arguably needed for the transition between non-life to life. We Ocean Worlds Edited by 56 Page 2 of 53 E. Camprubí et al.approach this topic from geological, biological, and chemical perspectives with the aim of providing answers in an integrative manner. We reflect upon the most prominent origins hypotheses and assess whether they match the aforementioned abiogenic requirements. Based on the conclusions extracted, we address whether the conditions for abiogenesis are/were met in any of the oceanic icy moons.

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“…In particular, 2-methylimidazole [56] and, more recently, 2-aminoimidazole, [57] have been found to be highly efficient phosphate activators, both of which might have been plausible under primitive Earth conditions (Figure 3b). [67] Other attractive environments are spatially confined thermal gradients, since these permit both size-selective trapping and thermal cycling of polynucleotides through convection and thermophoresis. [61] Compared to von Kiedrowski's and Zielinski and Orgel's early replicators, polymerization-based enzyme-free sequence copying still falls short of true autocatalytic self-replication, which prevents its use as primitive genetic system, e.g., in model protocells.…”

Section: Nonenzymatic Nucleic Acid Replicationmentioning

confidence: 99%

Templated Self‐Replication in Biomimetic Systems

et al. 2019

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nanostructures and nanopatterns. [13][14][15] The specificity of the molecular recognitions between replicative units is concomitant with the encoding and transmission of information, with the degree of specificity determining the fidelty and capacity of information transfer against competing background interactions in noisy "chemical" environments. [16] However, the ability to replicate in this manner does not imply the ability to transmit additional heritable information-simple replicators can only replicate information related to recognition and template directed autocatalysis as this information is intrinsically linked to phenotype. In contrast to most artificial autocatalytic replicators, living systems (including viruses) store the key instructions for replication on an inheritable genetic system rather than in the native structures of the individual sub-components. This decoupling of phenotype and genotype enables heredity and open-ended evolution, the possibility of an indefinite increase in complexity, as evolutionary innovations aquired by natural selection are anchored in the genotype only. [17,18] The most prominent self-replicating molecules are nucleic acids, which form the fundamental basis for information storage and propagation in biological systems. The ability of polynucleic acids to store information is self-evident, and based upon the ability to form cognate Watson-Crick base pair interactions. Nucleic acid systems may have also formed the first genetic replicators in biology. The RNA world hypothesis postulates a stage in the origin of life in which RNA proliferated before the emergence of DNA and proteins. To do this, RNA must be able to carry out several key roles: information storage, catalysis, and (self-) replication. Multiple examples of catalytic RNAs (ribozymes) are known both from nature and in vitro selection experiments, [19][20][21][22] but there is no fossil evidence of an RNA capable of (self-)replication without the involvement of proteins.While minimal nucleic acid-only systems with replicationlike properties have been identified by directed evolution and engineering, limitations such as low activity, lack of generality, and poor information capacity limit their usefulness in bottomup synthetic biology, except in origin of life research. For the creation of more complex biological in vitro systems, RNA or DNA replication mechanisms involving more powerful protein enzymes are likely to be necessary. Even so, the achievement of self-sustained in vitro self-replication inspired by the central dogma of molecular biology is currently hampered by the requirement to encode and efficiently express the enormous A key characteristic of living systems is the storage and replication of information, and as such the development of self-replicating systems capable of heredity is of great importance to the fields of synthetic biology and origin of life research. In this review, the design and implementation of self-replicating systems in the context of bottom-up synthetic biology is discusse...

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A viscous solvent enables information transfer from gene-length nucleic acids in a model prebiotic replication cycle

Cited by 70 publications

References 48 publications

Cooperative Ligation Breaks Sequence Symmetry and Stabilizes Early Molecular Replication

Cooperative Ligation Breaks Sequence Symmetry and Stabilizes Early Molecular Replication

The Emergence of Life

Templated Self‐Replication in Biomimetic Systems

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