Reciprocal Nucleopeptides as the Ancestral Darwinian Self-Replicator

Banwell, Eleanor F.; Piette, Bernard; Taormina, Anne; Heddle, Jonathan G.

doi:10.1093/molbev/msx292

Cited by 7 publications

(14 citation statements)

References 75 publications

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“…As other recent examples of guanine-based supramolecular structures have been shown to catalyze peroxidase reactions in the presence of hemin [ 35 ] and have provided a chiral scaffold for enantiomeric Freidel-Crafts alkylation [ 36 ], guanosine containing nucleopeptides should also be tested for emergent catalytic properties. Additionally, as the mutualism between nucleic acids and peptides in biological systems has positioned nucleopeptides [ 37 ] and co-assemblies of peptides and nucleic acids [ 38 , 39 ] as important systems in understanding chemical evolution, the self-assembled guanosine containing nucleopeptides reported in this study may inform future studies of dynamic chemical networks.…”

Section: Discussionmentioning

confidence: 99%

Impact of C-Terminal Chemistry on Self-Assembled Morphology of Guanosine Containing Nucleopeptides

et al. 2020

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Herein, we report the design and characterization of guanosine-containing self-assembling nucleopeptides that form nanosheets and nanofibers. Through spectroscopy and microscopy analysis, we propose that the peptide component of the nucleopeptide drives the assembly into β-sheet structures with hydrogen-bonded guanosine forming additional secondary structures cooperatively within the peptide framework. Interestingly, the distinct supramolecular morphologies are driven not by metal cation responsiveness common to guanine-based materials, but by the C-terminal peptide chemistry. This work highlights the structural diversity of self-assembling nucleopeptides and will help advance the development of applications for these supramolecular guanosine-containing nucleopeptides.

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Section: Discussionmentioning

confidence: 99%

Impact of C-Terminal Chemistry on Self-Assembled Morphology of Guanosine Containing Nucleopeptides

et al. 2020

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“…Our favoured nucleopeptide IDA model is a conceptual relative of the Carter and Kraut model (Figure 1). [43] It relies only on random production of short amino acids and RNAs (or possibly a mix of RNA, DNA, and other monomers since lost, known as XNA). Here, a short stretch of single-stranded (ss)RNA could act as both a primordial RNA (p-RNA) and a primordial ribosome (p-Rib), encoding a peptide sequence and catalysing its polymerisation.…”

Section: The Simplest Self-replicating Systemmentioning

confidence: 99%

“…A more appealing, soft stereochemical solution was recently elaborated in which a particular amino acid is linked to its anticodon not directly but via binding to specific sequences on primordial tRNA (p-tRNA), which are distal from the anticodon [43,53] (Figure 1). Such a p-tRNA combined with the dual function p-Rib/p-mRNA and the encoded p-Pol would comprise a functional IDA with a clear path connecting it to present day replication in cells [43].…”

Section: The Simplest Self-replicating Systemmentioning

confidence: 99%

A Peptide–Nucleic Acid Replicator Origin for Life

Piette

Heddle

2020

Trends in Ecology & Evolution

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Evolution requires self-replication. But, what was the very first self-replicator directly ancestral to all life? The currently favoured RNA World theory assigns this role to RNA alone but suffers from a number of seemingly intractable problems. Instead, we suggest that the self-replicator consisted of both peptides and nucleic acid strands. Such a nucleopeptide replicator is more feasible both in the light of the replication machinery currently found in cells and the complexity of the evolutionary path required to reach them. Recent theoretical and mathematical work supports this idea and provide a blueprint for future investigations. The Ancestral ReplicatorLife as we understand it is cellular. The last universal common ancestor (LUCA) of all cells (not a single cell of course but a population) is understood in some detail; it possessed a cell membrane, DNA, the basic molecular machines for copying DNA (i.e., polymerase etc.), and a functional ribosome, among many more [1]. From this highly truncated list alone it is clear that LUCA was far too complex to spontaneously assemble. It must have evolved from simpler systems, themselves able to self-replicate with some tolerance for error (otherwise they would not be able to evolve). Indeed, it is difficult to imagine that anything recognisably a cell could have spontaneous origins. This means that they in turn must have evolved from even simpler self replicators; that is, molecular selfreplicators. The first such replicator is referred to as the initial Darwinian ancestor (IDA) [2].The identity of the IDA has been cause for much speculation over the years. Nonbiological replicators such as clay crystals [3] have been invoked but are unconvincing as they require a complete takeover of one substrate with another and lack a persuasive argument to show how this could have occurred. An IDA built from biological molecules is more convincing and necessitates physicochemical conditions compatible with their formation, and with the self-replicating reaction cycle of the IDA itself. The latter likely required relatively mild conditions approaching those of analogous biochemical reactions today. There is now ample evidence that biological building blocks such as amino acids, ribose, and deoxyribose, among others, were present on the early Earth [4][5][6][7]. Potential chemistries for building block synthesis have been demonstrated, with cyanosulfidic chemistry [8] showing great promise. Furthermore, recent work has shown convincing peptide ligation in prebiotic conditions [9]. Given these findings, it now seems reasonable to assume that the IDA was constructed of components highly similar or identical to those found in life today. Indeed, such a replicator must have occurred at some stage very early in evolution even if not at the very beginning. The scene being set for an IDA constructed of biological molecules to arise, our focus turns to the main issue of this workdeciding on its identity. Three approaches will be useful to us in this endeavour. (i) Consideration of curren...

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“…Hypotheses for the evolutionary origins of life often include early replicators that are composed of RNA or other polymers (Szilagyi et al 2017; Stadler 2016; Czaran et al 2015; Takeuchi and Hogeweg 2012; Banwell et al 2018). In these models, the evolution of life proceeds through a stage where the gene is itself the replicator.…”

Section: Introductionmentioning

confidence: 99%

“…In modern cells, multiple genes cooperate to promote their own replication by encoding the components of the cell, including the multiple protein subunits of the chromosomal replisome (Yao and O’Donnell 2016). Similarly, several models for the evolution of early replicators involve cooperation between two or more polymeric species (Lincoln and Joyce 2009; Horning and Joyce 2016; Stadler 2016; Banwell et al 2018; Wagner et al 2017). One interesting question is how might the activity of a hypothetical multi-subunit replicator be affected by differences in the relative stability of the component subunits?…”

Section: Introductionmentioning

confidence: 99%

Models of Replicator Proliferation Involving Differential Replicator Subunit Stability

Lyu

Tower

2018

Orig Life Evol Biosph

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Several models for the origin of life involve molecules that are capable of self-replication, such as self-replicating polymers composed of RNA or DNA or amino acids. Here we consider a hypothetical replicator (AB) composed of two subunits, A and B. Programs written in Python and C programming languages were used to model AB replicator abundance as a function of cycles of replication (iterations), under specified hypothetical conditions. Two non-exclusive models describe how a reduced stability for B relative to A can have an advantage for replicator activity and/or evolution by generating free A subunits. In model 1, free A subunits associate with AB replicators to create AAB replicators with greater activity. In simulations, reduced stability of B was beneficial when the replication activity of AAB was greater than two times the replication activity of AB. In model 2, the free A subunit is inactive for some number of iterations before it re-creates the B subunit. A re-creates the B subunit with an equal chance of creating B or B', where B' is a mutant that increases AB' replicator activity relative to AB. In simulations, at moderate number of iterations (< 15), a shorter survival time for B is beneficial when the stability of B is greater than the inactive time of A. The results are consistent with the hypothesis that reduced stability for a replicator subunit can be advantageous under appropriate conditions.

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Reciprocal Nucleopeptides as the Ancestral Darwinian Self-Replicator

Cited by 7 publications

References 75 publications

Impact of C-Terminal Chemistry on Self-Assembled Morphology of Guanosine Containing Nucleopeptides

Impact of C-Terminal Chemistry on Self-Assembled Morphology of Guanosine Containing Nucleopeptides

A Peptide–Nucleic Acid Replicator Origin for Life

Models of Replicator Proliferation Involving Differential Replicator Subunit Stability

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