Unified prebiotically plausible synthesis of pyrimidine and purine RNA ribonucleotides

Becker, Sidney; Feldmann, Jonas; Wiedemann, Stefan; Okamura, Hirokazu; Schneider, Christina; Iwan, Katharina; Crisp, Antony; Rossa, Martin; Amatov, Tynchtyk; Carell, Thomas

doi:10.1126/science.aax2747

Cited by 228 publications

(227 citation statements)

References 51 publications

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“…An important point is that these potential monomers are not passive solutes, but instead are involved in a variety of chemical reactions that increase their chemical complexity. For instance, Becker et al (2018Becker et al ( , 2019 established cycling reaction pathways by which all four nucleobases, nucleosides and nucleotides can be synthesized in ''one pot'' systems through wet-dry cycling. Nam et al (2018) and Powner et al (2009) described surface conditions in which nucleosides and nucleotides can also be nonenzymatically synthesized.…”

Section: The Central Role Of Cyclingmentioning

confidence: 99%

The Hot Spring Hypothesis for an Origin of Life

2020

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We present a testable hypothesis related to an origin of life on land in which fluctuating volcanic hot spring pools play a central role. The hypothesis is based on experimental evidence that lipid-encapsulated polymers can be synthesized by cycles of hydration and dehydration to form protocells. Drawing on metaphors from the bootstrapping of a simple computer operating system, we show how protocells cycling through wet, dry, and moist phases will subject polymers to combinatorial selection and draw structural and catalytic functions out of initially random sequences, including structural stabilization, pore formation, and primitive metabolic activity. We propose that protocells aggregating into a hydrogel in the intermediate moist phase of wet-dry cycles represent a primitive progenote system. Progenote populations can undergo selection and distribution, construct niches in new environments, and enable a sharing network effect that can collectively evolve them into the first microbial communities. Laboratory and field experiments testing the first steps of the scenario are summarized. The scenario is then placed in a geological setting on the early Earth to suggest a plausible pathway from life's origin in chemically optimal freshwater hot spring pools to the emergence of microbial communities tolerant to more extreme conditions in dilute lakes and salty conditions in marine environments. A continuity is observed for biogenesis beginning with simple protocell aggregates, through the transitional form of the progenote, to robust microbial mats that leave the fossil imprints of stromatolites so representative in the rock record. A roadmap to future testing of the hypothesis is presented. We compare the oceanic vent with land-based pool scenarios for an origin of life and explore their implications for subsequent evolution to multicellular life such as plants. We conclude by utilizing the hypothesis to posit where life might also have emerged in habitats such as Mars or Saturn's icy moon Enceladus. Key Words: Origin of life-Prebiotic chemistry-Hydrothermal systems-Protocells-Progenotes-Microbial communities. Astrobiology 20, 429-452. ''To postulate one fortuitously catalyzed reaction, perhaps catalyzed by a metal ion, might be reasonable, but to postulate a suite of them is to appeal to magic.''

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Section: The Central Role Of Cyclingmentioning

confidence: 99%

The Hot Spring Hypothesis for an Origin of Life

2020

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“…One example is the requirement for wet-dry cycles for polymerization, mostly discussed in the context of geothermal fields [180], even though wet-dry cycles can also be found in hydrothermal pores [181] and even at the water-air interface [20]. On another note, some propose that different geological settings could have created different biomolecules that were then able to meet in an unchanged chemical state in the location where cells ultimately emerged [182].…”

Section: The Geological Settingmentioning

confidence: 99%

The Future of Origin of Life Research: Bridging Decades-Old Divisions

Preiner

Asche

Becker

et al. 2020

Life

Self Cite

109

150

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Research on the origin of life is highly heterogeneous. After a peculiar historical development, it still includes strongly opposed views which potentially hinder progress. In the 1st Interdisciplinary Origin of Life Meeting, early-career researchers gathered to explore the commonalities between theories and approaches, critical divergence points, and expectations for the future. We find that even though classical approaches and theories—e.g., bottom-up and top-down, RNA world vs. metabolism-first—have been prevalent in origin of life research, they are ceasing to be mutually exclusive and they can and should feed integrating approaches. Here we focus on pressing questions and recent developments that bridge the classical disciplines and approaches, and highlight expectations for future endeavours in origin of life research.

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“…Moreover, in a water restricted environment such as the topmost layers of the air/ice interface, the bases would be more prone to base-stacking, enabling the correct base pairing with other free nucleotide that would be floating in the topmost part of the ice-QLL, where the water diffusivity is faster. 42 In addition, since the synthesis of building blocks for nucleotide synthesis has been shown to be plausible in prebiotic aqueous conditions, 14,[43][44] an immobilized and stretched out ssRNA on ice, as the one shown in Fig. 1b, could be more prone to polymerization and self-replication with free nucleotides diffusing in the ice-QLL than a compact arrangement in the absence of protein-assisted replicase.…”

Section: Discussionmentioning

confidence: 99%

Solvation and Stabilization of Single Strand RNA at the Air/ice Interface Support a Primordial RNA World on Ice

Gladich¹,

Berrens²,

Rowe³

et al. 2020

Preprint

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<div>Outstanding questions about the RNA world hypothesis for the emergence of life</div><div>on Earth concern the stability and self-replication of prebiotic aqueous RNA.</div><div>Recent experimental work has suggested that solid substrates and low</div><div>temperatures could help resolve these issues. Here, we use classical molecular</div><div>dynamics simulations to explore the possibility that the substrate is ice itself. We</div><div>find that at -20 C, a quasi-liquid layer at the air/ice interface solvates a short (8-</div><div>nucleotide) RNA strand such that phosphate groups tend to anchor to specific</div><div>points of the underlying crystal lattice, lengthening the strand. Hydrophobic bases,</div><div>meanwhile, tend to migrate to the air/ice interface. Further, contacts between</div><div>solvent water and ribose 2-OH’ groups are found to occur less frequently for RNA</div><div>on ice than for aqueous RNA at the same temperature; this reduces the likelihood</div><div>of deprotonation of the 2-OH’ and its subsequent nucleophilic attack on the</div><div>phosphate diester. The implied enhanced resistance to hydrolysis, in turn, could</div><div>increase opportunities for polymerization and self-copying. These findings thus</div><div>offer the possibility of a role for an ancient RNA world on ice distinct from that</div><div>considered in extant elaborations of the RNA world hypothesis. This work is, to the</div><div>best of our knowledge, the first molecular dynamics study of RNA on ice</div>

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Unified prebiotically plausible synthesis of pyrimidine and purine RNA ribonucleotides

Cited by 228 publications

References 51 publications

The Hot Spring Hypothesis for an Origin of Life

The Hot Spring Hypothesis for an Origin of Life

The Future of Origin of Life Research: Bridging Decades-Old Divisions

Solvation and Stabilization of Single Strand RNA at the Air/ice Interface Support a Primordial RNA World on Ice

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