Experimentally Testing Origin of Life Hypotheses in the Laboratory, at Field Analogs and Computationally

A topical collection in Life (ISSN 2075-1729). This collection belongs to the section "Origin of Life".

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Collection Editor
1. Department of Biomolecular Engineering, University of California, Santa Cruz, CA 95064, USA
2. BIOTA Institute, Boulder Creek, CA 95006, USA
Interests: origins of life; nonenzymatic polymerization; lipid biophysics; astrobiology; biosignature detection; Archean geology; space mission design; computational simulation
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Topical Collection Information

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Dear Colleagues,

In the past three decades, research on the question of how and where the origin of life (OoL) might have occurred on Earth some four billion years ago has made great strides. Perhaps the most significant is the emergence of a number of alternative hypotheses that can be subject to experimental testing. Researchers are now focusing their attention on several geological settings that could support key prebiotic chemical processes in two of the leading OoL hypotheses: in salt water at hydrothermal vents in the ocean or in cycling fresh water hydrothermal pools on land. In addition, a number of other venues and scenarios have been proposed and are being investigated. Simultaneously, work in computer simulation and developments from emergent phenomena in complex systems have provided insight into the basic principles that might be required in abiogenesis. Finally, life detection missions to Mars and the icy moons of Jupiter and Saturn as well as the detection of biosignatures on exoplanets have intensified interest in the conditions and settings in which life can begin.

We therefore find ourselves with much more solid scientific footing to proceed with an accelerated program of testing of OoL hypotheses at the beginning of the 2020s, both in clean, laboratory settings and in field sites, which are analogs for early Earth, Mars, or water worlds. Equipment for use in the laboratory and the field has enabled a new generation of researchers to truly “push the limits” in testing OoL scenarios. In a 21st-century version of the famous Miller–Urey experiments, planetary atmospheres, and mineral surfaces can now be emulated inside chambers, and laboratory-based cycling hot spring simulators are being built by groups. Recent issues of the journal Astrobiology have focused on hot springs as hypothesized sites for the origin of life (Damer and Deamer, 2020), while other groups have advanced hypotheses and the in-laboratory testing of oceanic vent settings (Barge and White, 2017).

To guide authors, at the 2017 Astrobiology Science Meeting, the following language was developed and adopted to describe a crucial experiment (per Platt, 1964), which can be applied to test any origin of life hypothesis: Confirm or falsify a non-enzymatic process by which catalytic and replicating systems of polymers are produced under plausible prebiotic conditions that also support cycles of combinatorial selection in which encapsulated sets of these polymers emerge and begin to evolve.

This language can be used as a template for OoL experiments to directly test hypothesized scenarios. There are also a number of ancillary experiments, which can provide valuable insights into problems that do not meet the criteria of the crucial experiment. Experiments might employ inorganic or other compounds not deemed plausibly present on the prebiotic Earth.  Experiments can also be carried out with the tools of synthetic biology to design minimal protocells or progenotes. These experiments can “jump the queue” and shed light on the challenges and probabilities of informational or catalytic functional polymers arising from an initial pool of random sequences. In addition, computer simulations of abstract characteristics of self-maintaining and replicating chemical systems can provide guidance to experimenters.

Topic areas for this Topical Collection include:

  • Meteoritic, atmospheric, hydrothermal, and mineral-sourced material contributions to prebiotic chemical systems;
  • The non-enzymatic polymerization of RNA-like, DNA-like, and proto-peptides through wet–dry cycling, mineral interaction, and other methodologies;
  • Sources of lipids and mechanisms for the membranous encapsulation of polymers to form protocells;
  • Studies of polymer–membrane colocalized systems as the initial landscape for a quasi-biological world;
  • Proposals, models, and experiments demonstrating mechanisms to replicate systems encoding heritable traits;
  • Synthetic minimal cells and protocells;
  • Protocell to protocell competition and cooperation;
  • Non-membranous forms of encapsulation: coacervates, emulsion droplets of hydrocarbons, oligonucleotide origami, mineral surfaces, rock pores, and mineral gels;
  • Non-traditional solvents and “weird life” origins scenarios;
  • Testing of the RNA-world hypothesis through in vitro evolution;
  • Testing of the hot spring hypothesis through protocell self-assembly and combinatorial selection;
  • Testing the submarine vent hypothesis through carbon fixation of monomers within pressure vessels and microfluidics simulations of vents;
  • Models and experiments for the first energy-driven metabolic circuits including autocatalytic sets;
  • The spontaneous emergence of reaction networks driven by radiolytic and other energy sources;
  • Testing models for a proto-ribosome and distributed mechanisms enabling translation in silico and in vitro;
  • Models for complex emergent systems as applied to OoL;
  • Computational simulations of rates of polymer formation and degradation in monomer soups;
  • Analytical techniques and tools to analyze products of OoL experiments including: microscopy, gels, HPLC, nuclear and X-ray imaging, AFM imaging;
  • Automating and scaling throughput of synthetic protocell experiments;
  • Portable devices to enable OoL experiments in the field;
  • Bringing the hot spring into the laboratory: complex benchtop devices;
  • Early life rock record and its application to understanding the period of life's emergence (the "Progenean");
  • OoL-informed biosignature detection for surface missions on Mars;
  • OoL-informed biosignature detection in plumes from icy moons;
  • OoL-informed atmospheric biosignature detection on exoplanets.

The journal is pleased to be publishing its first Topical Collection dedicated to testing origin of life hypotheses not only in the traditional laboratory setting, but also at field analog sites.

This Topical Collection of Life welcomes the submission of unpublished original work or reviews on previous work. We plan to receive submissions for a nine-month period from 15 Sept 2020 to 15 July 2021.

References

Damer, B.; Deamer, D. The Hot Spring Hypothesis for an Origin of Life. Astrobiology 2020, 429–452. http://doi.org/10.1089/ast.2019.2045
Barge, L. and White, L. Experimentally Testing Hydrothermal Vent Origin of Life on Enceladus and Other Icy/Ocean Worlds. Astrobiology 2017, 17, 820-833. http://doi.org/10.1089/ast.2016.1633 
Platt, J.R. Strong Inference. Science 1964, 146, 347–353.

Dr. Bruce Damer
Collection Editor

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Keywords

  • origins of life
  • membrane biophysics
  • meteoritic, atmospheric and geochemical delivery of organics for prebiotic chemistry
  • disequilibria and away-from-equilibrium chemical systems
  • carbon fixation synthesis of organics
  • nonenzymatic polymerization
  • combinatorial selection
  • molecular evolution
  • the progenote
  • minimum viable synthetic protocells/cells
  • computational tools in the origin of life
  • stromatolites and microfossils
  • biosignature detection for space missions and exoplanet studies
  • astrobiology

Published Papers (9 papers)

2024

Jump to: 2023, 2022, 2021, 2020

28 pages, 17007 KiB  
Article
Could Life Have Started on Mars? Planetary Conditions That Assemble and Destroy Protocells
by Francesca C. A. Cary, David W. Deamer, Bruce F. Damer, Sarah A. Fagents, Kathleen C. Ruttenberg and Stuart P. Donachie
Life 2024, 14(3), 415; https://doi.org/10.3390/life14030415 - 20 Mar 2024
Viewed by 1447
Abstract
Early Mars was likely habitable, but could life actually have started there? While cellular life emerged from prebiotic chemistry through a pre-Darwinian selection process relevant to both Earth and Mars, each planet posed unique selection ‘hurdles’ to this process. We focus on drivers [...] Read more.
Early Mars was likely habitable, but could life actually have started there? While cellular life emerged from prebiotic chemistry through a pre-Darwinian selection process relevant to both Earth and Mars, each planet posed unique selection ‘hurdles’ to this process. We focus on drivers of selection in prebiotic chemistry generic to Earth-like worlds and specific to Mars, such as an iron-rich surface. Iron, calcium, and magnesium cations are abundant in hydrothermal settings on Earth and Mars, a promising environment for an origin of life. We investigated the impact of cations on the stability and disruption of different primitive cell membranes under different pH conditions. The relative destabilizing effect of cations on membranes observed in this study is Ca2+ > Fe2+ > Mg2+. Cation concentrations in Earth systems today are too low to disrupt primitive membranes, but on Mars concentrations could have been elevated enough to disrupt membranes during surface dehydration. Membranes and RNA interact during dehydration–rehydration cycles to mutually stabilize each other in cation-rich solutions, and optimal membrane composition can be ‘selected’ by environmental factors such as pH and cation concentrations. We introduce an approach that considers how life may have evolved differently under the Martian planetary conditions and selective pressures. Full article
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2023

Jump to: 2024, 2022, 2021, 2020

17 pages, 2847 KiB  
Article
Formation of Amino Acids and Carboxylic Acids in Weakly Reducing Planetary Atmospheres by Solar Energetic Particles from the Young Sun
by Kensei Kobayashi, Jun-ichi Ise, Ryohei Aoki, Miei Kinoshita, Koki Naito, Takumi Udo, Bhagawati Kunwar, Jun-ichi Takahashi, Hiromi Shibata, Hajime Mita, Hitoshi Fukuda, Yoshiyuki Oguri, Kimitaka Kawamura, Yoko Kebukawa and Vladimir S. Airapetian
Life 2023, 13(5), 1103; https://doi.org/10.3390/life13051103 - 28 Apr 2023
Cited by 6 | Viewed by 16671
Abstract
Life most likely started during the Hadean Eon; however, the environmental conditions which contributed to the complexity of its chemistry are poorly known. A better understanding of various environmental conditions, including global (heliospheric) and local (atmospheric, surface, and oceanic), along with the internal [...] Read more.
Life most likely started during the Hadean Eon; however, the environmental conditions which contributed to the complexity of its chemistry are poorly known. A better understanding of various environmental conditions, including global (heliospheric) and local (atmospheric, surface, and oceanic), along with the internal dynamic conditions of the early Earth, are required to understand the onset of abiogenesis. Herein, we examine the contributions of galactic cosmic rays (GCRs) and solar energetic particles (SEPs) associated with superflares from the young Sun to the formation of amino acids and carboxylic acids in weakly reduced gas mixtures representing the early Earth’s atmosphere. We also compare the products with those introduced by lightning events and solar ultraviolet light (UV). In a series of laboratory experiments, we detected and characterized the formation of amino acids and carboxylic acids via proton irradiation of a mixture of carbon dioxide, methane, nitrogen, and water in various mixing ratios. These experiments show the detection of amino acids after acid hydrolysis when 0.5% (v/v) of initial methane was introduced to the gas mixture. In the set of experiments with spark discharges (simulation of lightning flashes) performed for the same gas mixture, we found that at least 15% methane was required to detect the formation of amino acids, and no amino acids were detected in experiments via UV irradiation, even when 50% methane was used. Carboxylic acids were formed in non-reducing gas mixtures (0% methane) by proton irradiation and spark discharges. Hence, we suggest that GCRs and SEP events from the young Sun represent the most effective energy sources for the prebiotic formation of biologically important organic compounds from weakly reducing atmospheres. Since the energy flux of space weather, which generated frequent SEPs from the young Sun in the first 600 million years after the birth of the solar system, was expected to be much greater than that of GCRs, we conclude that SEP-driven energetic protons are the most promising energy sources for the prebiotic production of bioorganic compounds in the atmosphere of the Hadean Earth. Full article
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2022

Jump to: 2024, 2023, 2021, 2020

19 pages, 3587 KiB  
Article
A Mutation Threshold for Cooperative Takeover
by Alexandre Champagne-Ruel and Paul Charbonneau
Life 2022, 12(2), 254; https://doi.org/10.3390/life12020254 - 08 Feb 2022
Cited by 1 | Viewed by 2943
Abstract
One of the leading theories for the origin of life includes the hypothesis according to which life would have evolved as cooperative networks of molecules. Explaining cooperation—and particularly, its emergence in favoring the evolution of life-bearing molecules—is thus a key element in describing [...] Read more.
One of the leading theories for the origin of life includes the hypothesis according to which life would have evolved as cooperative networks of molecules. Explaining cooperation—and particularly, its emergence in favoring the evolution of life-bearing molecules—is thus a key element in describing the transition from nonlife to life. Using agent-based modeling of the iterated prisoner’s dilemma, we investigate the emergence of cooperative behavior in a stochastic and spatially extended setting and characterize the effects of inheritance and variability. We demonstrate that there is a mutation threshold above which cooperation is—counterintuitively—selected, which drives a dramatic and robust cooperative takeover of the whole system sustained consistently up to the error catastrophe, in a manner reminiscent of typical phase transition phenomena in statistical physics. Moreover, our results also imply that one of the simplest conditional cooperative strategies, “Tit-for-Tat”, plays a key role in the emergence of cooperative behavior required for the origin of life. Full article
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2021

Jump to: 2024, 2023, 2022, 2020

40 pages, 8513 KiB  
Article
Hitting Times of Some Critical Events in RNA Origins of Life
by Caleb Deen Bastian and Hershel Rabitz
Life 2021, 11(12), 1419; https://doi.org/10.3390/life11121419 - 17 Dec 2021
Viewed by 2319
Abstract
Can a replicase be found in the vast sequence space by random drift? We partially answer this question through a proof-of-concept study of the times of occurrence (hitting times) of some critical events in the origins of life for low-dimensional RNA sequences using [...] Read more.
Can a replicase be found in the vast sequence space by random drift? We partially answer this question through a proof-of-concept study of the times of occurrence (hitting times) of some critical events in the origins of life for low-dimensional RNA sequences using a mathematical model and stochastic simulation studies from Python software. We parameterize fitness and similarity landscapes for polymerases and study a replicating population of sequences (randomly) participating in template-directed polymerization. Under the ansatz of localization where sequence proximity correlates with spatial proximity of sequences, we find that, for a replicating population of sequences, the hitting and establishment of a high-fidelity replicator depends critically on the polymerase fitness and sequence (spatial) similarity landscapes and on sequence dimension. Probability of hitting is dominated by landscape curvature, whereas hitting time is dominated by sequence dimension. Surface chemistries, compartmentalization, and decay increase hitting times. Compartmentalization by vesicles reveals a trade-off between vesicle formation rate and replicative mass, suggesting that compartmentalization is necessary to ensure sufficient concentration of precursors. Metabolism is thought to be necessary to replication by supplying precursors of nucleobase synthesis. We suggest that the dynamics of the search for a high-fidelity replicase evolved mostly during the final period and, upon hitting, would have been followed by genomic adaptation of genes and to compartmentalization and metabolism, effecting degree-of-freedom gains of replication channel control over domain and state to ensure the fidelity and safe operations of the primordial genetic communication system of life. Full article
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16 pages, 1074 KiB  
Article
Computational Analysis of a Prebiotic Amino Acid Synthesis with Reference to Extant Codon–Amino Acid Relationships
by Tolga Yaman and Jeremy N. Harvey
Life 2021, 11(12), 1343; https://doi.org/10.3390/life11121343 - 04 Dec 2021
Cited by 2 | Viewed by 2147
Abstract
Novel density functional theory calculations are presented regarding a mechanism for prebiotic amino acid synthesis from alpha-keto acids that was suggested to happen via catalysis by dinucleotide species. Our results were analysed with comparison to the original hypothesis (Copley et al., PNAS, [...] Read more.
Novel density functional theory calculations are presented regarding a mechanism for prebiotic amino acid synthesis from alpha-keto acids that was suggested to happen via catalysis by dinucleotide species. Our results were analysed with comparison to the original hypothesis (Copley et al., PNAS, 2005, 102, 4442–4447). It was shown that the keto acid–dinucleotide hypothesis for possible prebiotic amino acid synthesis was plausible based on an initial computational analysis, and details of the structures for the intermediates and transition states showed that there was wide scope for interactions between the keto acid and dinucleotide moieties that could affect the free energy profiles and lead to the required proto-metabolic selectivity. Full article
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15 pages, 3302 KiB  
Article
Scum of the Earth: A Hypothesis for Prebiotic Multi-Compartmentalised Environments
by Craig Robert Walton and Oliver Shorttle
Life 2021, 11(9), 976; https://doi.org/10.3390/life11090976 - 16 Sep 2021
Cited by 4 | Viewed by 2982
Abstract
Compartmentalisation by bioenergetic membranes is a universal feature of life. The eventual compartmentalisation of prebiotic systems is therefore often argued to comprise a key step during the origin of life. Compartments may have been active participants in prebiotic chemistry, concentrating and spatially organising [...] Read more.
Compartmentalisation by bioenergetic membranes is a universal feature of life. The eventual compartmentalisation of prebiotic systems is therefore often argued to comprise a key step during the origin of life. Compartments may have been active participants in prebiotic chemistry, concentrating and spatially organising key reactants. However, most prebiotically plausible compartments are leaky or unstable, limiting their utility. Here, we develop a new hypothesis for an origin of life environment that capitalises upon, and mitigates the limitations of, prebiotic compartments: multi-compartmentalised layers in the near surface environment—a ’scum’. Scum-type environments benefit from many of the same ensemble-based advantages as microbial biofilms. In particular, scum layers mediate diffusion with the wider environments, favouring preservation and sharing of early informational molecules, along with the selective concentration of compatible prebiotic compounds. Biofilms are among the earliest traces imprinted by life in the rock record: we contend that prebiotic equivalents of these environments deserve future experimental investigation. Full article
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1 pages, 135 KiB  
Addendum
Addendum: Deamer, D. Where Did Life Begin? Testing Ideas in Prebiotic Analogue Conditions. Life 2021, 11, 134
by David Deamer
Life 2021, 11(7), 613; https://doi.org/10.3390/life11070613 - 25 Jun 2021
Viewed by 1318
Abstract
The author wishes to add the following information to the acknowledgements section of his paper published in Life [...] Full article
11 pages, 4961 KiB  
Essay
Where Did Life Begin? Testing Ideas in Prebiotic Analogue Conditions
by David Deamer
Life 2021, 11(2), 134; https://doi.org/10.3390/life11020134 - 10 Feb 2021
Cited by 18 | Viewed by 4831
Abstract
Publications related to the origin of life are mostly products of laboratory research and have the tacit assumption that the same reactions would have been possible on the early Earth some 4 billion years ago. Can this assumption be tested? We cannot go [...] Read more.
Publications related to the origin of life are mostly products of laboratory research and have the tacit assumption that the same reactions would have been possible on the early Earth some 4 billion years ago. Can this assumption be tested? We cannot go back in time, but we are able to venture out of the laboratory and perform experiments in natural conditions that are presumably analogous to the prebiotic environment. This brief review describes initial attempts to undertake such studies and some of the lessons we have learned. Full article
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2020

Jump to: 2024, 2023, 2022, 2021

11 pages, 4206 KiB  
Article
AFM Images of Viroid-Sized Rings That Self-Assemble from Mononucleotides through Wet–Dry Cycling: Implications for the Origin of Life
by Tue Hassenkam, Bruce Damer, Gabriel Mednick and David Deamer
Life 2020, 10(12), 321; https://doi.org/10.3390/life10120321 - 30 Nov 2020
Cited by 17 | Viewed by 2876
Abstract
It is possible that early life relied on RNA polymers that served as ribozyme-like catalysts and for storing genetic information. The source of such polymers is uncertain, but previous investigations reported that wet–dry cycles simulating prebiotic hot springs provide sufficient energy to drive [...] Read more.
It is possible that early life relied on RNA polymers that served as ribozyme-like catalysts and for storing genetic information. The source of such polymers is uncertain, but previous investigations reported that wet–dry cycles simulating prebiotic hot springs provide sufficient energy to drive condensation reactions of mononucleotides to form oligomers. The aim of the study reported here was to visualize the products by atomic force microscopy. In addition to globular oligomers, ring-like structures ranging from 10–200 nm in diameter, with an average around 30–40 nm, were abundant, particularly when nucleotides capable of base pairing were present. The thickness of the rings was consistent with single stranded products, but some had thicknesses indicating base pair stacking. Others had more complex structures in the form of short polymer attachments and pairing of rings. These observations suggest the possibility that base-pairing may promote polymerization during wet–dry cycling followed by solvation of the rings. We conclude that RNA-like rings and structures could have been synthesized non-enzymatically on the prebiotic Earth, with sizes sufficient to fold into ribozymes and genetic molecules required for life to begin. Full article
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