Astrobiology

Prebiotic chemistry for the origin of life requires a high degree of chemical and mineralogical complexity with the potential for multiple reactions under differing physico-chemical conditions. This includes processes that can promote the condensation reactions required to form polymers and the mechanisms to concentrate trace elements that can catalyze polymerization reactions. Competing hypotheses for favorable settings for life to emerge include submerged ocean hydrothermal vents and subaerial, terrestrial hot spring fields. A key challenge for permanently submerged hydrothermal vents is the inevitable dilution that occurs when fluids are ejected from deep-sea hydrothermal vents into a relatively uniform oceanic reservoir, meaning that whatever geochemical complexity that may have developed in the subsurface conduits of such systems is rapidly lost. Open water systems also lack the ability to form polymers and concentrate the trace elements required to catalyze polymerization reactions. Terrestrial hot spring environments experience wet–dry cycling, concentrate elements through multiple processes, and can have a range of pH values, yet they are regarded by some as unfavorable sites because they are too hot (the tar problem) and typically portrayed as individual, relatively static pools (e.g., Darwin’s “Warm Little Pond”). Here, we illustrate how the terrestrial hot spring field of the Taupō Volcanic Zone (TVZ) of New Zealand is much more dynamic and geochemically diverse than generally considered due to the many closely located pools with widely variable physico-chemical attributes that mix components at a variety of scales, creating a level of geochemical complexity unmatched elsewhere on Earth. The tens to thousands of diverse surface pools of the TVZ are characterized by wet–dry cycling and multiple mechanisms that can concentrate trace elements and mix fluids of very different composition that result in geochemical variability as well as mineral precipitation that can enhance the preservation of biosignatures.

The hot spring hypothesis for the origin of life proposes that naturally occurring wet–dry cycles in small bodies of water could have driven condensation reactions on prebiotic Earth. Mononucleotides exposed to wet–dry cycles in the laboratory have been shown to generate RNA oligomers. We tested whether similar reactions occur after wet–dry cycling in the laboratory of mononucleotides mixed with natural hot spring waters. Nucleotide solutions were prepared in the laboratory with effluent samples collected from hot springs of the Seltún (SE) and Hveradalir (HV) geothermal areas in Iceland. Sixteen wet–dry cycles with water collected from SE resulted in degradation of adenosine-5′-monophosphoric acid (95%), uridine 5′-monophosphate (63%) mononucleotides, while four wet–dry cycles were enough to destroy around 90% of both A10 and U10; thus, they displayed uniquely destructive properties for both purine and pyrimidine bases. Meanwhile, mononucleotides suspended in water collected from the HV hot spring were as stable as in nuclease-free water. Exposure of these solutions to wet–dry cycles also resulted in the synthesis of uridine dimers, cyclic mononucleotides, and other promising macromolecules.

High concentrations have long been thought to be important in prebiotic chemistry as they offer a way to circumvent a lack of available enzymatic catalysis to overcome kinetic barriers. Here, we argue that fluxes and timescales are also of critical importance. Fluxes and timescales determine, in part, whether an environment can achieve high concentrations of reactants and, in particular, place a critical constraint on whether high concentrations of product molecules can be maintained. We focus on closed basin lakes, which offer a viable way to concentrate molecules relative to background sources under benign conditions. From the perspective of P, HCN and its derivatives, and S, these systems may yield competitively high concentrations of reactants. Nonetheless, closed basin lakes often have limited fluxes of reactants, which places tight constraints on the concentrations of product molecules that can be maintained at steady state. In conjunction with experimentally measured reaction kinetics, an opportunity exists to discriminate between the plausibility of environments on the basis of their simulated ability to generate desired concentrations of products over relevant timescales. Crucially, to make such an evaluation is extremely difficult to do with confidence without quantitatively dealing with fluxes and timescales. Therefore, future work should routinely and systematically consider these aspects alongside molecule concentrations in environmental systems of interest and in experiments.

Solid surfaces have long been considered catalysts in prebiotic chemistry, yet their physical energy has rarely been explored as a driver of protocell assembly. This opinion article highlights recent experimental advances demonstrating that oxide minerals, Hadean Earth analogs, and martian meteorite specimens autonomously promote the assembly and transformation of lipid protocells without chemical catalysis. Surface-adhered compartments form mechanically resilient protocell colonies, nanotube-connected protocell networks enabling direct molecular transport, and flat protocells with spontaneous fusion and compositional diversification—capabilities absent in cell-sized free-floating vesicles. Extending these findings to extraterrestrial materials, new results indicate that micrometeorites, with their freshly generated, rough, and porous surfaces produced during atmospheric entry, efficiently nucleate protocell assembly. Given the continuous global influx of micrometeorites and growing astrobiological evidence of organics in cosmic dust, I propose that micrometeorites represent previously underappreciated initiators of protocell development, linking early Earth environments with contemporary planetary science and the search for life elsewhere.

Evolution on Earth often follows unpredictable pathways for the emergence of new species that are dependent upon the environment. Therefore, we can assume that the chemical origins of life and Darwinian evolution began with processes that are not apparent today. In this review, we highlight recent progress toward elucidating such pathways and mechanisms that led to the emergence of life-like behavior in prebiotically plausible chemical systems. To this end, we focus on the growing and dividing of protocells that encapsulated genetic materials and the ways in which functional protocells could have adapted to their environment by forming a rudimentary metabolism out of prebiotic chemistry. We highlight the importance of genotype-to-phenotype coupling and possible cooperative or competitive pathways for evolutionary mechanisms to build upon. We consider coacervation by liquid–liquid phase separation as an emerging crucial element and argue that in order to study a system’s chemistry at the onset of Darwinian evolution, we must involve the protocellular populations early on. By examining and drawing analogies from the physical and chemical dynamics that are at play in extant life, we provide a perspective on how the differences between nonliving and living entities on early Earth may have faded away gradually.

The original conditions from which primitive life emerged on the early Earth were likely to be dilute mixtures of organic compounds in aqueous solutions. A significant challenge for origins of life research is to discover the reactions that allowed such mixtures to become increasingly complex with products such as polymers that had structural and functional properties related to biology. The chances are low that potential reactants could find one another in dilute solutions composed of thousands of different molecular species. To improve the probability of such encounters, we have investigated a novel condition that both concentrates and organizes potential reactants and encapsulates polymeric products to form protocells. The condition involves a source of freshwater that falls as rainfall precipitation on land masses such as volcanic islands. The water dissolves exogenously and endogenously available organic compounds and feeds into hydrothermal fields where the solutions undergo cycles of evaporation and rehydration, a process easily observed today. Most researchers would agree that monomers such as amino acids and nucleotides would be present in the mixture, but less attention has been paid to the self-assembly of amphiphilic compounds that are also essential components of widely studied protocells. Here, we hypothesize how a closely related medium––multilamellar lipid–polymer (LP) matrices exposed to wet–dry cycles––can act as a progenitor and drive three essential processes: concentration of monomers, polymerization by synthesis of ester and peptide bonds, and promotion of interactions between peptides and nucleotide oligomers. We propose that such matrices represent “combinatorial engines” that can generate otherwise improbable functional complexes. After characterizing the sources of organics, the geochemical settings, and energetic environments in which such an LP progenitor can assemble, we present a conceptual model system that informs both chemical and computational experimental approaches to test this hypothesis.

The three signature structures of cells are membranes, proteins, and nucleic acids. These structures differ markedly in their composition, so how did they first come together in one unit? And how were peptides and oligonucleotides with functions benefiting the unit selected from random sequences? I review evidence for the following scheme: The first membranes were composed of fatty acids that self-assembled in shallow bodies of fresh water into dynamic, metastable vesicles. The vesicles encapsulated peptides and oligonucleotides during cycles of dehydration and rehydration. Alternatively, polymer formation from membrane-associated monomers yielded peptide and oligonucleotide-containing vesicles. In either case, the polymer-bearing vesicles then became enriched for specific polymers due to the dynamic character of fatty acid membranes. Vesicles bearing peptides that increased vesicle stability and growth would have increased in frequency. Vesicles bearing oligonucleotides that increased the concentration of beneficial peptides would have been further favored. Complementary oligonucleotides could have stabilized peptides and reduced their diffusion out of the vesicles. They could also have directed de novo, templated peptide synthesis, which would have opened the path to the generation of novel peptides.

In addition to being delivered via exogenous means (e.g., chondritic meteorites and comets), amino acids are hypothesized to have been present on early Earth via Urey–Miller-type abiotic processes. They conceivably coexisted in the primordial soup with nucleotides/RNA, amphiphiles and other co-solutes, highlighting the importance of characterizing how they would have influenced relevant prebiotic processes. In previous studies, amino acids have been shown to interact with protocellular moieties and affect nucleotide oligomerization. Nonetheless, the outcome of such interactions on templated-RNA replication, and on the physicochemical properties of protocells made of single-chain amphiphiles, is largely unknown. In this work, we characterize the role of amino acids as crucial prebiotic co-solutes in RNA copying chemistry. Additionally, we show how amino acids can promote the self-assembly of fatty acid vesicles under suboptimal pH conditions. Overall, our results show that amino acids influence both information copying and compartmentalization, underscoring their importance in shaping the molecular pathways crucial to life’s origin. In all, this study highlights how interactions between early biomolecular systems would have affected their co-evolution, thus setting the stage for the transition of chemistry to biology on early Earth.

The emergence of protocells, membranous compartments with encapsulated genetic material, was a crucial step in life’s origin and evolution. The hot spring hypothesis for the origin of life suggests that protocells with the capacity to encapsulate organic matter could have formed in hot spring pools during wet–dry (WD) cycling of hydrothermal fluids. Previous investigations have focused on mimicking WD cycles within a single pool, which precludes simulation of many hydrothermal field conditions, such as different mineralogies and variable temperature, pH, and water flow within and between multiple hot spring pools. Here, we present a modular 3D-printed hydrothermal field simulator that mimics many more aspects of the complex nature of hot spring fields by controlling the temperature, pH, and mineralogical variability of a series of linked pools. Furthermore, the pools can be programmed to experience fluid mixing between proximal pools and periodic WD cycling events. Results with the prototype hot spring field design demonstrate the ability to spontaneously form lipid vesicles that encapsulate organic matter within membranous compartments comprised of decanoic acid:decanol (4:1) or the phospholipids POPC:POPG (1:1). We observed that the vesicles formed during multiple WD cycles in the simulator pools displayed variation in their size distribution and differences in the number of membrane layers. Cargo encapsulation was favored in giant unilamellar vesicles and oligolamellar vesicles. Overall, the hot spring simulator offers a novel and customizable approach for studying multiple processes within hydrothermal field dynamics that include prebiotic chemical reactions, mineral surface catalysis, and the complexities of fluid mixing between proximal hot spring pools.

In future years, it seems likely that someone will claim they have discovered a process that allows a mixture of simple molecules to assemble into structures and systems with the fundamental properties of life. A useful exercise for researchers is to imagine what those properties might be and then design experiments to test ideas about how those properties could emerge on early Earth and other habitable planets. A variety of polymers play key roles in living systems, and we now have powerful analytical tools to analyze their structure and functions. One of these tools is the ability to determine base sequences of nucleic acids by gel electrophoresis, which led to the publication of the human genome in 2001 by the International Human Genome Sequencing Consortium. Another is nanopore sequencing, which has the unique ability to sequence not just fragments from a purified source of DNA but also individual molecules in mixed populations of nucleic acid polymers. Here, I will describe how we are using nanopore sequencing to explore processes by which nucleic acids could have emerged on early Earth 4 billion years ago, before life began.

This article provides a discussion of the scientific, intellectual, and ideological frameworks that influenced Oparin’s formulation of the heterotrophic theory of the origin of life. Based on a Darwinian perspective, Oparin rejected the generally accepted idea that the first entities were photosynthetic microbes. He proposed instead that life had emerged through a gradual, stepwise, non-teleological process of prebiotic evolution that started with the abiotic synthesis and accumulation of organic compounds on primitive Earth. Influenced by Haeckel’s and Timiriazev’s evolutionary ideas and by biochemical oxidation processes proposed by Bakh, Oparin concluded that the first organisms were anaerobic heterotrophs that had evolved from colloidal aggregates such as gels and coacervate-like systems. In sharp contrast to proposals that explained the origin of life with the chance appearance of viruses or living molecules, Oparin’s theory connected the emergence of fermentative cells as the first life-forms with the early evolution of Earth. The construction of a stepwise, slow evolution of different stages suggested by Oparin with colloids and coacervate as models of precellular evolution separated the biochemical and chemical origin of life from the idea of spontaneous generation and led to the development of a multi- and interdisciplinary research program.