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Co-polymerization of glycol nucleic acid monomers with dicarboxylic acid linkers under plausible early Earth dry-down scenario conditions.

Nucleic acid segregation and compartmentalization were likely essential functions that primitive compartment systems resolved during evolution. Recently, polyester microdroplets generated from dehydration synthesis of various α-hydroxy acids (αHA) were suggested as potential primitive compartments. Some of these droplets can differentially segregate and compartmentalize organic dyes, proteins, and nucleic acids. However, the previously studied polyester microdroplets included limited αHA chemical diversity, which may not reflect the chemical diversity available in the primitive Earth environment. Here, we increased the chemical diversity of polyester microdroplet systems by combinatorially adding an αHA monomer with a basic side chain, 4-amino-2-hydroxybutyric acid (4a2h), which was incorporated with different ratios of other αHAs containing uncharged side chains to form combinatorial heteropolyesters via dehydration synthesis. Incorporation of 4a2h in the polymers resulted in the assembly of some polyester microdroplets able to segregate fluorescent RNA or potentially acquire intrinsic fluorescent character, suggesting that minor modifications of polyester composition can significantly impact the functional properties of primitive compartments. This study suggests one process by which primitive chemical systems can increase diversity of compartment "phenotype" through simple modifications in their chemical composition.

The chemical space of prebiotic chemistry is extremely large, while extant biochemistry uses only a few thousand interconnected molecules. Here we discuss how the connection between these two regimes can be investigated, and explore major outstanding questions in the origin of life.

The 1953 Miller–Urey experiment was a ground-breaking attempt to understand stages in the origins of life on Earth. In the experiment, Stanley Miller added water and reduced gases to a sealed flask to simulate the primitive atmosphere and hydrosphere, then subjected the contents to an electric discharge to simulate atmospheric lightning. Miller's chemical analysis of the products revealed a number of amino acids used by modern organisms to construct coded proteins, suggesting these may then have been available for the construction of the first organisms. The experiment was inspired by both Oparin's early writings on the origins of life and Urey's conception of the primitive atmosphere. Since the publication of the original results, there has been considerable development in thinking regarding the nature of the primitive environment, as well as a proliferation of alternative, detailed models for the origins of life which do not necessarily hinge on the results of this kind of experiment. Nevertheless, while considerable uncertainty lingers regarding the primitive environment, the Miller–Urey experiment remains relevant to many modern origins of life models, and its impact on modern thinking regarding the origins of life cannot be overstated.

Carboxylation and decarboxylation are two fundamental classes of reactions that impact the cycling of carbon in and on Earth’s crust. These reactions play important roles in both long-term (primarily abiotic) and short-term (primarily biotic) carbon cycling. Long-term cycling is important in the subsurface and at subduction zones where organic carbon is decomposed and outgassed or recycled back to the mantle. Short-term reactions are driven by biology and have the ability to rapidly convert CO2 to biomass and vice versa. For instance, carboxylation is a critical reaction in primary production and metabolic pathways like photosynthesis in which sunlight provides energy to drive carbon fixation, whereas decarboxylation is a critical reaction in metabolic pathways like respiration and the tricarboxylic acid cycle. Early life and prebiotic chemistry on Earth likely relied heavily upon the abiotic synthesis of carboxylic acids. Over time, life has diversified (de)carboxylation reactions and incorporated them into many facets of cellular metabolism. Here we present a broad overview of the importance of carboxylation and decarboxylation reactions from both abiotic and biotic perspectives to highlight the importance of these reactions and compounds to planetary evolution.

“Prebiotic soup” often features in discussions of origins of life research, both as a theoretical concept when discussing abiological pathways to modern biochemical building blocks and, more recently, as a feedstock in prebiotic chemistry experiments focused on discovering emergent, systems-level processes such as polymerization, encapsulation, and evolution. However, until now, little systematic analysis has gone into the design of well-justified prebiotic mixtures, which are needed to facilitate experimental replicability and comparison among researchers. This paper explores principles that should be considered in choosing chemical mixtures for prebiotic chemistry experiments by reviewing the natural environmental conditions that might have created such mixtures and then suggests reasonable guidelines for designing recipes. We discuss both “assembled” mixtures, which are made by mixing reagent grade chemicals, and “synthesized” mixtures, which are generated directly from diversity-generating primary prebiotic syntheses. We discuss different practical concerns including how to navigate the tremendous uncertainty in the chemistry of the early Earth and how to balance the desire for using prebiotically realistic mixtures with experimental tractability and replicability. Examples of two assembled mixtures, one based on materials likely delivered by carbonaceous meteorites and one based on spark discharge synthesis, are presented to illustrate these challenges. We explore alternative procedures for making synthesized mixtures using recursive chemical reaction systems whose outputs attempt to mimic atmospheric and geochemical synthesis. Other experimental conditions such as pH and ionic strength are also considered. We argue that developing a handful of standardized prebiotic recipes may facilitate coordination among researchers and enable the identification of the most promising mechanisms by which complex prebiotic mixtures were “tamed” during the origin of life to give rise to key living processes such as self-propagation, information processing, and adaptive evolution. We end by advocating for the development of a public prebiotic chemistry database containing experimental methods (including soup recipes), results, and analytical pipelines for analyzing complex prebiotic mixtures.

Life uses a common set of 20 coded amino acids (CAAs) to construct proteins. This set was likely canonicalized during early evolution; before this, smaller amino acid sets were gradually expanded as new synthetic, proofreading and coding mechanisms became biologically available. Many possible subsets of the modern CAAs or other presently uncoded amino acids could have comprised the earlier sets. We explore the hypothesis that the CAAs were selectively fixed due to their unique adaptive chemical properties, which facilitate folding, catalysis, and solubility of proteins, and gave adaptive value to organisms able to encode them. Specifically, we studied in silico hypothetical CAA sets of 3–19 amino acids comprised of 1913 structurally diverse α-amino acids, exploring the adaptive value of their combined physicochemical properties relative to those of the modern CAA set. We find that even hypothetical sets containing modern CAA members are especially adaptive; it is difficult to find sets even among a large choice of alternatives that cover the chemical property space more amply. These results suggest that each time a CAA was discovered and embedded during evolution, it provided an adaptive value unusual among many alternatives, and each selective step may have helped bootstrap the developing set to include still more CAAs.

Compartmentalization was likely essential for primitive chemical systems during the emergence of life, both for preventing leakage of important components, i.e., genetic materials, and for enhancing chemical reactions. Although life as we know it uses lipid bilayer-based compartments, the diversity of prebiotic chemistry may have enabled primitive living systems to start from other types of boundary systems. Here, we demonstrate membraneless compartmentalization based on prebiotically available organic compounds, α-hydroxy acids (αHAs), which are generally coproduced along with α-amino acids in prebiotic settings. Facile polymerization of αHAs provides a model pathway for the assembly of combinatorially diverse primitive compartments on early Earth. We characterized membraneless microdroplets generated from homo- and heteropolyesters synthesized from drying solutions of αHAs endowed with various side chains. These compartments can preferentially and differentially segregate and compartmentalize fluorescent dyes and fluorescently tagged RNA, providing readily available compartments that could have facilitated chemical evolution by protecting, exchanging, and encapsulating primitive components. Protein function within and RNA function in the presence of certain droplets is also preserved, suggesting the potential relevance of such droplets to various origins of life models. As a lipid amphiphile can also assemble around certain droplets, this further shows the droplets’ potential compatibility with and scaffolding ability for nascent biomolecular systems that could have coexisted in complex chemical systems. These model compartments could have been more accessible in a “messy” prebiotic environment, enabling the localization of a variety of protometabolic and replication processes that could be subjected to further chemical evolution before the advent of the Last Universal Common Ancestor.

Searching for life in the Universe depends on unambiguously distinguishing biological features from background signals, which could take the form of chemical, morphological, or spectral signatures. The discovery and direct measurement of organic compounds unambiguously indicative of extraterrestrial (ET) life is a major goal of Solar System exploration. Biology processes matter and energy differently from abiological systems, and materials produced by biological systems may become enriched in planetary environments where biology is operative. However, ET biology might be composed of different components than terrestrial life. As ET sample return is difficult, in situ methods for identifying biology will be useful. Mass spectrometry (MS) is a potentially versatile life detection technique, which will be used to analyze numerous Solar System environments in the near future. We show here that simple algorithmic analysis of MS data from abiotic synthesis (natural and synthetic), microbial cells, and thermally processed biological materials (lab-grown organisms and petroleum) easily identifies relational organic compound distributions that distinguish pristine and aged biological and abiological materials, which likely can be attributed to the types of compounds these processes produce, as well as how they are formed and decompose. To our knowledge this is the first comprehensive demonstration of the utility of this analytical technique for the detection of biology. This method is independent of the detection of particular masses or molecular species samples may contain. This suggests a general method to agnostically detect evidence of biology using MS given a sufficiently strong signal in which the majority of the material in a sample has either a biological or abiological origin. Such metrics are also likely to be useful for studies of possible emergent living phenomena, and paleobiological samples.

Prebiotic chemists often study how modern biopolymers, e.g., peptides and nucleic acids, could have originated in the primitive environment, though most contemporary biomonomers don’t spontaneously oligomerize under mild conditions without activation or catalysis. However, life may not have originated using the same monomeric components that it does presently. There may be numerous non-biological (or “xenobiological”) monomer types that were prebiotically abundant and capable of facile oligomerization and self-assembly. Many modern biopolymers degrade abiotically preferentially via processes which produce thermodynamically stable ring structures, e.g. diketopiperazines in the case of proteins and 2′, 3′-cyclic nucleotide monophosphates in the case of RNA. This weakness is overcome in modern biological systems by kinetic control, but this need not have been the case for primitive systems. We explored here the oligomerization of a structurally diverse set of prebiotically plausible xenobiological monomers, which can hydrolytically interconvert between cyclic and acyclic forms, alone or in the presence of glycine under moderate temperature drying conditions. These monomers included various lactones, lactams and a thiolactone, which varied markedly in their stability, propensity to oligomerize and apparent modes of initiation, and the oligomeric products of some of these formed self-organized microscopic structures which may be relevant to protocell formation.

We model nitrogen (N) partitioning in the magma ocean stage and cycling between the surface and mantle through Earth's history, and suggest that N in the present-day mantle may be set by subduction before the development of the modern N cycle. Introduction: On present-day Earth, N cycling between the surface and mantle is largely controlled by biological N fixation and aerobic biological processing. Biological N fixation brings the majority of inorganic N into the modern N cycle. In the oceans, dissolved nitrate is the main form of nitrogen available for life, and dissimilatory denitrification leads to residual nitrate being kinetically enriched in 15N by ~6‰. The isotopically enriched nitrate is then reduced to ammonium and finally trapped in sediments (e.g., Stüeken al. 2016). Though secular subduction of 15N-rich sediments should cause 15N enrichment in the mantle, the mantle N sampled from mid-ocean ridge basalt (MORB) is rather depleted in 15N (~-5‰), which is known as the N isotopic disequilibrium. Previous studies hypothesized that N in the mantle is a primordial component (Cartingy & Marty, 2013; Labidi et al. 2020). In the primordial origin scenario, the isotopic disequilibrium is attributed to atmospheric escape, which enriched the atmosphere with 15N. Another study proposed a recycling origin scenario in which the N isotopic composition of sediments has changed over time (Marty & Dauphas, 2003). Neither of these scenarios has been modeled quantitatively. Here we test the different scenarios by using numerical models coupled with N isotopes. Methods: We developed two sets of models for the origin of observed mantle N isotopic composition: i) the primordial origin and ii) the recycling origin. The results are either accepted or rejected by the comparison to the amounts and isotopic compositions of N in contemporary surface reservoirs and mantle (Johnson & Goldblatt, 2015; Labidi et al. 2020). For the primordial origin scenario, we calculate N partitioning between the atmosphere and mantle upon magma ocean solidification by using a melt-trapping model (Hier-Majumder & Hirschmann, 2017) and the partitioning coefficients between minerals, silicate melt, and the atmosphere (Li et al. 2013; Dalou et al. 2017). We consider the range of oxygen fugacity relevant to Earth's formation. We also estimate the 15N-enrichment effect due to EUV-driven escape (Watson et al. 1981) and solar-wind pick-up (Lichtenegger et al. 2010) to see how much atmospheric N should be removed to reproduce ~+5‰ difference between the atmosphere and mantle. For the recycling origin scenario, we calculate secular N exchange between the surface reservoirs and mantle. Our model is based on that of Labidi et al. (2020). The isotopic fractionation between the atmosphere and subducting sediments is taken to be ~-9‰ and ~+6‰ before and after the Great Oxidation Event at 2.4 Ga, respectively, considering the change from abiotic fixation and anaerobic processing to biological fixation and aerobic processing. We fix the subduction and degassing fluxes on present-day Earth, and their power-law indices as a function of time as parameters. Bulk N partitioning and the isotopic difference between the reservoirs in the initial state are also treated as parameters. Figure 1: Nitrogen partitioning between the atmosphere and mantle at the time of magma ocean solidification (PAN = present-day atmospheric nitrogen). The range of the modeled mantle N content reflects the uncertainty in the oxygen fugacity of the magma ocean. Figure 2: Evolution of masses (left) and 15N/14N ratios (right) in the surface reservoirs (blue) and mantle (red). Curves show accepted models having different initial conditions and fluxes. Gray areas are the estimates for present-day surface reservoirs and mantle. Results: Because N is relatively insoluble in silicate melts, it is mostly partitioned into the atmosphere even when trapping in interstitial melts is considered (Figure 1). Partitioning N into the mantle as much as present-day leads to 100 times excess in PAL N. We found that the excess amount of N can be removed neither by EUV- nor solar-wind-induced loss without excessive 15N enrichment in the atmosphere. Impact erosion by the late veneer bombardment removes atmospheric N without isotopic fractionation up to ~10 bar (Sakuraba et al. 2019), but it may not be sufficient to remove all excess N in the atmosphere. Since the results of our partitioning model suggest that the primordial origin is unlikely, next we tested the recycling scenario in our N cycling model (Figure 2). In our successful runs, the mantle is initially depleted in N, and N in the present-day mantle is a result of higher net subduction flux on early Earth where sedimentary N is depleted in 15N due to abiotic N fixation and anaerobic N processing. The change to modern N cycle is visible in the kink in δ15N evolution, which may provide a way to test our model with evidence from geologic record. Discussion: We suggest that N partitioning between the surface and deep Earth may be set by subduction driven by plate tectonics and partially by biology. This also suggests that the difference of atmospheric N contents between Venus and Earth, the former of which has three times more N in the atmosphere, is caused by their long-term evolution rather than early formation and differentiation processes. Conclusions: We conclude that N in the present-day mantle may be set by subduction before the development of the modern N cycle. Further results for parameter survey and discussion on other geological and geochemical constraints will be shown in our presentation.

While tensions may lie between science and policy, we argue that dissemination and public engagement are key in alleviating those perceived tensions. Science being valued by society results in fact-based policy-making being demanded by constituents. Constituents’ demands will yield representatives who are familiar with the scientific process and research to inform policy decisions.

Continuous reaction networks, which do not rely on purification or timely additions of reagents, serve as models for chemical evolution and have been demonstrated for compounds thought to have played important roles for the origins of life such as amino acids, hydroxy acids, and sugars. Step-by-step chemical protocols for ribonucleotide synthesis are known, but demonstrating their synthesis in the context of continuous reaction networks remains a major challenge. Herein, compounds proposed to be important for prebiotic RNA synthesis, including glycolaldehyde, cyanamide, 2-aminooxazole, and 2-aminoimidazole, are generated from a continuous reaction network, starting from an aqueous mixture of NaCl, NH(4)Cl, phosphate, and HCN as the only carbon source. No well-timed addition of any other reagents is required. The reaction network is driven by a combination of γ radiolysis and dry-down. γ Radiolysis results in a complex mixture of organics, including the glycolaldehyde-derived glyceronitrile and cyanamide. This mixture is then dried down, generating free glycolaldehyde that then reacts with cyanamide/NH(3) to furnish a combination of 2-aminooxazole and 2-aminoimidazole. This continuous reaction network models how precursors for generating RNA and other classes of compounds may arise spontaneously from a complex mixture that originates from simple reagents.

Selective binding of aqueous-phase amino acids to mineral surfaces is regarded as a plausible first step in oligopeptide formation on early Earth. To clarify the strength and underlying mechanism of amino acid binding to pyrite surfaces, we measured the unbinding (pull-off) force of ten amino acids and two oligo-peptides from water-pyrite interfaces using atomic force microscopy (AFM). The most probable unbinding force could be described by a linearly increasing function with the size of the amino acid and a characteristic offset. A good correlation was obtained between the most probable unbinding force and the residue volume, surface area and polarizability of samples suggesting at least a partial contribution of van der Waals (vdW) forces, especially the London dispersion force. These results are useful in analysis of adhesion phenomena of amino acids in the given environmental settings such as in this work.

The chemistry occurring in the universe generates a huge variety of organic compounds abiotically. Significant progress has been made in understanding the types and distributions of these compounds...

We studied the radiolysis of a wide variety of N-heterocycles, including many of biological importance, and find that the majority are remarkably stable in the solid-state when subjected to large doses of ionizing gamma radiation from a 60Co source. Degradation of N-heterocycles as a function of dose rate and total dose was measured using high-performance liquid chromatography with UV detection. Many N-heterocycles show little degradation when γ-irradiated up to a total dose of ~1 MGy, which approximates hundreds of millions of years’ worth of radiation emitted in meteorite parent bodies due to slow radionuclide decay. Extrapolation of these results suggests that these N-heterocyclic compounds would be stable in dry parent bodies over solar system timescales. We suggest that the abundance of these N-heterocycles as measured presently in carbonaceous meteorites is largely reflective of their abundance at the time aqueous alteration stopped in their parent bodies and the absence of certain compounds in present-day samples is either due to the formation mechanisms or degradation which occurred during periods of aqueous alteration or thermal metamorphism.

Nitrogen is the major component of Earth's atmosphere and plays important roles in biochemistry. Biological systems have evolved a variety of mechanisms for fixing and recycling environmental nitrogen sources, which links them tightly with terrestrial nitrogen reservoirs. However, prior to the emergence of biology, all nitrogen cycling was abiological, and this cycling may have set the stage for the origin of life. It is of interest to understand how nitrogen cycling would proceed on terrestrial planets with comparable geodynamic activity to Earth, but on which life does not arise. We constructed a kinetic mass-flux model of nitrogen cycling in its various major chemical forms (e.g., N2, reduced (NHx) and oxidized (NOx) species) between major planetary reservoirs (the atmosphere, oceans, crust, and mantle) and included inputs from space. The total amount of nitrogen species that can be accommodated in each reservoir, and the ways in which fluxes and reservoir sizes may have changed over time in the absence of biology, are explored. Given a partition of volcanism between arc and hotspot types similar to the modern ones, our global nitrogen cycling model predicts a significant increase in oceanic nitrogen content over time, mostly as NHx, while atmospheric N2 content could be lower than today. The transport timescales between reservoirs are fast compared to the evolution of the environment; thus atmospheric composition is tightly linked to surface and interior processes.

It is widely believed that the origin of life depended on environmentally driven complexification of abiotically produced organic compounds. Polymerization is one type of such complexification, and it may be important that many diverse polymer sequences be produced for the sake of selection. Not all compound classes are easily polymerized under the environmental conditions present on primitive planets, and it is possible that life’s origin was aided by other monomers besides those used in contemporary biochemistry. Here we show that alpha-hydroxy acids, which are plausibly abundant prebiotic monomers, can be oligomerized to generate vast, likely sequence-complete libraries, which are also stable for significant amounts of time. This occurs over a variety of reaction conditions (temperature, concentration, salinity, and presence of congeners) compatible with geochemical settings on the primitive Earth and other solar system environments. The high-sequence heterogeneity achievable with these compounds may be useful for scaffolding the origin of life. The origins of life likely involved abiotic combinatorial polymer synthesis but the characterisation of such mixtures is challenging. Here the authors show that large libraries of linear and cyclic oligomers spontaneously form from α-hydroxy acids under mild conditions which may be relevant to prebiotic synthesis.

Water creates special problems for prebiotic chemistry, as it is thermodynamically favorable for amide and phosphodiester bonds to hydrolyze. The availability of alternative solvents with more favorable properties for the formation of prebiotic molecules on the early Earth may have helped bypass this so-called “water paradox”. Formamide (FA) is one such solvent, and can serve as a nucleobase precursor, but it is difficult to envision how FA could have been generated in large quantities or accumulated in terrestrial surface environments. We report here the conversion of aqueous acetonitrile (ACN) via hydrogen cyanide (HCN) as an intermediate into FA by γ-irradiation under conditions mimicking exposure to radioactive minerals. We estimate that a radioactive placer deposit could produce 0.1‒0.8 mol FA km−2 year−1. A uraninite fission zone comparable to the Oklo reactors in Gabon can produce 0.1‒1 mol m−2 year−1, orders of magnitude greater than other scenarios of FA production or delivery for which reaching sizeable concentrations of FA are problematic. Radioactive mineral deposits may be favorable settings for prebiotic compound formation through emergent geologic processes and FA-mediated organic chemistry.

The reverse tricarboxylic acid (rTCA) cycle has been explored from various standpoints as an idealized primordial metabolic cycle. Its simplicity and apparent ubiquity in diverse organisms across the tree of life have been used to argue for its antiquity and its optimality. In 2000 it was proposed that chemoinformatics approaches support some of these views. Specifically, defined queries of the Beilstein database showed that the molecules of the rTCA are heavily represented in such compound databases. We explore here the chemical structure “space,” e.g. the set of organic compounds which possesses some minimal set of defining characteristics, of the rTCA cycle’s intermediates using an exhaustive structure generation method. The rTCA’s chemical space as defined by the original criteria and explored by our method is some six to seven times larger than originally considered. Acknowledging that each assumption in what is a defining criterion making the rTCA cycle special limits possible generative outcomes, there are many unrealized compounds which fulfill these criteria. That these compounds are unrealized could be due to evolutionary frozen accidents or optimization, though this optimization may also be for systems-level reasons, e.g., the way the pathway and its elements interface with other aspects of metabolism.

How did chemicals first become organized into systems capable of self-propagation and adaptive evolution? One possibility is that the first evolvers were chemical ecosystems localized on mineral surfaces and composed of sets of molecular species that could catalyze each other&rsquo, s formation. We used a bottom-up experimental framework, chemical ecosystem selection (CES), to evaluate this perspective and search for surface-associated and mutually catalytic chemical systems based on the changes in chemistry that they are expected to induce. Here, we report the results of preliminary CES experiments conducted using a synthetic &ldquo, prebiotic soup&rdquo, and pyrite grains, which yielded dynamical patterns that are suggestive of the emergence of mutual catalysis. While more research is needed to better understand the specific patterns observed here and determine whether they are reflective of self-propagation, these results illustrate the potential power of CES to test competing hypotheses for the emergence of protobiological chemical systems.

In this review, we describe some of the central philosophical issues facing origins-of-life research and provide a targeted history of the developments that have led to the multidisciplinary field of origins-of-life studies. We outline these issues and developments to guide researchers and students from all fields. With respect to philosophy, we provide brief summaries of debates with respect to (1) definitions (or theories) of life, what life is and how research should be conducted in the absence of an accepted theory of life, (2) the distinctions between synthetic, historical, and universal projects in origins-of-life studies, issues with strategies for inferring the origins of life, such as (3) the nature of the first living entities (the “bottom up” approach) and (4) how to infer the nature of the last universal common ancestor (the “top down” approach), and (5) the status of origins of life as a science. Each of these debates influences the others. Although there are clusters of researchers that agree on some answers to these issues, each of these debates is still open. With respect to history, we outline several independent paths that have led to some of the approaches now prevalent in origins-of-life studies. These include one path from early views of life through the scientific revolutions brought about by Linnaeus (von Linn.), Wöhler, Miller, and others. In this approach, new theories, tools, and evidence guide new thoughts about the nature of life and its origin. We also describe another family of paths motivated by a” circularity” approach to life, which is guided by such thinkers as Maturana & Varela, Gánti, Rosen, and others. These views echo ideas developed by Kant and Aristotle, though they do so using modern science in ways that produce exciting avenues of investigation. By exploring the history of these ideas, we can see how many of the issues that currently interest us have been guided by the contexts in which the ideas were developed. The disciplinary backgrounds of each of these scholars has influenced the questions they sought to answer, the experiments they envisioned, and the kinds of data they collected. We conclude by encouraging scientists and scholars in the humanities and social sciences to explore ways in which they can interact to provide a deeper understanding of the conceptual assumptions, structure, and history of origins-of-life research. This may be useful to help frame future research agendas and bring awareness to the multifaceted issues facing this challenging scientific question., This project/publication was supported by the ELSI Origins Network (EON), which is supported by a grant from the John Templeton Foundation. T.F.’s work on this article was supported by an ELSI Origins Network (EON) Long-Term Visitor Award and by an UNAM-DGAPA-PAPIIT project (IA104717).

The surface metabolism theory posits that adaptive evolution initiated when autocatalytic chemical systems became spatially localized on mineral surfaces. We searched for such surface-limited metab...

Searching for life in the Universe depends on unambiguously distinguishing biological features from background signals, which could take the form of chemical, morphological, or spectral signatures. The discovery and direct measurement of organic compounds unambiguously indicative of extraterrestrial (ET) life is a major goal of Solar System exploration. Biology processes matter and energy differently from abiological systems, and materials produced by biological systems may become enriched in planetary environments where biology is operative. However, ET biology might be composed of different components than terrestrial life. As ET sample return is difficult, in situ methods for identifying biology will be useful. Mass spectrometry (MS) is a potentially versatile life detection technique, which will be used to analyze numerous Solar System environments in the near future. We show here that simple algorithmic analysis of MS data from abiotic synthesis (natural and synthetic), microbial cells, and thermally processed biological materials (lab-grown organisms and petroleum) easily identifies relational organic compound distributions that distinguish pristine and aged biological and abiological materials, which likely can be attributed to the types of compounds these processes produce, as well as how they are formed and decompose. To our knowledge this is the first comprehensive demonstration of the utility of this analytical technique for the detection of biology. This method is independent of the detection of particular masses or molecular species samples may contain. This suggests a general method to agnostically detect evidence of biology using MS given a sufficiently strong signal in which the majority of the material in a sample has either a biological or abiological origin. Such metrics are also likely to be useful for studies of possible emergent living phenomena, and paleobiological samples.

Rationale Spark discharge experiments, like those performed by Stanley Miller in the 1950s, generate complex, analytically challenging mixtures that contain biopolymer building blocks. Recently, α-amino acids and α-hydroxy acids (AHAs) were subjected to environmental cycling to form simple depsipeptides (peptides with both amide and ester linkages). The synthesis of AHAs under possible primordial environments must be examined to better understand this chemistry. Methods We report a direct, quantitative method for AHAs using ultrahigh-performance liquid chromatography and triple quadrupole mass spectrometry. Hexylamine ion-pairing chromatography and selected reaction monitoring detection were combined for the rapid analysis of ten AHAs in a single run. Additionally, prebiotic simulation experiments, including the first-ever reproduction of Miller's 1958 cyanamide spark discharge experiment, were performed to evaluate AHA synthesis over a wide range of possible primitive terrestrial environments. Results The quantitating transition for each of the AHAs targeted in this study produced a limit of detection in the nanomolar concentration range. For most species, a linear response over a range spanning two orders of magnitude was found. The AHAs glycolic acid, lactic acid, malic acid, and α-hydroxyglutaric acid were detected in electric discharge experiments in the low micromolar concentration range. Conclusions The results of this work suggest that the most abundant building blocks available for prebiotic depsipeptide synthesis would have been glycolic, lactic, malic, and α-hydroxyglutaric acids, and their corresponding amino acids, glycine, alanine, and aspartic and glutamic acids. Copyright © 2016 John Wiley & Sons, Ltd.

At the time before ∼3.5 Ga that life originated and began to spread on Earth, Mars was a wetter and more geologically dynamic planet than it is today. The Argyre basin, in the southern cratered highlands of Mars, formed from a giant impact at ∼3.93 Ga, which generated an enormous basin approximately 1800 km in diameter. The early post-impact environment of the Argyre basin possibly contained many of the ingredients that are thought to be necessary for life: abundant and long-lived liquid water, biogenic elements, and energy sources, all of which would have supported a regional environment favorable for the origin and the persistence of life. We discuss the astrobiological significance of some landscape features and terrain types in the Argyre region that are promising and accessible sites for astrobiological exploration. These include (i) deposits related to the hydrothermal activity associated with the Argyre impact event, subsequent impacts, and those associated with the migration of heated water along Argyre-induced basement structures; (ii) constructs along the floor of the basin that could mark venting of volatiles, possibly related to the development of mud volcanoes; (iii) features interpreted as ice-cored mounds (open-system pingos), whose origin and development could be the result of deeply seated groundwater upwelling to the surface; (iv) sedimentary deposits related to the formation of glaciers along the basin's margins, such as evidenced by the ridges interpreted to be eskers on the basin floor; (v) sedimentary deposits related to the formation of lakes in both the primary Argyre basin and other smaller impact-derived basins along the margin, including those in the highly degraded rim materials; and (vi) crater-wall gullies, whose morphology points to a structural origin and discharge of (wet) flows.

From a geochemical perspective, significant amounts of pure formamide (HCONH2) would have likely been rare on the early Earth. There may have been mixed formamide-water solutions, but even in the presence of catalyst, solutions with >20 weight% water in formamide would not have produced significant amounts of prebiotic compounds. It might be feasible to produce relatively pure formamide by a rare occurrence of freezing formamide/water mixtures at temperatures lower than formamide's freezing point (2.55 °C) but greater than the freezing point of water. Because of the high density of formamide ice it would have sunk and accumulated at the bottom of the solution. If the remaining water froze on the surface of this ice, and was then removed by a sublimation-ablation process, a small amount of pure formamide ice might have been produced. In addition a recent report suggested that ∼85 weight% formamide could be prepared by a geochemical type of fractional distillation process, offering another possible route for prebiotic formamide production.

A variety of organic chemicals were likely available on prebiotic Earth. These derived from diverse processes including atmospheric and geochemical synthesis and extraterrestrial input, and were delivered to environments including oceans, lakes, and subaerial hot springs. Prebiotic chemistry generates both molecules used by modern organisms, such as proteinaceous amino acids, as well as many molecule types not used in biochemistry. As prebiotic chemical diversity was likely high, and the core of biochemistry uses a rather small set of common building blocks, the majority of prebiotically available organic compounds may not have been those used in modern biochemistry. Chemical evolution was unlikely to have been able to discriminate which molecules would eventually be used in biology, and instead, interactions among compounds were governed simply by abundance and chemical reactivity. Previous work has shown that likely prebiotically available α-hydroxy acids can combinatorially polymerize into polyesters that self-assemble to create new phases which are able to compartmentalize other molecule types. The unexpectedly rich complexity of hydroxy acid chemistry and the likely enormous structural diversity of prebiotic organic chemistry suggests chemical evolution could have been heavily influenced by molecules not used in contemporary biochemistry, and that there is a considerable amount of prebiotic chemistry which remains unexplored.

The standard alphabet of the 20 genetically encoded amino acids is considered to have been selected during early evolution from a larger pool of α-amino acids based on its coverage of the chemical space. Chemical space is here defined by charge, size and hydrophobicity, leading to 6-tuples representing coverage, which is composed of range and evenness in these three physico-chemical properties. We summarize findings of previous studies on the adaptive properties of the 20 encoded amino acids and show how we extend these computational experiments to subsets of the standard alphabet.

Ribonucleic acid (RNA) is one of the two nucleic acids used by extant biochemistry and plays a central role as the intermediary carrier of genetic information in transcription and translation. If RNA was involved in the origin of life, it should have a facile prebiotic synthesis. A wide variety of such syntheses have been explored. However, to date no one-pot reaction has been shown capable of yielding RNA monomers from likely prebiotically abundant starting materials, though this does not rule out the possibility that simpler, more easily prebiotically accessible nucleic acids may have preceded RNA. Given structural constraints, such as the ability to form complementary base pairs and a linear covalent polymer, a variety of structural isomers of RNA could potentially function as genetic platforms. By using structure-generation software, all the potential structural isomers of the ribosides (BC5H9O4, where B is nucleobase), as well as a set of simpler minimal analogues derived from them, that can potentially serve as monomeric building blocks of nucleic acid–like molecules are enumerated. Molecules are selected based on their likely stability under biochemically relevant conditions (e.g., moderate pH and temperature) and the presence of at least two functional groups allowing the monomers to be incorporated into linear polymers. The resulting structures are then evaluated by using molecular descriptors typically applied in quantitative structure–property relationship (QSPR) studies and predicted physicochemical properties. Several databases have been queried to determine whether any of the computed isomers had been synthesized previously. Very few of the molecules that emerge from this structure set have been previously described. We conclude that ribonucleosides may have competed with a multitude of alternative structures whose potential proto-biochemical roles and abiotic syntheses remain to be explored. Key Words: Evolution—Chemical evolution—Exobiology—Prebiotic chemistry—RNA world. Astrobiology 15, 538–558.

The origins of life bring into stark relief the inadequacy of our current synthesis of thermodynamic, chemical, physical and information theory to predict the conditions under which complex, living states of organic matter can arise. Origins research has traditionally proceeded under an array of implicit or explicit guiding principles in lieu of a universal formalism for abiogenesis. Within the framework of a new guiding principle for prebiotic chemistry called subsumed complexity , organic compounds are viewed as by-products of energy transduction phenomena at different scales (subatomic, atomic, molecular and polymeric) that retain energy in the form of bonds that inhibit energy from reaching the ground state. There is evidence for an emergent level of complexity that is overlooked in most conceptualizations of abiogenesis that arises from populations of compounds formed from atomic energy input. We posit that different forms of energy input can exhibit different degrees of dissipation complexity within an identical chemical medium. By extension, the maximum capacity for organic chemical complexification across molecular and macromolecular scales subsumes, rather than emerges from, the underlying complexity of energy transduction processes that drive their production and modification. This article is part of the themed issue ‘Reconceptualizing the origins of life’.