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date: 23 November 2017

Origins of Life: Open Questions and Debates

Summary and Keywords

Stanley Miller demonstrated in 1953 that it was possible to form amino acids from methane, ammonia, and hydrogen in water, thus launching the ambitious hope that chemists would be able to shed light on the origins of life by recreating a simple life form in a test tube. However, it must be acknowledged that the dream has not yet been accomplished, despite the great volume of effort and innovation put forward by the scientific community. A minima, primitive life can be defined as an open chemical system, fed with matter and energy, capable of self-reproduction (i.e., making more of itself by itself), and also capable of evolving. The concept of evolution implies that chemical systems would transfer their information fairly faithfully but make some random errors.

If we compared the components of primitive life to parts of a chemical automaton, we could conceive that, by chance, some parts self-assembled to generate an automaton capable of assembling other parts to produce a true copy. Sometimes, minor errors in the building generated a more efficient automaton, which then became the dominant species. Quite different scenarios and routes have been followed and tested in the laboratory to explain the origin of life.

There are two schools of thought in proposing the prebiotic supply of organics. The proponents of a metabolism-first call for the spontaneous formation of simple molecules from carbon dioxide and water to rapidly generate life. In a second hypothesis, the primeval soup scenario, it is proposed that rather complex organic molecules accumulated in a warm little pond prior to the emergence of life. The proponents of the primeval soup or replication first approach are by far the more active. They succeeded in reconstructing small-scale versions of proteins, membranes, and RNA. Quite different scenarios have been proposed for the inception of life: the RNA world, an origin within droplets, self-organization counteracting entropy, or a stochastic approach merging chemistry and geology. Understanding the emergence of a critical feature of life, its one-handedness, is a shared preoccupation in all these approaches.

Keywords: amino acids, comets, homochirality, hydrothermal systems, lipids, meteorites, micrometeorites, nucleotides, prebiotic chemistry, RNA world

Over thousands of years, the comforting theory of spontaneous generation of life provided an answer to the enduring question of its origin. The theory safely crossed the Middle Ages and the Renaissance until Pasteur gave the finishing blow to spontaneous generation by designing a rigorous experimental setup for sterilization, showing that a sterile nutrient broth could not spontaneously generate microbial life.

Pasteur’s demonstration opened up the question of the historical origin of life. Charles Darwin had first formulated the modern approach to the chemical origin of life. In February 1871, he wrote in a private letter to Joseph Hooker:

If (and oh, what a big if) we could conceive in some warm little pond, with all sorts of ammonia and phosphoric salts, light, heat, electricity, etc., present that a protein compound was chemically formed, ready to undergo still more complex changes, at the present day such matter would be instantly devoured or adsorbed, which would not have been the case before living creatures were formed. (C. Darwin, personal communication, 1871)

For 50 years, the idea lay dormant. In 1924, the Russian biochemist Oparin pointed out that life must have arisen in the process of the evolution of matter, thanks to the reducing nature of the atmosphere. In 1929, the British biologist Haldane independently speculated on the early conditions suitable for the emergence of life. When ultraviolet (UV) light acts on a mixture of water, carbon dioxide, and ammonia, a vast variety of organic substances are made, including sugars and apparently some of the materials from which proteins are built up (Haldane, 1929). Before the emergence of life, they must have accumulated in water to form a hot, dilute “primordial soup.” In 1953, Miller reported the formation of amino acids when exposing a mixture of methane, ammonia, hydrogen, and water to spark discharges and silent electric discharge. Miller’s publication really opened the field of experimental prebiotic chemistry described here.

Assembling the Pieces for the Origin of Life

It is difficult to define life, although many definitions have been proposed (Luisi, 1998; Palyi et al., 2002; Bedau & Cleland, 2010). Perhaps the most general working definition is that adopted in 1992 by the NASA Exobiology Program: “Life is a self-sustained chemical system capable of undergoing Darwinian evolution” (Joyce, 1995, p. 140). In other words, primitive life can be defined, a minima, as an open chemical system, fed with matter and energy provided by the environment, capable of self-reproduction (i.e., making more of itself by itself), and also capable of evolving.

The concept of evolution implies that a chemical system could transfer its information fairly faithfully but making also a few random errors, which may potentially lead to a higher complexity/efficiency and possibly to a better adaptation to changes under existing environmental constraints. Schematically, the premises of primitive life can be compared to parts of a “chemical automaton.” By chance, some parts self-assembled to generate an automaton capable of assembling other parts to issue a true copy. Sometimes, a minor error in the building generated a more efficient automaton, which became the dominant species (Brack & Troublé, 2010).

The word “origin” is ambiguous since it can be understood as “origin-cause” (i.e., an in situ birth of life on Earth) or “origin-beginning” (a point of inception or an emergence, which could as well include an interplanetary transfer of life (panspermia), thus pushing the origin of life behind the scene without deciphering it). Although it would be difficult to prove that life has been transported to the Earth, the chances for the different steps of the process can be envisioned. These steps include: (1) the escape process (i.e., the removal to space of biological material that has survived being lifted off from the surface of a parent body to high altitudes), (2) the travel conditions in space (i.e., the survival of the biological material over timescales comparable with an interplanetary journey), and (3) the entry process (i.e., the likelihood for the nondestructive deposition of the biological material on another planet). Following the identification of meteorites of lunar and Martian origin, the escape of material ranging from small particles up to boulder-size from a planet after the impact of a large asteroid is a feasible process. Bacterial spores have been shown to survive shockwaves produced by a simulated meteorite impact (Horneck et al., 2001) and huge accelerations (Roten et al., 1998). In order to study step (2), the survival of resistant microbial forms in the upper atmosphere and free space, Bacillus subtilis spores, bacteria, bacteria infecting virus, tobacco mosaic virus, microbes adapted to high salt concentrations (osmophilic), cyanobacteria, and lichens have been exposed aboard balloons, rockets, spacecraft, and space stations—such as Gemini, Apollo, Spacelab, the Long-Duration Exposure Facility, Foton, Eureca, and ISS—and their responses investigated after recovery (Horneck et al., 2010; Raggio et al., 2011; Panitz et al., 2015; Mancinelli, 2015). Laboratory experiments under simulated interstellar medium conditions point to a remarkably less damaging effect of UV radiation at low temperatures. Treating B. subtilis spores with three simulated factors simultaneously (UV, vacuum, and a temperature of 10K) produces an unexpectedly high survival rate, even at very high UV fluxes. It has been estimated that, under average conditions in space, spores may survive for hundreds of years (Weber & Greenberg, 1985). Based on the mean sizes and numbers of meteorites ejected (e.g., from Mars) and percentages falling on Earth, models for galactic cosmic rays, and laboratory responses to accelerated heavy ions of B. subtilis spores and Deinococcus radiodurans cells, it has been calculated that viable transfer of microbes from Mars to Earth via impact ejecta is possible due to the high number of meteorites and the impressive resistance of microorganisms to the dangers of space (Mileikowsky et al., 2000). However, even if it appears feasible, panspermia does not shed any light on the chemical origin of life.

Inorganic Versus Organic

It is generally assumed that Earth life emerged in liquid water in the presence of organic molecules containing carbon and hydrogen atoms associated with oxygen, nitrogen, and sulphur atoms, like present life. However, some scientists promote an alternative scenario based on inorganic substrates. Schneider (1977), for example, suggested that complex dislocation networks encountered in some crystals could follow the criteria of living units and lead to a crystalline physiology. According to Cairns-Smith (1982), there is no compelling reason to relate a first life with a last common ancestor made of organic molecules. He proposed that the first living systems, and the chemical evolution preceding them, could have been based on some clay chemistry, different from life that we know. Although each step of the hypothetical sequence of events was developed in detail, the scenario has not been supported by experimental facts. Weiss (1981) published data that appeared to experimentally support Cairns-Smith’s scenario. Unfortunately, the results could not be replicated. Since no satisfactory answers could be obtained, the clay-mediated replication cannot be taken for granted.

Autotrophs Versus Heterotrophs

The assumption that life emerged in water and was based on organic molecules is not just an anthropocentric point of view, since water and carbon chemistry have very specific properties (Brack, 1993). Two types of primitive living species are considered depending on their use of organic molecules: autotrophs supposed to be able to produce their own organics from CO2 while heterotrophs used already made organics. The proponents of a metabolism-first call for the spontaneous formation of simple molecules from carbon dioxide and water to rapidly generate life (Wächtershäuser, 1988). In the second hypothesis, the primeval soup scenario, rather complex organic molecules accumulated in a warm little pond before leading to life (Haldane, 1929; Oparin, 1924).

Autotrophic processes (from the Greek autós, self, and trophe, nourishment) would be expected to produce their ingredients from very simple substances present in their surroundings. Carbon dioxide was abundant in the primitive atmosphere. The energy source required to reduce the carbon dioxide might have been provided by the oxidative formation of pyrite from iron sulphide and hydrogen sulphide. Pyrite has positive surface charges and bonds the products of carbon dioxide reduction, giving rise to a two-dimensional reaction system, a “surface metabolism” (Wächtershäuser, 1994, 2007). Laboratory work has provided some support for this promising hypothesis. The reduction of carbon dioxide in the presence of FeS and H2S provided mainly methyl- and ethyl-thiol along with smaller amounts of other thiols containing up to five carbon atoms. The CO2 was also converted to CS2 and COS (Heinen & Lauwers, 1996). The direct reduction of CO2 to acetic acid, acetaldehyde, ethanol, and smaller amounts of carbon compounds containing up to six carbon atoms was observed to take place at 350°C and high pressure in the presence of magnetite (Fe3O4) and small amounts of water (Chen & Bahnemann, 2000). Along with the scenario proposed by Michael Russel (Martin et al., 2008), a laboratory setup simulating conditions prevailing in alkaline hydrothermal vents generated low yields of simple organics (Herschy et al., 2014). So far, the proponents of a metabolism-first approach have not been able to produce large enough precursor prebiotic molecules to create simple primitive life in a test tube.

The Primeval Soup

The primeval soup approach, also called replication first, requires complex organic molecules accumulating in a warm little pond, as Darwin proposed. The sources for such molecules would be threefold: the atmosphere, submarine hydrothermal systems, and space delivery. The simplest sources of carbon for building prebiotic organic molecules are gaseous (i.e., carbon dioxide and monoxide for the oxidized forms, and methane for the reduced ones). The Russian biochemist Oparin (1924) suggested that the small reduced organic molecules needed for primitive life were formed in a primitive atmosphere dominated by methane.

Miller (1953) tested the idea by exposing a mixture of methane, ammonia, hydrogen, and water to spark discharges and silent electric discharge. In his initial experiment, he obtained three amino acids (glycine, alanine, and β‎-alanine) via the intermediary formation of hydrogen cyanide and aldehydes. The Miller laboratory synthesis of amino acids occurs efficiently when using a reducing gas mixture containing significant amounts of hydrogen.

However, the dominant view is that the primitive atmosphere consisted mainly of CO2, N2, and H2O, along with small amounts of CO and H2 (Catling & Kasting, 2007). Only small yields of amino acids are formed in such a mixture (Schlesinger & Miller, 1983), though more recent studies show that the low yields previously reported could be the outcome of oxidation of the organic compounds during hydrolytic reprocessing by nitrite and nitrate produced in the reactions. The yield of amino acids is greatly increased when oxidation inhibitors, such as ferrous iron, are added prior to hydrolysis, suggesting that synthesis from neutral primitive atmospheres may be more important than previously thought (Cleaves et al., 2008). Additionally, 22 amino acids and five amines were obtained when reanalyzing archived samples from Miller’s experiments.

This later analysis suggests that, even if the overall atmosphere was not reducing, localized prebiotic synthesis could have been effective in volcanic plumes (Johnson et al., 2008). Miller also sparked a gas mixture of CH4, NH3, and H2O while intermittently adding the plausible prebiotic condensing reagent cyanamide. After his death, the archived samples were analyzed for amino acids, dipeptides, and diketopiperazines. A dozen amino acids, 10 glycine-containing dipeptides, and three glycine-containing diketopiperazines were found. These results highlight the potential importance of condensing reagents in generating diversity within the prebiotic chemical inventory (Parker et al., 2014).

Intense bombardment probably caused some chemical reprocessing of the Earth’s primitive atmosphere by impact shock chemistry. For example, hydrogen cyanide was produced in the laboratory by impact of a polycarbonate projectile and graphite through a N2-rich atmosphere. A significant fraction (>0.1 mol %) of the vaporized carbon was converted to HCN and cyanide condensates, even when the ambient gas contained as much as a few hundred mbar of CO2 (Kurosawa et al., 2013).

Submarine Hydrothermal Systems

The reducing conditions in hydrothermal systems, which are due to serpentinization reactions (reviewed by Holm et al., 2015), may have been an important source of biomolecules on the primitive Earth (Baross & Hoffman, 1985; Holm, 1992; Holm & Andersson, 1998, 2005). These reducing environments result from the flow of substances dissolved in seawater past inorganic compounds present in very hot crustal material that reduce organic compounds in the seawater. The reduced compounds flow out of the hydrothermal system, and the inorganic sulfides formed will precipitate when they mix with the cold (4°C) ocean water. For example, hydrocarbons and oxidized organic compounds have been detected in hydrothermal fluids from Rainbow and Lost City ultramafic-hosted vents (Konn et al., 2009).

However, hydrothermal vents are often disqualified as efficient reactors for the synthesis of bioorganic molecules because of their frequently high temperatures. Experiments have been conducted to explore the potential for amino acid synthesis at high temperature from synthetic seawater solutions of varying composition (Aubrey et al., 2009). Using very favorable reactant conditions (high concentrations of reactive, reduced species), small amounts of a limited set of amino acids are generated at moderate temperature conditions (∼125–175°C) over short heating times of a few days, but even these products are significantly decomposed after exposure times of approximately one week. Therefore, although amino acids can be generated from simple, likely environmentally available precursors under submarine hydrothermal system conditions, the equilibrium at high temperatures favors net amino acid degradation rather than synthesis. Nevertheless, the products that are synthesized in hot vents are rapidly quenched in the surrounding cold water thanks to the good heat conductivity of water and may be preserved (Ogata et al., 2000).

There have been reports on the reaction of CO in simulated hydrothermal systems. When a mixture of CO and CH3SH was reacted with a combination of a NiS-FeS at 100°C, acetic acid and its corresponding thioester were formed (Huber & Wächtershäuser, 1997). This system was extended to the formation of keto esters at higher temperatures and pressures where CO inserted into the thioester to form a keto thioester that in turn hydrolyzed to pyruvic acid (Cody et al., 2000). More recently, α‎-hydroxy and α‎-amino acids have been obtained under possible volcanic origin-of-life conditions by heating CO in the presence of nickel or nickel/iron with carbonyl, cyano, and methylthio ligands as carbon sources (Huber and Wächtershäuser, 2006). However, the plausibility of the conditions used has been debated (Bada et al., 2007). The formation of the same α‎-hydroxy and α‎-amino acids has been observed at temperatures from 145 to 280°C with catalytic Ni2+, cyano ligands as a source for carbon and nitrogen, and CO as a reductant and also source for carbon (Huber et al., 2010).

A nuclear geyser driven by a natural nuclear reactor has also been proposed as a birthplace for prebiotic chemistry. Such a nuclear geyser would have supplied the following advantages: high-density ionizing radiation to promote chemical chain reactions, a system to maintain the circulation of material and energy, a lower temperature, a locally reductive environment, and a container to confine and accumulate volatile chemicals (Ebisuzaki & Maruyama, 2017). It is supposed that 235U was common and in high abundance in the Hadean Earth. However, large amounts of 235U would have required an oxidizing system, which appeared much later, after the Great Oxidation Event (2.4–2.3 billion years ago).

Extraterrestrial Organic Matter

The Earth experienced a large spectrum of impactors ranging from the Mars-sized impactor that created the Moon, the late heavy bombardment thought to have occurred approximately 4.1 to 3.8 billion years ago, and meteorites of various sizes to cosmic dust less than 1 µm in size. A great number of organic molecules, including amino acids, have been found in carbonaceous chondrites. Micrometeorite collection and analysis from the Greenland and Antarctic ice sheets suggests that the Earth accreted large amounts of extraterrestrial complex organic molecules. Intense bombardment probably caused some chemical reprocessing of the Earth’s primitive atmosphere. Laboratory and space experiments support the extraterrestrial delivery of organics to the primitive Earth.

Comets are the most primitive planetary objects in the solar system and are expected to be the richest in organic compounds. Ground-based observations have detected hydrogen cyanide and formaldehyde in the coma of comets. In 1986, onboard analyses performed by the two Russian missions Vega 1 and 2, as well as observations obtained by the European mission Giotto and the two Japanese missions Suisei and Sakigake, demonstrated that Comet Halley contains substantial amounts of organic material. According to Delsemme’s analysis, dust particles ejected from the Comet Halley nucleus contain 14% organic carbon by mass (Delsemme, 1998). About 30% of cometary grains are dominated by light elements C, H, O, and N, and 35% are close in composition to carbonaceous chondrites (Langevin et al., 1987). Among the molecules identified in comets are hydrogen cyanide and formaldehyde. The presence of purines, pyrimidines, and formaldehyde polymers has also been inferred from the fragments analyzed by Giotto PICCA and Vega PUMA mass spectrometers (Kissel & Krueger, 1987). Many chemical species of interest for exobiology were detected in Comet Hyakutake in 1996, including ammonia, methane, acetylene, acetonitrile, and hydrogen isocyanide. In addition to hydrogen cyanide and formaldehyde, detected in several earlier comets, Comet Hale–Bopp was also shown to contain methane, acetylene, formic acid, acetonitrile, hydrogen isocyanide, isocyanic acid, cyanoacetylene, and thioformaldehyde (Irvine et al., 1996; Dello Russo et al., 2000; Bockelée-Morvan et al., 2000).

The collision of Comet Shoemaker–Levy 9 with Jupiter in July 1994 gave an example of such events. Such collisions were probably more frequent 4 billion years ago, the comets orbiting around the Sun being more numerous. Comets could therefore appear as an important source of organic molecules delivered to the primitive Earth (Ehrenfreund & Charnley, 2000; Despois & Cottin, 2005). However, it is unlikely that whole comets could have safely delivered organics to the Earth. They exploded either while crossing the atmosphere or when impacting the Earth’s surface.

The European Space Agency (ESA) Rosetta robotic spacecraft performed the most detailed study of a comet ever attempted (Glassmeir et al., 2007). Launched in March 2004, the spacecraft reached Comet 67P/Churyumov–Gerasimenko in August 2014. The spacecraft consisted of two main elements: the Rosetta space probe orbiter and the Philae robotic lander. The orbiter featured eleven instruments. Among them, ROSINA (Rosetta Orbiter Spectrometer for Ion and Neutral Analysis) measured the deuterium-to-hydrogen ratio of water vapor emanating from the comet and found it to be more than three times greater than for Earth’s oceans (Altwegg et al., 2015). The discovery fuels the debate on the origin of Earth’s oceans.

The instrument also made the first measurement of molecular nitrogen at a comet, providing clues about the temperature environment in which the comet formed (Rubin et al., 2015). Moreover, ROSINA detected volatile glycine, accompanied by methylamine and ethylamine, in the coma, confirming the Stardust results (Elsila et al., 2009). Together with the detection of phosphorus and a multitude of organic molecules, this result demonstrates that comets could have played a crucial role in the emergence of life on Earth (Altwegg et al., 2016). The same instrument measured xenon isotopes and showed that comets contributed to Earth’s atmosphere (Marty et al., 2017). Another Rosetta instrument, COSIMA, dedicated to the analysis of cometary grains by TOF-SIMS (Time of Flight Secondary Ion Mass Spectrometry) showed the presence of complex macromolecular organics in the grains emitted by the cometary nucleus, similar to the insoluble organic matter found in carbonaceous chondrites (Fray et al., 2016). The Philae robotic probe landed on Comet 67P/Churyumov–Gerasimenko on 12 November 2014, achieving the first-ever landing on a comet nucleus. It hosted nine instruments. Among them, COSAC (Cometary Sampling and Composition experiment) was designed to detect and identify complex organic molecules from their elemental and molecular composition. SD2 (Sample and Distribution Device) was designed to drill more than 20 cm into the surface, collect samples, and deliver them to different ovens or for microscope inspection. At the end of 2014, the Philae lander successfully touched down on the comet. Unfortunately it bounced twice, finally settling in a location and in a configuration that impeded the solar panels from charging the batteries. After a year of silence from the craft, the ESA began to power down the systems. Philae provided interesting results for astrobiology. Just after the first comet touchdown, the COSAC mass spectrometer took a spectrum in sniffing mode of the ejected material. The spectrum displayed a suite of 16 organic compounds, including methyl isocyanate, acetone, propionaldehyde, and ethanamide (Goesmann et al., 2015).

In contrast to comets, carbon-containing meteorites (the carbonaceous chondrites, mainly) have delivered organic materials to the Earth since it formed. They contain from 1.5% to 4% of carbon, for the most part as organic materials. One hundred kilograms of the Murchison meteorite, a CM2 type carbonaceous chondrite that fell in Australia in 1969, have been extensively analyzed (see Pizzarello, 2007; Pizzarello & Shock, 2010; Cooper & Riosa, 2016). Murchison organic materials are generally classified according to their solubility in water and organic solvents. Insoluble and soluble components represent respectively 70% and 30% of total carbon components. The insoluble organic material is referred to as kerogen-like, a poorly identified insoluble macromolecular material of complex composition with average elemental abundances C100H46N10O15S4.5. Nuclear magnetic resonance (NMR), infrared (IR), and pyrolysis analyses suggest the presence of aromatic ring clusters bridged by aliphatic chains, with peripheral branching and functional groups.

The insoluble organic material releases a variety of aromatic and heteroatomic hydrocarbons, as well as a suite of alkyl dicarboxylic acids up to C18 chain length under conditions similar to those of hydrothermal vents (Yabuta et al., 2007). The soluble organic compounds of the Murchison meteorite represent a diverse and abundant group of organics that vary from volatile compounds such as methane and ethane (Yuen et al., 1984) to small water-soluble compounds such as amino acids and polyols up to 30-carbon-long hydrocarbons. The amino acid diversity has been analyzed in detail. The total number of amino acids detected in meteorites is about one hundred. All the possible α‎-amino alkylamino acids up to seven-carbon were identified, as well as large abundances of N-substituted, cyclic, β‎-, γ‎-, δ‎-, and ε‎-amino acids (Cronin et al., 1988). Eight biological amino acids (glycine, alanine, proline, leucine, isoleucine, valine, aspartic acid, and glutamic acid) have been found. Nucleic acid bases, purines and pyrimidines, have also been found in the Murchison meteorite (Stoks & Schwartz, 1982; Callahan et al., 2011). No ribose (the sugar linking together the nucleic acid building blocks) was detected in meteorites. Droplet-forming fatty acids have been extracted from different carbonaceous meteorites (Deamer, 1985, 1998). A combination of high-resolution analytical methods, including organic structural spectroscopy (FTICR/MS, UPLC-QTOF-MS, and NMR) applied to the organic fraction of Murchison extracted under mild conditions has extended its indigenous chemical diversity to tens of thousands of different molecular compositions and likely millions of diverse structures (Schmitt-Kopplin et al., 2010; Hertkorn et al., 2015). Most of the amino acids detected in the carbonaceous chondrites are chiral but present as racemic (i.e., L- and D-enantiomers are present in equal proportions). However, some unbalanced mixtures of enantiomers have been detected (see the section “Intriguing One-Handedness of Life”). The discovery of a large number of meteorites since 1969 has provided new opportunities to search for organic compounds in CM type carbonaceous chondrites (Pizzarello et al., 2001; Glavin et al., 2006; Pizzarello & Shock, 2010).

Micrometeorite collections in the Greenland and Antarctica ice sheet (Maurette, 1998, 2006) show that the Earth captures interplanetary dust as micrometeorites at a rate of about 20,000 tonnes per year. About 99% of this mass is carried by micrometeorites in the 50–500 µm size ranges. This value is about 2,000 times higher than the most reliable estimate of the meteorite flux (i.e., about 10 tonnes per year). This amazing dominance of micrometeorites already suggests their potentially important role in delivering complex organics to the early Earth, especially 4.1–3.9 Ga when the micrometeorite flux was probably enhanced by several orders of magnitude. Antarctic micrometeorite flux measurements suggest that a huge mass (~5x1024 g) of micrometeorites was accreted by the Earth during the first ~300 Ma of the post-lunar period. At least approximately 20 wt.% of the micrometeorites survives unmelted upon atmospheric entry. As their kerogen fraction represents about 2.5 wt.% of carbon, this amounts to a total mass of kerogen of ~2.5x1022 g on the early Earth surface (Maurette & Brack, 2006). For comparison, this delivery represents more carbon than is present in the biomass of the present-day Earth (1018 g). One amino acid, α‎-amino isobutyric acid, has been identified in Antarctic micrometeorites (Brinton et al., 1998; Matrajt et al., 2004). These grains also contain a high proportion of metallic sulfides, oxides, and clay minerals, a rich variety of inorganic catalysts that could have promoted the reactions of the carbonaceous material leading to the origin of life. Analysis of the dust grains collected by the Cosmic Dust mission supports a cometary origin for the micrometeorites collected in Antarctica. A collection of CONCORDIA Antarctic micrometeorites recovered from ultraclean snow close to Dome C provided the most unbiased collection of large cosmic dust available. Many similarities can be found between Antarctic micrometeorites and samples from Comet Wild 2, in terms of chemical, mineralogical, and isotopic compositions, and in the structure and composition of their carbonaceous matter (Dobrica et al., 2013). The cometary origin has been confirmed by a zodiacal cloud model based on the orbital properties and lifetimes of comets and asteroids, and constrained by Infrared Astronomical Satellite observations of thermal emission, but also qualitatively consistent with meteor observations, with spacecraft impact experiments, and with properties of recovered micrometeorites (Nesvorny et al., 2010).

From Building Blocks to Life

By analogy with contemporary living systems, it is tempting to consider that primitive life emerged as a cell-like system. Such a system requires, at least, boundary molecules able to isolate a system from the aqueous environment (membrane), catalytic molecules conducting the basic chemical work of the cell (like enzymes), and information molecules able to store and transfer the information needed for reproduction (like nucleic acid polymers). Great efforts have been deployed in laboratories to produce these three prerequisites, albeit separately. Notably, Sutherland’s team produced simultaneously precursors of nucleic acid amino acids and lipids starting with just hydrogen cyanide, hydrogen sulfide, and UV light (Patel et al., 2015), a step toward the congruence hypothesis advocated by de Duve (2003).

Fatty acids are known to form vesicles when their hydrocarbon chains contain more than 10 carbon atoms. Such vesicle-forming fatty acids have been identified in the Murchison meteorite. However, the membranes obtained with these simple amphiphiles (molecules bearing both water-soluble and water-insoluble portions) are not stable over a broad range of environmental conditions (Deamer, 1998, 2017; Pohorille & Deamer, 2009). Ourisson and Nakatani suggested that primitive membranes were composed of densely branched isoprene-derived chains instead of long-alkyl amphiphilic hydrocarbons (Streiff et al., 2007). How different prebiotically available building blocks could have become precursors of phosphorus-containing lipids that form vesicles has been reviewed (Fiore & Strazewski, 2016).

Protein enzymes, made of 20 major L-amino acids, catalyze most of the chemical reactions in a living cell. Amino acids were most likely available on the primitive Earth as complex mixtures. Chemical reactions able to selectively condense the protein amino acids, at the expense of the nonprotein ones in water, have been identified. Helical and sheet structures can be modeled with the aid of only two different amino acids, one hydrophobic and the other hydrophilic. Polypeptides with alternating hydrophobic and hydrophilic residues adopt water-soluble layered structures (β‎-sheets) because of hydrophobic side-chain clustering. Owing to the formation of a β‎-sheet, alternating sequences gain good resistance toward chemical degradation. Aggregation of alternating sequences into β‎-sheets is possible only with all-L or all-D polypeptides. Short peptides have also been shown to exhibit catalytic properties (Brack, 2007).

Matsuno and colleagues (Imai et al., 1999) reported peptide formation in an organized flow reactor that mimicked the conditions in a hydrothermal system. The team was able to polymerize glycine monomers up to six units in the presence of Cu ions. This setup was also able to demonstrate polymerization at temperatures of 200–250°C, contrary to the popular belief that organic molecules are unstable under high temperatures. Rodriguez-Garcia and colleagues (2015) mimicked this hydrothermal system and developed an automated method to expose glycine monomers to prolonged dehydration–hydration cycles and, interestingly, chain lengths of 20 amino acids were observed. In addition to homo-oligomerization, the team was able to observe hetero-oligomerization to chain lengths involving eight different amino acids.

In contemporary living systems, the hereditary memory is stored in nucleic acids, long chains built from nucleotides. Each nucleotide is composed of a base (purine or pyrimidine), a sugar (ribose for RNA, deoxyribose for DNA), and a phosphate group. The synthesis of nucleotides is complex, due mainly to the poor yield of sugars obtained from formaldehyde in the formose reaction (Decker et al., 1982) and the instability of sugars. The half-life of the ribose sugar is so short—73 minutes at 100°C—(Larralde et al., 1995) that it is hard to imagine that it could have remained stable enough to accumulate over geological timescales. However, several developments in the prebiotic synthesis of ribose have improved the prospect. For example, borate minerals have been shown to stabilize ribose (Prieur, 2001; Ricardo et al., 2004). The condensation of amide derivatives of pyrimidine (formamidopyrimidines) with sugars provides the natural N-9 nucleosides (ribose bound to a nucleic base) in good yields (60%). Formamidopyrimidines are available from formic acid and amino pyrimidines, which are in turn available from prebiotic molecules that were also detected during the Rosetta comet mission. This nucleoside formation pathway can be fused to sugar-forming reactions, providing a plausible scenario of how purine nucleosides may have formed under prebiotic conditions (Becker et al., 2016). Two plausible prebiotic heterocycles, melamine and barbituric acid, have been shown to form sugar-type linkages with ribose and ribose-5-phosphate in water to produce nucleosides and nucleotides in good yields. Even without purification, these nucleotides base-pair in aqueous solution to create linear supramolecular assemblies containing thousands of ordered nucleotides. Supramolecular assemblies favor the biologically relevant form of these ribonucleotides, revealing abiotic mechanisms by which nucleotide structure and configuration could have been originally favored (Cafferty et al., 2016).

Another step forward was the observation that glycolaldehyde phosphate reacting with glyceraldehyde phosphate gives ribose-2,4-diphosphate as the principal reaction product (Müller et al., 1990). This synthesis was improved by performing the reaction with glycolaldehyde phosphate and glyceraldehyde phosphate on a mixed-valence double-layer hydroxide mineral surface, where ribose 2,4-diphosphate was the major pentose phosphate formed with overall yield of about 12% (Krishnamurthy et al., 1999). Heated solutions containing both 5-hydroxymethyluracil and 5-hydroxymethylcytosine result in mixed oligomers of uracil and cytosine (Smith et al., 2017). Instead of trying to assemble the three subunits of a ribonucleotide, the building block of RNA, John Sutherland and his colleagues created a ribonucleotide from simple chemicals under conditions that might have existed on the early Earth (Powner et al., 2009). The plausibility of such prebiotic multistage syntheses has been evaluated by Alan Schwartz (2013). Ribose has not been detected in meteorites; however, irradiation by UV photons of interstellar ice analogs made of water, methanol, and ammonia at 78 K in a high-vacuum chamber generated substantial quantities of ribose and a diversity of structurally related sugar molecules such as arabinose, xylose, and lyxose (de Marcellus et al., 2015; Meinert et al., 2016).

Binding phosphorus to nucleosides with phosphorylating agents likely to be present in a primitive Earth is another complex issue. Studies using the mineral schreibersite, (Fe,Ni)3P, conducted independently by Pasek (2017) and Kee and colleagues (2013), provide a possible solution to this problem. On the other hand, in a geological environment that contains borate, magnesium, sulfate, calcium, and phosphate, Mg2+ ions and borate sequester phosphate from calcium to form the mineral lüneburgite. Ribonucleosides stabilized by borate mobilize borate and phosphate from lüneburgite, and are then region-specifically phosphorylated by the mineral (Kim et al., 2016). Phosphorus-rich basaltic glasses have also been proposed as a possible source of condensed phosphates on the early Earth (Holm, 2014). A urea/ammonium formate/water eutectic solution leads to an increase in phosphorylation when compared to urea alone for phosphate sources of varying solubility. In addition, under evaporative conditions and in the presence of MgSO4, the eutectic mobilizes the phosphate sequestered in water-insoluble hydroxyapatite, giving rise to a marked increase in phosphorylation. The results suggest that the prebiotic concentrations of urea in a geologically plausible evaporitic environment could solve the problem of organic phosphorylation on a prebiotic Earth (Burcar et al., 2016).

The RNA World Hypothesis

In 1986, Zaug and Cech (1986) found that some RNAs, the ribozymes, have catalytic properties. For example, they increase the rate of hydrolysis of oligoribonucleotides. They also act as polymerization templates, because chains of up to 30 monomers long can be obtained starting from a pentanucleotide. Since this primary discovery, the catalytic spectrum of these ribozymes has been considerably enlarged by directed test-tube molecular evolution experiments (Prywes et al., 2016; Horning & Joyce, 2016). Since RNA was shown to be able to act simultaneously as an information molecule and as a catalytic molecule, RNA has been considered as the first living system on the primitive Earth. A ribozyme-based “RNA world” has been modeled in some detail and reviewed (Higgs & Lehman, 2015). The route to the RNA world has been paved by the impressive work of Jim Ferris, who polymerized RNA-like monomers on clays (Ertem, 2004; Ferris, 2005, 2006; Huang & Ferris, 2007).

A key role of clay minerals in the origin of life was first suggested by Bernal (1949). The advantageous features of clays are: (1) their ordered arrangement, (2) their large adsorption capacity, (3) their shielding against sunlight UV, (4) their ability to concentrate organic chemicals, and (5) their ability to serve as polymerization templates. One should, however, remember that the synthesis of RNA itself, under prebiotic conditions, remains a difficult challenge. The RNA world appears as a probable episode in the evolution of life before the appearance of cellular life, but the question is still open as to whether life started with RNA molecules or with simpler RNA analogues or surrogates that evolved to RNA, as highlighted by the brilliant series of publications of Albert Echenmoser (2011). One should, however, remember that the complete synthesis of RNA under “prebiotic conditions” remains an unsolved challenge. It seems therefore unlikely that life started with RNA molecules, because these molecules are not simple enough and their synthesis is not simple enough.

A Vesicular Origin of Life

Harold Morowitz (1992) postulated that the first step toward the origin of life was the spontaneous condensation of amphiphilic molecules to form vesicles, and examples of autocatalytic micelle growth have been described (Bachmann et al., 1992). However, these autocatalytic systems alone do not store hereditary information and cannot therefore evolve by natural selection. Szostak and colleagues (Hanczyc et al., 2007; Budin & Szostak, 2010; Schrum et al., 2010; Adamala & Szostak, 2013) found that the presence of naturally occurring clay minerals, such as montmorillonite, can help in the assemblage of vesicles and bring bound RNA into the interior of the vesicles, thus providing information to the vesicular system. Even more ambitious, the “minimal cell project” has aimed to synthesize a cell model having the minimal number of components to be defined as living. Liposomes are used as cell membranes, and attempts are made to introduce a minimal genome (for a comprehensive review, see Meierhenrich et al., 2010). The role of vesicles in the origins of life is unquestionable and is being explored extensively. Montmorillonite clay vesicles have been found to offer robust, inorganic, semipermeable compartments. They exhibit size-selective permeability and support spontaneous compartmentalization of self-assembling molecules in aqueous environments (Subramaniam et al., 2011). More recently, it has been demonstrated that droplets maintained away from thermodynamic equilibrium by an external supply of energy grow by the addition of droplet material generated by chemical reactions. Surprisingly, chemically driven droplet growth can lead to shape instabilities that trigger the division of droplets into two smaller daughters, thus exhibiting cycles of growth and division that resemble the proliferation of living cells (Zwicker et al., 2016).

Entropy, Self-Organization and Autocatalysis

It is often argued that the slow and irreversible progression of complexity toward life runs against the second law of thermodynamics, which rules that entropy (i.e., disorder) increases over time and that order and organization always decline. Considering that the law specifically applies to isolated systems whereas living systems are necessarily open systems, Prigogine showed that many systems spontaneously organize themselves if they are forced away from thermodynamic equilibrium (Nicolis & Prigogine, 1977). For example, amphiphilic molecules, with a hydrophobic hydrocarbon tail and a hydrophilic polar head, self-associate spontaneously in water to form droplet-like vesicles. As already mentioned, strictly alternating polypeptides, with charged hydrophilic and hydrophobic residues, self-organize into asymmetrical β‎-sheet bilayers with a hydrophobic interior and a hydrophilic exterior (Brack & Orgel, 1975). More recently, an attempt has been made to reconcile Darwinian theory and the second law of thermodynamics through the concept of dynamic kinetic stability and persistence. Provided they are held far from equilibrium, systems that are capable of making more of themselves can evolve toward increased kinetic stability, which is another form of persistence (Pascal & Pross, 2016).

Chemists have been tempted to consider that primitive replicating systems must have used simpler information-retaining molecules than biological nucleic acids or their analogues and looked for simple, self-sustaining chemical systems capable of self-replication, mutation, and selection. It has been shown that simple molecules unrelated to nucleotides can actually provide exponentially replicating autocatalytic models. Autocatalysis is observed when the product of the reaction catalyzes its own formation. Von Kiedrowski (Terfort & von Kiedrowski, 1992) tested different templates while Burmeister (1998) reported information-transfer templates in complex systems. In most cases, the rate of the autocatalytic growth did not vary in a linear sense, in contrast to most autocatalytic reactions known so far. Two preformed fragments of a peptide have been demonstrated to be autocatalytically ligated by the whole peptide acting as a template (Lee et al., 1996, 1997; Saghatelian et al., 2001). However, the replicated molecules contain only two “letters” and possess therefore a very low level of information.

The Intriguing One-Handedness of Life

Pasteur was the first to postulate that optical activity was the demarcation line between animate and inanimate kingdoms and expressed the concept that life is dominated by dissymmetric actions whose existence is cosmic (Pasteur, 1860). The carbon atom, which has a tetrahedral distribution of its bonds, becomes asymmetric when attached to four different substituents. A molecule that has at least one such carbon is then chiral and, a priori, can exist in two forms that are mirror images of each other and are called enantiomers (Pizzarello & Groy, 2011). Most of the constituents of present life—amino acids, sugars, and lipids—contain at least one asymmetric carbon. Life is one-handed, so only one enantiomer of each chiral biomolecule is present in living systems—that is, proteins use only L-amino acids and DNA and RNA D-sugars. Proteins also may adopt asymmetrical, rigid geometries, helices, and sheets, which play a key role in the catalytic activity. One-handedness (homochirality) is believed to be not just a consequence of life, but also a prerequisite for life because structures such as described above do not form with mixtures of monomers of both-handedness. The use of one-handed biomonomers also refines the sequence information of the biopolymers. For a polymer made of n units, the number of sequence combinations will be divided by 2n when the system uses only homochiral monomers. Taking into account the fact that enzyme chains are generally made of hundreds of monomers, the tremendous gain in simplicity offered by the use of monomers restricted to one-handedness is self-evident. Any chemical reaction performed in a symmetrical environment that forms chiral molecules yields a racemic mixture (i.e., a mixture of equal quantities of right- and left-handed enantiomers). Racemic biomolecules probably formed initially on the primitive Earth; however, it is unlikely that the first life contained both the right- and left-handed forms of the same biological molecules. Theoretical models show that autocatalytic systems fed with both left- and right-handed molecules must become one-handed in order to survive.

The problem in understanding the generation of homochirality is twofold: the origin of a prevalent enantiomer and its further amplification until the appearance of life. Amplification of a few percent of enantiomeric excesses has been well documented in the laboratory using crystals, crystallization processes, or biopolymers. Soai (Shibata et al., 1998) has nicely demonstrated that a few percent of a chiral initiator can dramatically amplify molecular one-handedness via autocatalysis. Theoretical models for the existence of the slightly prevalent enantiomer excess on Earth can be divided into two kinds: those calling for a chance mechanism and those implicating a determinate mechanism resulting from an asymmetrical environment on Earth or even in the universe.

The proponents of the chance mechanism argue that the notion of a racemic mixture perfectly equilibrated is relative, and random fluctuations may favor one enantiomer over the other. For instance, for a population of 10 million molecules, which is about the amount of chiral constituents of the smallest living cell, the probability of finding an excess of 0.02% or more in one enantiomer is about 50% (Spach & Brack, 1988). In a rather simple kinetic model proposed by Frank (1953), an open flow reactor, run in far from equilibrium conditions, is fed with potentially asymmetric compounds and forms two enantiomers reversibly and autocatalytically. If the two enantiomers can react to form an irreversible combination flowing out the reactor—by precipitation, for instance—and if certain conditions of fluxes and concentrations are reached, the racemic production may become metastable and the system may switch permanently toward the production of either one or the other enantiomer, depending on a small excess in one enantiomer. The Frank model has inspired a model described as a theoretical framework, based on the one-handed driven reactivity of preexisting chiral monomeric building blocks maintained out of equilibrium by a continuous energy income, via an activation reaction. It permits the self-conversion of all monomeric subunits into a single chiral configuration (Plasson et al., 2004). A model featuring enantiomer cross-inhibition and chiral bias has been used to study the diffusion equations controlling the spatio-temporal development of left- and right-handed domains in the context of autocatalytic polymerization reaction networks (Gleiser, 2007). A fully self-contained model of homochirality has been proposed that contains the effects of both polymerization and dissociation (Brandenburg et al., 2005).

Crystallization represents the most effective mechanism for molecular symmetry breaking by chance, as exemplified by Kondepudi et al. (1990) with the crystallization of sodium chlorate. When the solution was stirred, almost all the NaClO4 crystals (99.7%) in a given sample had the same chirality, either L or D. Enantio enrichment of a variety of amino acids has also been obtained by sublimation of near-racemic samples (Fletcher et al., 2007; Perry et al., 2007; Tarasevych et al., 2013, 2015). Clays have also been claimed to exhibit asymmetric effects by several authors, although common clays, such as kaolinite and montmorillonite, have no intrinsic chirality and thus are not expected to develop stereoselective interactions with chiral prebiotic molecules. They have attracted a great deal of interest but have generated, at the same time, a lot of controversies about false positives (Brack, 2013).

As for the determinate mechanisms, parity nonconservation has raised many hopes and caused many disappointments. This fundamental asymmetry of matter has been examined from various aspects, such as circularly polarized photons emitted by the slowing down of longitudinally polarized electrons (Bremsstrahlung), inducing degradation reactions or stereoselective crystallization of racemic mixtures. No experiment has convincingly supported these theoretical considerations for the origin of a dominant enantiomer on Earth. Either the results were shown to be artefacts or to be so weak that they are doubtful (MacDermott, 1995). There is a very tiny parity-violating energy difference in favor of L-amino acids in their preferred conformations in water and in favor of D-sugars (Nordén et al., 1985). The energy difference is about 3x10−19 eV corresponding to one part in 10+17 for the excess of L-molecules in a racemic mixture at thermodynamic equilibrium at ambient temperature. However, such a tiny energy difference is not sufficient to form one enantiomer preferentially.

The possibility to induce a chiral effect by submitting a suitable chemical reaction to a magnetic field, already conceived by Pasteur, has received an experimental support by Rikken and Raupach (2000). The authors used a chiral chromium complex, which is unstable in solution and spontaneously dissociates and reassociates. The dissociation is accelerated by the absorption of light. In the presence of an unpolarized laser beam traveling parallel to a static magnetic field, a small excess of one enantiomer is produced and maintained. On reversing the magnetic field direction, the mirror-image enantiomer is obtained. Magnetochiral photochemistry appears therefore as a possible source for biological homochirality.

Extraterrestrial Source of Homochirality

Cronin and Pizzarello (Cronin & Pizzarello, 1997; Pizzarello & Cronin, 2000) found small L-enantiomer excesses in six α‎-methyl-α‎-amino alkanoic acids from the Murchison (2.8–9.2%) and Murray (1.0–6.0%) carbonaceous chondrites. Enantiomeric excesses up to 15% have been measured for isovaline, 2-methyl-2-aminobutyric acid (Pizzarello et al., 2003). These amino acids are either unknown or rare in the terrestrial biosphere and cannot therefore be attributed to terrestrial contamination (Pizzarello, 2007). In addition, the indigeneity of D- and L-isovaline enantiomers is supported by carbon and hydrogen isotopic data (Pizzarello et al., 2003; Pizzarello & Huang, 2005). The Renazzo-type (CR) chondrites found in Antarctica revealed native enantiomeric excesses of up to 60% (Pizzarello et al., 2012). The excess of one-handed amino acids found in the Murchison meteorite may result from the processing of the organic mantles of interstellar grains by circularly polarized synchrotron radiation from a neutron star remnant of a supernova (Bonner, 1991). Strong infrared circular polarization, resulting from dust scattering in reflection nebulae in the Orion OMC-1 star-formation region, has been observed (Bailey et al., 1998). Circular polarization at shorter wavelengths might have been important in inducing chiral asymmetry in interstellar organic molecules, which could have been subsequently delivered to the early Earth (Bailey, 2001).

Ultraviolet circularly polarized light (UV CPL) irradiation provides a way to obtain enantiomeric excesses (ee). The gain in ee values achievable during photolysis of a racemate is a function of the magnitude of the anisotropy factor g (i.e., the difference between the two enantiomers’ adsorption coefficients for a CPL of given frequency (g=Δ‎e/e)) and of the extent of reaction. This is a strict physical parameter that will govern the possible extent of ee obtained before the enantiomers are both destroyed. It so happens that this factor has a very low value for amino acids (0.02), and that the maximum estimated ee possible, even with 99.99% photodestruction, is 9.2% (Balavoine et al., 1974). Solid-state films of racemic D,L-leucine were irradiated with an intense, circularly polarized synchrotron radiation (CPSR). After 70% photodecomposition, the highest gain in enantiomeric excess value was found to be +2.6 in D-leucine when irradiating with r-CPSR at 182 nm. Irradiation with l-CPSR resulted in an enantiomeric excess value of +0.88% in L-leucine (Meierhenrich et al., 2005). Irradiation of ice mixtures of H2O/CH3OH/NH3 by circularly polarized light provided 16 distinct amino acids. L-enantiomeric excesses were measured in five of them, with enantiomeric excess values ranging from −0.2% to −2.54%. The results support an astrophysical scenario in which the solar system was formed in a region where icy grains were irradiated during the protoplanetary phase by an external source of circularly polarized light, inducing a stereo-specific photochemistry (Modica et al., 2014).

Toward Stochastic Prebiotic Chemistry

By demonstrating in 1953 that it was possible to form amino acids—the building blocks of proteins—from methane, a simple organic molecule containing only one carbon atom, Stanley Miller generated the ambitious hope that chemists will be able to create life in a test tube. Despite the tremendous efforts of chemists tackling the problem, it must be acknowledged that the dream has not yet been accomplished. This calls for us to truly review our approaches to chemical origins of life. A new strategy could be to more closely mimic the primordial soup and to let random chemistry run. By doing so, chemists will no longer control each step of the process, but it is perhaps the price to pay to realize the dream of creating a simple life in the laboratory. A pioneer approach should adhere to geologically relevant environments pertinent to the early Earth. This aspect of experiments in the literature is too often poorly constrained or, indeed, entirely ignored. A rational methodology involving chemical systems and their stochastic reactivity on heterogeneous geological surfaces has been proposed, based on the relationship between prebiotic chemistry and the geological conditions of the Hadean Earth (Dass et al., 2016). The interaction of stochastic prebiotic chemistry with compositionally heterogeneous rocks, such as silica-based hydrogels upon heterogeneous Hadean basalts, brings along a higher level of complexity in addition to the inherent heterogeneity of chemical systems.

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