December 2016 Issue Table of Contents
The onset of life on Earth was preceded by prebiotic chemistry in which complex organic molecules were formed from simpler ones in the presence of energy sources. These prebiotic organics were either synthesized on Earth itself (endogenously) or synthesized extraterrestrially (exogenously) and then delivered to Earth. Organics have been detected in space and have been successfully synthesized under experimental conditions simulating both extraterrestrial environments and early Earth environments. Homochirality and enantiomeric enrichment of organic molecules, which were once considered to be biosignatures, can, in fact, be achieved abiotically. It is important to determine conditions that allow the formation of prebiotic organics and those that preserve them against degradation.
Keywords: prebiotic, hydrothermal, meteorites, cosmic dust, organics, chirality, enantiomeric excess
Life was not formed in one step. Rather, life was formed as a sequence of physico-chemical processes that caused prebiotic chemistry to transition into biology with the emergence of the first cells. Organic monomers may have first formed in a warm “primordial soup,” then polymerized into functional molecules and eventually evolved to more complex life. Important steps in the prebiotic chemical evolution on Earth likely took place during the Hadean and early Archean Eons lasting from the time of Earth’s formation to the end of the late heavy bombardment at ~3.8 Ga. Abiogenic synthesis of organic compounds must have occurred in the atmosphere, in aqueous solutions, and at the mineral–water interface in multiple geological settings (Fig. 1).
It was once believed that organic molecules were synthesized only on Earth. However, spectroscopic investigations of the interstellar medium and the direct analysis of cosmic dust particles, meteorites, asteroids, and comets have revealed that a rich variety of organic compounds exists in space. These organics span a diverse range: from simple molecules, such as hydrogen cyanide (HCN), up to complex macromolecules. These various extraterrestrial sources could have contributed to the total inventory of organics on early Earth, leading to the origin of life (Anders 1989). It has been estimated that ~1,000–10,000 tons of organic matter was delivered annually to Earth 4.2 billion years ago by comets alone. When Carl Sagan famously said in the US television series Cosmos: A Personal Voyage, “We are made of star stuff,” he may have meant not only that it is the pure elements that are made in stars but also that the very organic molecules that are required by life are also produced in space.
Unfortunately, there is practically no geological record of this early chemistry. Thus, it is of special importance to analyze compounds extracted from exogenous sources and also those compounds synthesized in laboratory experiments that attempt to simulate natural terrestrial and extraterrestrial environments. However, experimental conditions must reflect realistic early geological conditions (Sahai et al. 2016 this issue).
In this article, we present a brief discussion on the possible sources of organics on the primordial Earth. Readers are also guided to excellent reviews on the complex organic compounds detected in exogenous sources and synthesized in experiments that simulate endogenous processes (McCollum 2013; Kwok 2016; Sandford et al. 2016).
Terrestrial Prebiotic Organic Sources
More than seven decades ago, Urey and Miller synthesized organic molecules in an experiment designed to simulate lightning in what had been presumed to be a reducing atmosphere on early Earth. An electrical discharge was passed through a mixture of CH4, H2, and NH3 gases. The resulting organic products detected included glycine, alanine, aspartic acid, and a-aminobutyric acid (Table 1). More recently, other amino acids, urea, carboxylic acids, amines, and other compounds have also been detected (Cleaves et al. 2008). In experiments where H2S was used along with the other reducing gases, sulfur-containing amino acids and amines were formed (Bada 2013). However, our present understanding is that the Earth’s early atmosphere was not highly reducing but, rather, was redox neutral, with CO2, N2, and H2O as the dominant gases. Under redox-neutral conditions, amino acids can still be generated in the presence of antioxidants (such as ascorbic acid or ferrous iron) (Cleaves et al. 2008) (Table 1).
In the experiments mentioned above, as well as in some experiments discussed below, amino acid synthesis likely follows the Strecker pathway. In this process, aminonitrile [H2NCH(R)CN] is first formed by a condensation reaction of cyanide, aldehydes, or ketone with ammonium salt, and is then converted to amino acids by hydrolysis and oxidation (McCollum 2013). Unlike amino acids, the synthesis of purines and pyrimidines has not been achieved in experiments simulating atmospheric synthesis.
Earth Surface Environments
The synthesis of organic compounds from the simple starting compounds of NH3, H2O, CO2, and HCN typically involves condensation, addition, hydrolysis, and/or redox reactions. Condensation reactions best proceed in the absence of aqueous solutions. Moreover, many of the synthetic reactions require high concentrations of the reactants. Intertidal pools, inland evaporitic playas, flanks of volcanic crater lakes, sedimentary pores in the unsaturated zone of groundwater, and altiplano desert soils offer a range of geological environments that undergo periodic wetting and drying cycles, freeze–thaw cycles, and sublimation, all of which have the potential to facilitate condensation reactions and concentrate compounds.
A wide range of biologically relevant organic compounds have been synthesized by heating NH3, H2O, and HCN in aqueous solutions at temperatures between 30 °C to 100 °C (Oró 1961). Combining HCN with H2O yields formamide [HC(O)NH2], a molecule that is highly reactive and that can subsequently be reacted to yield most of the precursor compounds required for biologically important molecules, such as amino acids, glycinamides, and even adenine and imidazole. The addition of formaldehyde (CH2O) to the system yields monosaccharides. Using HCN chemistry, nucleotides (i.e. nucleobase + ribose + phosphate), amino acids, and phospholipids can all be synthesized (Sutherland 2016).
Despite these experimental successes in prebiotic synthesis, they are not geochemically realistic. In most cases, high concentrations of reactants are typically required. For example, 1 M phosphate is required for nucleotide synthesis (Sutherland 2016). Oró (1961) used 1–11 M HCN. Amino acids were not detected in studies where more dilute solutions were used (McCollum 2013). Furthermore, although formamide is a versatile compound for prebiotic synthesis, its high reactivity means that it may not survive long enough in natural environments in order to build up to the concentrations used in the experiments. Apart from the problems with high concentrations, in some synthesis reactions, purification and separation steps of the intermediate compounds may be required at different stages of the reaction. The geological environments to accumulate such high reactant concentrations, as well as the correct sequence of physical separation processes, remain to be elucidated.
High-temperature hydrothermal vents emit fluids at temperatures of ~250–400 °C, containing reduced transition metals and high concentrations of dissolved gases CO2 and H2S, all of which results in very acidic pH values of ~2–3. An example is the Rainbow hydrothermal field in the Azores region of the Atlantic Ocean. The vent solutions come in contact with cool, alkaline ocean water, which creates concentration, redox, and thermal gradients that can be exploited for the synthesis of organic compounds and metabolic reactions. Dark-colored metal sulfide minerals and CH4 and H2 are formed at these “black smoker” vents. Interestingly, some iron sulfide minerals, such as greigite, have crystal structures that are similar to the structures of transition metal–sulfide clusters at the active sites of many metabolically related enzymes.
A fundamentally different kind of oceanic vent system, hosted by ultramafics, gives rise to the so-called “white smokers” (e.g. the Lost City and the Strytan hydrothermal fields of the mid-Atlantic and north of Iceland, respectively). These vent fluids have milder temperatures (60–90 °C), alkaline pHs of ~9–11, and precipitate white-colored calcium and magnesium carbonates. The hydrothermal activity in these systems is driven by the chemical reactions between seawater and the mantle peridotite that underlies the oceanic crust. Olivine in peridotite reacts with seawater and dissolved CO2 to form serpentine, magnetite, and either brucite or magnesite, while releasing dissolved silica and H2 or CH4.
Both black and white smokers could provide the ideal environment for supporting the emergence of the earliest metabolisms (methanogenesis, acetogenesis, and methanotrophy) without the need for a preceding RNA world. Amino acid oligomers were detected in experiments simulating black smoker hydrothermal systems (Kawamura et al. 2005). Organics have been detected in both Rainbow and Lost City vent fluids, but the 13C isotopic analyses do not preclude a partial biological origin (Konn et al. 2009).
Various aliphatic hydrocarbons, aromatic hydrocarbons, and carboxylic acids have been produced under simulated hydrothermal conditions (McCollum 2013). Organics are formed abiotically by Fischer–Tropsch type (FTT) reactions in which a solid surface catalyzes the reduction of CO or CO2 by H2. But, as with the Strecker synthesis of amino acids, the FTT reactions require unrealistically high concentrations (~0.1 M or greater) of reactants, and product yields decrease with increasing carbon chain length.
In other experiments where sulfur is included, the reaction of pyrrhotite (FeS) with H2S and CO2 at 25–90 °C produces pyrite (FeS2) and H2. The H2 subsequently reduced CO2 to form alkylthiols and carboxylic acids via a pathway different from the FTT (reviewed in McCollum 2013). In the presence of FeS, pyruvate [H3CC(O)COO−] was formed at a temperature of 250 °C and 50–200 MPa pressure from alkylthiols, with formic acid being a source of CO (Cody et al. 2000). This was a milestone achievement because pyruvate is a key intermediate step in the metabolic pathways for the synthesis of many biological macromolecules. Following Cody’s work, Novikov and Copley (2013) reacted pyruvate with H2S, H2 and NH4+ with various transition metal sulfides (e.g. pyrite, arsenopyrite, marcasite, sphalerite, and pyrrhotite) at 25–110 °C. Interestingly, only a few dominant products were formed with high yields, rather than the myriad of possible compounds, and the dominant compounds are ones widely used in modern metabolic pathways. This result reflects the “sparse metabolism” concept described in Sahai et al. (2016 this issue).
The synthesis of sugars by self-condensation of formaldehyde (known as the formose reaction) requires alkaline conditions and may be catalyzed by calcite and kaolinite. The discovery of white smokers may provide plausible natural alkaline environments by which calcite might facilitate the formose reaction. However, nonselectivity of the formose reaction leads to a mixture of sugars (ketoses, aldoses, and sugar alcohols) with only a small amount of ribose, which is an essential component of nucleic acids. The concentration of formaldehyde required for the experimental system is, again, too high to be geologically plausible. The yield of ribose is increased with the addition of borate, but borate minerals are unlikely to have been abundant on early Earth.
Extraterrestrial Prebiotic Organic Sources
Cosmic dust particles range in size from nanometers to 100s of microns and were formed in various regions of space at different times in the history of the Universe. Sources include intergalactic dust, interstellar grains, circumstellar dust, and interplanetary dust particles (dust from asteroids, comets, Kuiper belt objects, and planetary rings). Meteorites and comets are larger bodies from space that sometimes arrive at Earth’s surface. A few of these extraterrestrial sources have been sampled directly: most easily by collection on Earth, but also by spacecraft that have landed on planets of our Solar System and their satellites, and also asteroids and comets and that have either sent data back to Earth or returned samples back to Earth.
Interstellar Medium (ISM)
The interstellar medium (ISM) refers to gas clouds in neutral and ionic states, cosmic rays between stars, and cosmic dust. Infrared, microwave, and millimeter-wave spectroscopies have been used to probe space for the spectral signatures of organic molecules. Gas-phase saturated and unsaturated hydrocarbons, alcohols, aldehydes, carboxylic acids, ethers, and N-bearing compounds have all been detected in the ISM. Of particular interest are glycolaldehyde [HOCH2CH(O)], which is related to sugars, and cyanamide (H2NCN), formamide [HC(O)NH2] and acetamide [CH3C(O)NH2], which are related to peptides. Imidazole, a component of nucleotides, is one of the heterocyclic compounds of C, N and H that has been detected in the ISM (Kwok 2016). Nitriles, which are the precursors of amino acid, have also been detected directly in the ISM using millimeter-wave emission spectroscopy (Kalenskii et al. 2000). There are many spectral lines in the ISM that have yet to be assigned to specific compounds.
It is now generally accepted that gas-phase reactions alone cannot be responsible for the synthesis of such a diverse array of organics, especially for complex molecules. Interstellar grains are nanometer-size grains found in the ISM and are composed of an amorphous silicate or carbon core with outer icy layers of H2O, CH4, NH3, CO, CO2, CH3OH, and HCOOH among others (Fig. 2). The surface of the cores is believed to catalyze the reactions of H, O, N and C to form organic molecules (Burke and Brown 2010).
Interplanetary Dust Particles and Micrometeorites
Interplanetary dust particles (IDPs) are nanometer to ~ 1–100 mm-size cosmic dust particles, and they can be collected from Earth’s stratosphere by high-flying aircraft. They are usually porous, anhydrous, multicomponent grains of inorganic and organic phases, that were formed in the pre-solar and solar accretionary disk. Comets and asteroids are the sources of IDPs. Tens of thousands of tons of IDPs enter the Earth’s atmosphere annually, and the rate would have been much greater on early Earth (Kwok 2016).
The chemical composition of the IDPs reflects their diverse origins. The inorganic phases of IDPs consist of glassy silicates and grains of chondritic composition. The crystalline phases within the chondritic grains include Mg-olivine, Mg-pyroxene, and feldspathoids, with small quantities of Fe–Ni alloys, sulfides, and calcium–aluminum-rich inclusions. Pre-solar grains also include refractory inorganic materials such as SiC, graphite, corundum, and spinel. The carbonaceous component of an IDP can be up to 50 wt%, ranging in organic species from simple aliphatic and aromatic compounds to macromolecular polyaromatic hydrocarbons. Many IDPs show only minimal aqueous alteration. Micrometeorites are similar to IDPs except that they are collected from deep ocean sediments and from the Greenland and Antarctica ice sheets.
Meteorites are the surviving fragments of asteroids that reach the Earth’s surface. Among meteorites, the most primitive are the carbonaceous chondrites, which contain ~2 wt% carbon. Organic compounds were first detected by Nagy et al. (1962) in the Orgeuil carbonaceous chondrite, which fell to Earth in 1864. Since then, more than 14,000 organic compounds, including 70 amino acids and other biologically important organic molecules, have been detected (Table 1, Table 2) (Sephton 2002; Llorca 2004; Callahan et al. 2011). The major portion (up to 70%) of the organics in meteorites is present as complex insoluble organic matter (Kwok 2016) (Fig. 3). The insoluble organic matter consists of high molecular weight compounds, that contain C, H, N, O, S and P, and is similar to kerogen, which is of biological origin on Earth. Carbon isotopic analysis of these compounds suggest an extraterrestrial origin. The organic matter appears to be preferentially associated with hydrothermally altered minerals in some carbonaceous chondrites and these organics can also undergo reactions during hydrothermal processing.
Asteroids and Comets
Spacecraft have remotely examined some asteroids and comets and landers have sampled their surfaces. Hydrogen cyanide and its polymers have been found on asteroids and comets. For example, infrared spectroscopy of the asteroids 24 Themis and 65 Cybele showed the presence of water ice and red-colored material similar to “tholins.” The latter are complex macromolecular organic compounds formed artificially by ultraviolet radiation of N2, NH3 and CH4. The Stardust spacecraft collected IDPs from the coma of comet 82P/Wild 2 in 2004 and returned the samples to Earth in 2006. Along with various other organics, glycine was detected in these particles. Hydrogen and nitrogen isotopic analyses of these particles indicate an extraterrestrial interstellar or protosolar origin (Kwok 2016; Sandford et al. 2016). The Rosetta spacecraft remotely examined comet 67P/Churumov–Gerasimenko and the Philae lander directly examined this comet’s surface in 2014. Nonvolatile organic compounds, which are probably polycyclic aromatic hydrocarbons, plus sulfides, an Fe–Ni alloy, and an unknown source of P, were identified (Altwegg et al. 2016).
Moon and Other Planets in Our Solar System
Various probes and landers have also been sent to the planets and their satellites in our Solar System. No organics have been detected on the Moon. But CH4 and H2O ice are known to exist on Mars. Europa, a satellite of Jupiter, has a water-ice crust and probably a liquid water “mantle.” Among the satellites of Saturn, water ice, methane, propane, and formaldehyde have been detected on Enceladus, whereas Titan has an atmosphere composed mainly of nitrogen, methane, and H2, plus other organics such as hydrocarbons, HCN, cyanoacetylene (HC3N), CO, CO2, and liquid hydrocarbon lakes at its poles. The New Horizons spacecraft observed tholin-like dark reddish material in the polar regions of Pluto’s moon Charon.
Homochirality of Life and Enantiomeric Excess of Amino Acids
Some of the molecular building blocks of life, such as amino acids and sugars, are chiral: that is, they have non superimposable mirror image structures, known as enantiomers. Chiral molecules have an asymmetric carbon center with four different substituents (Fig. 4). Enantiomers have identical physical and chemical properties except that they interact selectively in chiral environments. Therefore, 50% of each enantiomer (a racemic mixture) is expected in any abiotic chemical reaction.
However, chiral molecules formed biologically show a characteristic preference of one enantiomer over another. For example, sugar residues in nucleotides and polysaccharides are found solely in D-configuration, whereas amino acids are primarily present only in the L-configuration in proteins. The origin of homochirality is one of the key issues in understanding the origin of life. The excess of one enantiomer over another is called an enantiomeric excess. Because homochirality is a characteristic feature of life on Earth, detection of enantiomeric excess in extraterrestrial sources was once considered as a biosignature.
Because extraterrestrial organics are assumed to have formed abiotically, it was expected that they would be found in racemic quantities, that is they have equal concentrations of L- and D- isomers. It was tremendously interesting, then, that significant excesses of the D- isomer of sugar-derived compounds (sugar acids and sugar alcohols) (Cooper and Rios 2016) and the L- isomer of a specific subfamily of amino acids (a,a-dialkyl-a-amino acids) and were found in carbonaceous chondrites (Cronin and Pizzarello 1999; Glavin and Dworkin 2009). Isovaline (2-amino-2-methylbutanoic acid), for example, was found to have L- isomeric excesses of 18.5% in the Murchison meteorite, 15.2% in the Orgeuil meteorite, and 6.0% in the Murray meteorite. Thus, enantiomeric enrichment must have occurred abiotically and is not necessarily a biosignature.
If enantiomeric excess is not exclusively a biosignature then the origin of abiological chiral selection must be explained. Many mechanisms might produce enantiomeric excess. In space, the interaction of chiral molecules with circularly polarized light (CPL), which is itself chiral, could introduce enantioselective synthesis up to a few percent. However, the large excesses observed in meteorites cannot be explained solely by an ultraviolet (UV) CPL hypothesis, and additional mechanisms are being investigated.
Minerals such as clays, calcite, and quartz possess chirality and may exhibit stereoselective adsorption for certain amino acids. However, an excess of one chiral form of the mineral over another would be required for an enantiomeric excess to develop. Such an enantiomeric excess of chiral minerals has never been shown.
By whatever means enantiomeric excess began, even a small enrichment could be amplified through subsequent processes such as the preferential sublimation of “conglomerate-forming” crystals. For example, Fletcher et al. (2007) found more than 80% enantiomeric excess of L-leucine in a sublimate compared to a starting value of only 10%.
Forming and Sustaining Organic Molecules
The formation of reduced C compounds from CO2 or CO, and the polymerization of monomers by condensation reactions, are generally thermodynamically unfavorable at ambient temperatures and in the presence of water. Energy must be put into the system to drive the reactions forward. Various energy sources such as UV radiation, cosmic rays, X-rays, hypervelocity impacts, volcanic eruptions with lightning, geothermal heat, and redox gradients were available in the interstellar medium and on the young Earth for the abiotic synthesis of organic molecules. Conversely, under different environmental conditions, many of these same energy sources may serve to degrade organic molecules.
The organics in meteorites survive entry into Earth’s atmosphere because only the outer layers of the meteorite are affected by frictional heating while the interior of a meteorite remains cold. Furthermore, an organic haze in Earth’s early atmosphere might have protected organic molecules from degradation by short-wave UV-radiation, analogous to the role played by ozone in the modern atmosphere.
Oceans may also have protected dissolved organics from UV radiation because the depth of penetration of UV light is ~200 m. On the other hand, the organics would have been diluted and/or hydrolyzed in water. The deleterious effects of dilution and hydrolysis could have been rescued by thermomelanoid, which is an insoluble glycine polymer. When hydrolyzed, thermomelanoid serves as a source of alanine, aspartic acid, and glycine peptides (Fox et al. 2015).
Heating simple organic molecules or their precursors can yield biologically relevant molecules, but may also result in their destruction. Amino acids, for example, may be shielded from thermal degradation by adsorption within the interlayer spaces of clay minerals (Dalai et al. 2016).
The thermal and chemical gradients at hydrothermal vents on the Earth’s surface may have played an important role in thermodynamically favorable reactions for organic synthesis. These reactions may have been catalyzed by transition metal–sulfide minerals such as pyrite. However, destructive free radicals are also generated photo catalytically at the surface of these sulfides and at the surfaces of the ultramafic minerals that constitute peridotite and komatiite.
The yield of relevant products in abiotic synthesis reactions is often very small. For stable and for reactive molecules, achieving the relevant concentration to form a protocell would have required processes such as adsorption, evaporation, freezing, and sublimation, as well as a continuous flux of reactants.
An interesting aspect of prebiotic organic chemistry is the relative scarcity of phosphorous-bearing compounds detected in space. Phosphorus mononitride has been detected in the interstellar medium, low concentrations of apatite and merrillite (whitlockite) are found in chondrites and chondritic grains, and schreibersite occurs in iron meteorites. Intriguingly, despite the low abundance of phosphorous, it is unquestionably one of the essential elements for life.
The organic inventory of early Earth contained contributions from terrestrial and extraterrestrial sources. In order to understand prebiotic organic synthesis processes on Earth it is important to conduct experiments under conditions that represent plausible early Earth environmental conditions. The identification of nucleic acid monomers and lipids, or their precursors, in extraterrestrial sources, as well as the synthesis of these compounds experimentally, remains as open avenue of research.
Sahai gratefully acknowledges financial support from the following grants: NSF EAR Geobiology and Low-Temperature Geochemistry #1251479; the Simons Collaboration on the Origins of Life (SCoL) award #290359 from the Simons Foundation, NY; and “startup” funds from the University of Akron.
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