The evolution of organic matter in space

Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 The evolution of organic matter in space Pascale Ehrenfreund, Marco Spaans and Nils G. Holm Phil. Trans. R. Soc. A 2011 369, doi: 10.1098/rsta.2010.0231, published 10 January 2011 Supplementary data "Audio Supplement" http://rsta.royalsocietypublishing.org/content/suppl/2011/01/05/ 369.1936.538.DC1.html References This article cites 111 articles, 13 of which can be accessed free http://rsta.royalsocietypublishing.org/content/369/1936/538.full. html#ref-list-1 Article cited in: http://rsta.royalsocietypublishing.org/content/369/1936/538.full.html#r elated-urls Subject collections Articles on similar topics can be found in the following collections astrobiology (23 articles) interstellar medium (18 articles) Email alerting service Receive free email alerts when new articles cite this article - sign up in the box at the top right-hand corner of the article or click here To subscribe to Phil. Trans. R. Soc. A go to: http://rsta.royalsocietypublishing.org/subscriptions Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 Phil. Trans. R. Soc. A (2011) 369, 538–554 doi:10.1098/rsta.2010.0231 REVIEW The evolution of organic matter in space B Y P ASCALE E HRENFREUND1,2, *, M ARCO S PAANS3 AND N ILS G. H OLM4 1 Space Policy Institute, 1957 E Street, Suite 403, 20052, Washington DC, USA Institute of Chemistry, Astrobiology Laboratory, 2300 RA Leiden, The Netherlands 3 Kapteyn Astronomical Institute, PO Box 800, 9700 AV Groningen, The Netherlands 4 Department of Geological Sciences, Stockholm University, Stockholm, Sweden 2 Leiden Carbon, and molecules made from it, have already been observed in the early Universe. During cosmic time, many galaxies undergo intense periods of star formation, during which heavy elements like carbon, oxygen, nitrogen, silicon and iron are produced. Also, many complex molecules, from carbon monoxide to polycyclic aromatic hydrocarbons, are detected in these systems, like they are for our own Galaxy. Interstellar molecular clouds and circumstellar envelopes are factories of complex molecular synthesis. A surprisingly high number of molecules that are used in contemporary biochemistry on the Earth are found in the interstellar medium, planetary atmospheres and surfaces, comets, asteroids and meteorites and interplanetary dust particles. Large quantities of extra-terrestrial material were delivered via comets and asteroids to young planetary surfaces during the heavy bombardment phase. Monitoring the formation and evolution of organic matter in space is crucial in order to determine the prebiotic reservoirs available to the early Earth. It is equally important to reveal abiotic routes to prebiotic molecules in the Earth environments. Materials from both carbon sources (extra-terrestrial and endogenous) may have contributed to biochemical pathways on the Earth leading to life’s origin. The research avenues discussed also guide us to extend our knowledge to other habitable worlds. Keywords: astrobiology; early Universe; interstellar chemistry; solar nebula processes; extra-terrestrial delivery; hydrothermal vents 1. The evolution of carbon in the Universe The Universe is currently estimated to be approximately 13.7 Gyr old [1]. During Big-Bang nucleosynthesis, only H and He and traces of a few other light nuclei, such as D, T, Li and Be, were formed. Since the Universe was expanding, cooling and decreasing in density, heavier elements (called metals by astronomers) could not be formed during its early history, up to 500 Myr after the Big Bang. The *Author for correspondence (pehren@gwu.edu). One contribution of 17 to a Discussion Meeting Issue ‘The detection of extra-terrestrial life and the consequences for science and society’. 538 This journal is © 2011 The Royal Society Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 Review. Organic matter in space 539 triple-a process (3 × 4 He → 12 C) in the cores of stars is the fundamental source of carbon, the basis of organic chemistry. After hydrogen is exhausted, further nuclear reactions start in the core of stars with masses greater than half a solar mass leading to carbon and heavier elements, and up to 56 Fe for the more massive stars. Heavier elements than iron are formed during the final stages of stars in stellar explosions by neutron absorption (s and r processes). In this phase, no equilibrium can be reached: the stars undergo mass loss either in a smooth way or in violent way, leading to the enrichment of the interstellar medium. Analytical arguments [2], as well as numerical simulations [3], showed that a significant amount of star formation could have occurred when the Universe was only 100 Myr old in the standard cold dark matter theory. The high opacity to Thomson scattering of the Universe found by the Wilkinson Microwave Anisotropy Probe provides support for this theory. The first stars (so called population III or zero metallicity stars) are expected to form in dark matter halos, growing from primordial fluctuations, in which the baryonic gas could cool efficiently enough. Although atomic cooling can ensure temperatures down to 10 000 K, molecular cooling is necessary to reach lower temperatures. The dominant cooling molecule at these stages is believed to be molecular hydrogen, H2 , formed through H + e− → H− and H− + H → H2 + e− [4]. First stars are believed to be more massive than present day ones because H2 cooling could not decrease the temperature as low as metals do. The Jeans mass is therefore higher, up to 100–1000 solar masses [5]. These massive stars are very short lived, with life times of less than 30 Myr and can no longer be observed. When they explode, large amounts of metals, in particular carbon and oxygen, are distributed. Subsequently, dust is synthesized and dispersed throughout the Universe [6]. There is evidence that a copious amount of molecules, such as O2 , CO, SiS, SO, CO and SiO, may form in the ejecta of Pop III progenitor supernovae [7] that can be recycled in the next generation of forming stars. The recent detection of hyper metal-poor stars (HMPs) in the Milky Way halo also provides important constraints for early star formation processes [8,9]. The observed HMP stars have an Fe/H ratio less than 1/100 000 of the solar ratio. They have an overabundance in C and O relative to Fe, and are slightly less massive than the Sun. Their modest masses allow them to exist for longer than 10 Gyr, and thus to act as ‘fossil’ record. Investigations of those stars may provide clues regarding the properties of the initial generation of stars and supernovae that distributed the first heavy elements in the early Universe. The star BD+44 493 has been recently identified as the brightest extremely low-metallicity star among all objects reported [10]. Carbon appears to be favoured as a formation product of the first generation of stars. Molecules like CO and water, formed once oxygen and carbon atoms were present (less than 1 Gyr after the Big Bang), as well as very small grains, cool interstellar gas much more efficiently than H2 . This stimulates cloud fragmentation and triggers the formation of low-mass stars like our Sun [11–14]. Low-mass stars live much longer, approximately 10 Gyr for the Sun, a duration that enables the formation of terrestrial planets and possibly the emergence of life. Once the first generation of population III stars had formed and exploded as supernovae about 500 Myr after the Big Bang, the subsequent existence of metals and dust is expected to lead to the efficient formation of molecules like Phil. Trans. R. Soc. A (2011) Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 540 P. Ehrenfreund et al. WC IV (×10–8) 10 1 0.1 2 4 redshift 6 Figure 1. The evolution of the intergalactic ion C IV (C3+ ) abundance as a function of redshift, in units of its contribution to the closing density. The constancy of the curve indicates that vigorous star formation was already underway when the Universe was only 7% (at redshift z = 6) of its present age. Reproduced with permission from Simcoe [19]. CO, water, hydrides and carbon chains [15]. Indeed, high excitation CO emissions from the distant quasar SDSS 114816.64 + 525150.3 at redshift z = 6.4 have been detected, indicating that CO, one of the most important coolants of interstellar gas, has been present in the Universe since approximately 800 Myr after the Big Bang [16]. Furthermore, detections of C and C+ have been made and upper limits on HCN and water exist [17]. Somewhat more recently, at a redshift z = 3.9, the gravitationally lensed quasar APM 08279 allows the inner 200 parsecs of the galaxy to be probed. Large amounts of warm (100 K) CO gas and warm dust (assuming a frequency squared absorption-coefficient dependence) appear to be present, indicative of active star formation [18]. Clearly, carbon and dust surface chemistry was occurring already in the earliest epochs of the Universe. That these objects with a significant amount of carbon are not flukes, is shown in figure 1, where the relative amount of carbon is presented as a function of redshift. In this, redshifts of 1 and 6 mean 35 and 7 per cent of the present age of the Universe, respectively. Clearly, carbon and thus star formation was already very much present in the young Universe [19]. This fits well with the star formation and metal-production history of the Universe [20], where the metals produced by massive stars lead to the formation of molecular gas and thus more stars. For a metallicity of 1 per cent of solar and up, one develops a multi-phase interstellar medium (ISM) that supports a cool dense phase, with a density larger than 100 cm−3 and a temperature less than 100 K, in which stars form and complex (carbon-chain) molecules can be produced [21]. Such a metallicity is certainly reached in the quasar sources mentioned above, and an active carbon chemistry therefore appears to have been in place for at least the past 10 Gyr. Closer to home, many if not all active galaxies are enjoying an active carbon chemistry, as exemplified by species such as CO, HCN, HNC, HCO+ , CH3 OH, H2 CO, C2 H and polycyclic aromatic hydrocarbons (PAHs; e.g. [22–24]). Some galaxies form stars with a very high rate, so-called starburst galaxies like Arp 220 Phil. Trans. R. Soc. A (2011) Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 Review. Organic matter in space 541 and M82. Carbonaceous molecules are detected in those systems as well, even in the presence of strong mechanical feedback owing to supernova explosions and outflows [25]. UV radiation produced by stars or X-ray photons created by an accreting supermassive black hole can destroy complex molecules in the nuclei of galaxies [26]. Nevertheless, species like CO may survive even such extreme environments, already in the early Universe at metal-enrichment levels of only a few per cent [27]. Also, PAHs have been detected with Spitzer out to high (z > 1) redshift (e.g. [28]). The cycle of birth and death of stars that was initiated by population III stars constantly increases the abundance of heavy elements in the interstellar medium, a crucial prerequisite for rocky-planet formation [29,30]. Understanding the early and active Universe is thus extremely relevant to the question of terrestrial-planet formation and consequently life. 2. The complexity of organic matter in space (a) Interstellar clouds Interstellar molecular clouds and circumstellar envelopes are factories of complex molecular synthesis [31–33]. Interstellar clouds constitute a few per cent of galactic mass and are composed primarily of H and He. They are enriched primarily by matter ejected from evolved stars and can vary strongly in their fundamental physical parameters such as temperature and density. Dominated by gas, interstellar material also contains approximately 1 per cent of small micron-sized particles. Gas-phase and gas–grain interactions lead to the formation of complex molecules. Surface catalysis on solid interstellar particles enables molecule formation and chemical pathways that cannot proceed in the gas phase owing to reaction barriers [34,35]. H2 is by far the most abundant molecule in cold interstellar regions, followed by CO, the most abundant carbon-containing species, with CO/H2 ∼ 10−4 . CO is characterized by a high binding energy (11.2 eV) and strongly influences the chemistry in interstellar clouds. Two main types of interstellar clouds drive molecular synthesis. In cold dark clouds, the temperature is low (approx. 10 K) and therefore the sticking coefficients of most atoms and molecules are close to unity, leading to a freeze out of practically all species (except H2 and He). The high density in dark clouds (up to approx. 106 cm−3 ) attenuates UV radiation and offers a protected environment for the formation of larger molecules by gas-phase reactions and ice chemistry on grains. A large number of complex organic gas-phase molecules was identified through infrared, radio, millimetre and sub-millimetre observations (www.astrochemistry.net lists more than 150 molecules). Among them are nitriles, aldehydes, alcohols, acids, ethers, ketones, amines and amides, as well as longchain hydrocarbons. The main species observed in interstellar ice mantles are H2 O, CO2 , CO and CH3 OH, with smaller admixtures of CH4 , NH3 , H2 CO and HCOOH [36]. A recent c2d (core to disks) Spitzer survey of ices investigated the 6–8 mm region that displays the prominent bending mode of water ice. Five independent components that can be attributed to eight different carriers [37] have been identified. Observations of CO2 in low-mass protostars showed high abundances (average of 32% relative to water ice) [38]. CH4 ice was detected in 25 out of 52 targets, with abundances ranging from 2 to 8 per cent relative to water ice and reach 13 per cent in a few sources [39]. Phil. Trans. R. Soc. A (2011) Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 542 P. Ehrenfreund et al. Diffuse interstellar clouds are characterized by a low density (approx. 103 atoms cm−3 ) and temperatures less than or equal to 100 K. Ion–molecule reactions, dissociative recombination with electrons, radiative association reactions and neutral–neutral reactions contribute to gas-phase processes and influence interstellar chemistry [40]. A variety of small molecules, including CO, CH, CN, OH, C2 , C3 and others, are observed [41]. Gaseous PAHs are highly abundant, with fractions of about 10−7 [42]. Carbonaceous grains composed of macromolecular aromatic networks account for most of the molecular carbon fraction in these clouds as evidenced by a ubiquitous strong UV absorption band at 2175 Å [43]. Amorphous carbon, hydrogenated amorphous carbon, diamonds, refractory organics and carbonaceous networks such as coal, soot, graphite and quenchedcarbonaceous condensates have been proposed as possible carbon compounds [31,42,44,45]. PAHs are observed to be widely distributed in galactic and extragalactic regions [42,46–49]. In diffuse interstellar clouds, dust interacts with hot gas, UV radiation and cosmic rays, and evolves or gets destroyed in shocks and by sputtering. Strong differences in the dust component of dense and diffuse interstellar clouds exclude rapid cycling of cloud material [50]. The formation pathway of solid carbonaceous matter is not yet understood. However, circumstellar envelopes are identified as factories of complex molecular synthesis [32]. Figure 2 shows a route to the formation of PAHs and soot material that has been proposed over two decades to occur in the shielded environment of stellar envelopes. (b) Solar-System materials The gravitational collapse of an interstellar cloud led to the formation of the protosolar nebula from which planets and small bodies of our Solar System formed [54]. Observations of protoplanetary disks show that gas and solids drift inward in time. Solids migrate inwards faster than gas, and small particles grow to kilometre-sized bodies that accrete to planets. The chemical composition of protoplanetary disks is expected to hold clues to the physical and chemical processes that influence the formation of planetary systems. Recently, it has been reported that the protoplanetary disks of AA Tauri possess a rich molecular emission spectrum in the mid-infrared, indicating a high abundance of simple organic molecules (HCN, C2 H2 and CO2 ), water vapour and OH [55]. Data from recent space missions, such as the Spitzer telescope, Stardust and Deep Impact, show that the dynamic environment of the solar nebula with the simultaneous presence of gas, particles and energetic processes, including shock waves, lightning and radiation (e.g. [56]) can trigger a rich organic chemistry. Turbulent motion leads to radial mixing of the products within the disk [57,58], which has been confirmed by Stardust data [59]. The carbonaceous inventory of our Solar System therefore contains a mixture of material that was (i) highly processed by exposure to high temperatures and radiation, (ii) newly formed within the solar nebula, and (iii) captured as relatively pristine material with significant interstellar heritage. Many organic compounds are observed or sampled from our Solar System, including planetary surfaces/atmospheres, comets and interplanetary dust [31,60–62]. More than 50 molecules have been identified in cometary comae [63,64]. The analysis of carbon compounds in fragments of asteroid 2008 TC3 Phil. Trans. R. Soc. A (2011) Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 Review. Organic matter in space 543 Figure 2. Acetylene chemistry leading to the formation of benzene and small PAHs that subsequently build up larger structures has been proposed to occur in the shielded environments of carbon-rich circumstellar envelopes (e.g. [32,51]). Aromatic materials, in solid and gaseous form, constitute the largest fraction of organic material in the Universe [52,53]. by Jenniskens et al. [65] recently revealed interesting insights into the asteroid chemistry. Carbonaceous chondrites (meteorites) and micrometeorites, which represent fragments of cometary and asteroidal bodies, do contain a variety of organics (e.g. see [62,66] for reviews). In the soluble fraction of the Murchison meteorite, more than 70 extraterrestrial amino acids have been identified in addition to many other organic compounds, including N-heterocycles, carboxylic acids, sulphonic and phosphonic acids, and aliphatic and aromatic hydrocarbons [67–70]. However, the major carbon component in meteorite samples is composed of a macromolecular organic fraction [71]. A recent study using ultra-high resolution molecular analysis of the solvent-accessible organic fraction of Murchison shows high molecular diversity [72]. The remaining population of planetesimals not incorporated into planets exists until today as asteroids and comets. Most of the asteroids and comets are confined to stable orbits (such as the asteroid belt between Mars and Jupiter) or reservoirs in the outer Solar System (such as the Kuiper Belt) or beyond our Solar System (Oort cloud). In the early history of our Solar-System small bodies, such as comets Phil. Trans. R. Soc. A (2011) Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 544 P. Ehrenfreund et al. and asteroids, and their fragments impacted the young planets [73]. A destabilized planetesimal disk caused a massive delivery of planetesimals to the inner Solar System at 3.9 Gyr ago. This so-called Late Heavy Bombardment (LHB) phase was likely triggered by rapid migration of giant planets [74]. The large quantities of extra-terrestrial material delivered to young terrestrial planetary surfaces during this period may have provided raw material useful for protocell assembly on the Earth [73,75]. The analysis of extra-terrestrial matter in the Earth laboratories indicates that the dominant form of carbonaceous material that was delivered to young planets must have been aromatic macromolecular matter. 3. Terrestrial planets (a) Conditions on the early Earth Planet Earth was formed through a hot accretion process about 4.6 Gyr ago, which allowed only the rocky material from the inner Solar System to survive. Although many interesting geological data of the early Earth were revealed in the last decade, we still have limited knowledge regarding the exact atmospheric composition, the temperature of the oceans and geological activity. Considerable geochemical evidence supports an initiation of plate tectonics on the Earth shortly after the end of the Hadean about 3.9 Gyr ago. It is unclear if the transition to plate tectonics resulted from radioactive decay-driven mantle heating or from cooling to the extent that large lithospheric plates stabilized [76]. Any existing carbon material from the solar nebula (volatile and refractory) was destroyed during the Earth’s formation. Therefore, organic molecules found on terrestrial planets must have formed after the planetary surface cooled, or have been delivered via impacts by small bodies in the young Solar System. All terrestrial planets have been seeded with organic compounds through the impact of small bodies during Solar-System formation. There is a consensus that a combination of exogenous and endogenous sources has provided the first precursor molecules for life on the young Earth. These simple molecules reacted and assembled on catalytic surfaces (such as minerals) and formed more complex structures that later developed into primitive cells (protocells). The endogenous synthesis of prebiotic organic compounds (molecules that are involved in the processes leading to the origin of life) may have been limited to protective environments such as the oceans, owing to the hostile conditions on the young Earth, including volcanism, radiation and bombardment by comets and asteroids. Whatever the inventory of endogenous organic compounds on the ancient Earth was, it would have been augmented by extra-terrestrial material. It is estimated that these sources delivered approximately 109 kg of carbon per year to the Earth during the heavy bombardment phase of 4.5–3.9 Gyr ago [73]. Life on Earth is one of the outcomes of the formation and evolution of our Solar System and has adapted to every possible environment on planet Earth. Life on Earth can be found in extreme environments, such as hydrothermal vents, in dry deserts, the Earth atmosphere and in polar regions. These findings challenge the definition of the ‘planetary habitable zone’. Primitive life, in the form of bacteria, emerged approximately 3.5 Gyr ago [77,78]. The homologous series of long-chain aliphatic hydrocarbons found in old sedimentary rocks Phil. Trans. R. Soc. A (2011) Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 Review. Organic matter in space 545 characterized by odd-over-even carbon-number predominance is only consistent with a biological origin and indicates that, despite the hostile conditions, planet Earth was habitable in its early history [79]. Today, the Earth provides an ideal environment for life to sustain. Dynamic processes in the interior of the Earth have established a magnetosphere that protects the Earth from harmful cosmic radiation. Oceans and atmosphere enable a stable climate and temperature cycle. Our neighbour planets are less fortunate. Venus, with an average surface temperature of 500◦ C and a steamy atmosphere, is unable to sustain life at its surface. Mars, with an average surface temperature of −60◦ C and a thin toxic atmosphere, provides a hostile surface environment, but may harbour life in the subsurface. Nitrogen is an essential element of both nucleotides (genetic code, energy transfer) and proteins. Systems containing NH3 /NH+ 4 are more efficient in abiotic organic synthesis than those dominated by N2 in both aqueous and and gaseous environments [80]. The reason is that the triple bond between the atoms in molecular nitrogen is very stable and hard to break. Geochemically plausible abiotic synthesis pathways of prebiotic molecules and concentration mechanisms for nitrogen-containing molecules must eventually be found since nitrogen-based life is likely to have existed on the Earth from early Archean about 3.8 Gyr ago and onwards [81]. High ammonium contents (54–95 ppm) have been found in authigenic clays of the Isua supracrustal rocks of western Greenland, suggesting that clays were major sinks of NH+ 4 or other nitrogen compounds on the Earth’s surface already at 3.8 Gyr ago [82]. Ward & Brownlee [83] have argued that plate tectonics is necessary for the origin of life on terrestrial planets and have listed a number of reasons in support of their opinion. However, one argument that they have never mentioned is the connection between plate tectonics, hydrothermal geochemistry, and reduction of simple carbon and nitrogen compounds suitable for abiotic organic chemistry. The best location where such processes could occur would be at convergent margins during the early phases of subduction of oceanic plates. As a plate descends, fluids distilled from the plate influence, and even control, fundamental processes in the subduction zone [84]. The subducting plate, along with its fluids and altered igneous rock, interact with the over-riding plate along the subduction zone. Fluids originating in the subducting plate will rise through the upper plate containing hydrated ultramafic mantle material in its lower parts. The fluids may thus move from a relatively acidic environment in weathered basalt into an alkaline environment in serpentinized peridotite. The strong pH increase promotes the formation of carbohydrates like ribose from simple organic compounds. It also supports the synthesis of amino acids and purine nitrogen bases, as well as their condensation to nucleotides in the presence of phosphorylated ribose. (b) Hydrothermal environments Hydrogen cyanide is a key compound in abiotic synthesis of organic molecules. HCN is formed by a variety of processes driven by thermal energy, but is normally present in trace amounts [85]. HCN is, for instance, readily formed by the reaction of CO or CH4 with NH3 (figure 3) [84]. Hydrothermal systems represent regions of the highest conversion rates of nitrate and nitrite to ammonium on the Earth [86]. In general, the purine-coding elements of RNA (adenine and guanine) can be Phil. Trans. R. Soc. A (2011) Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 546 P. Ehrenfreund et al. accretionary prism over-riding plate oceanic lithosphere , ids ac s o e in rin am pu 12 d ate dr tle hy man pH H dr hy n c du ub s pH 3–5 seafloor spreading n tio 9– spreading centre mid-oceanic ridge o ati oxidation Fe(II) Fe(III) de CN off-axis hydrothermalism and fluid flow CO NH+ 3 CH4 magma chamber HCN reduction (Fe(II) Fe) Ni) (Ni(II) H2 H2O CO2 CO, CH4 adsorption on smectites and zeolites NO–3, NO–2 NH4+ Figure 3. Cartoon showing a cross-section of oceanic lithosphere, extending from the spreading centre to the subduction zone. Off-axis hydrothermal flow in the oceanic lithosphere causes oxidation of Fe(II) to Fe(III) and reduction of water to molecular hydrogen. Some Fe(II) and Ni(II) is reduced to native metals. Carbon dioxide is reduced to carbon monoxide and methane, while nitrate and nitrite may be reduced to ammonium and adsorbed on secondary minerals like smectite and zeolites. During early subduction the descending plate is heated and dehydrated. Adsorbed carbon monoxide and methane may react with ammonia and form hydrogen cyanide. The released fluid carrying hydrogen cyanide rises from an environment of relatively low pH into hydrated mantle rock of high pH. At the high pH hydrogen cyanide may form HCN oligomers as well as amino acids, purine bases, nucleosides and, perhaps, nucleotides (adapted from [84]). synthesized in the same abiotic reactions that yield amino acids [87–90]. Adenine is likely to have been the first nucleobase formed abiotically, and has been shown to remain in detectable concentrations still after 200 h at 300◦ C under fugacities of CO2 , N2 and H2 that are supposedly representative of those in marine hydrothermal systems on the early Earth [91]. The purines are formed from HCN via two routes. One route is via HCN oligomers, which may also form amino acids; the second one is via the HCN tetramer diaminomaleonitrile (DAMN) [87,88]. DAMN formation is accelerated by the presence of formaldehyde under mildly alkaline conditions (pH 9.2) [92]. Amino acids can be released by hydrolysis of HCN oligomers that form by the self-condensation of hydrogen cyanide in aqueous solution [88]. Furthermore, amino acids may be synthesized in putative prebiotic chemistries like Strecker-type reactions (synthesis of amino acids from cyanide and aldehyde in the presence of ammonia) in hydrothermal environments at fairly low temperatures (150◦ C) [93,94]. In order to participate in abiotic organic reactions, HCN must first be concentrated. One possibility is the concentration to a reservoir of ferrocyanide at relatively low pH from which free HCN can be released upon local elevation of the pH [81,95]. HCN reacts with ferrous ions to give ferrocyanide, provided that the concentration of hydrogen sulphide is low [96], like in the Lost City serpentinite-hosted hydrothermal field off the Mid-Atlantic Ridge [97]. The elevation of pH would lead to oxidation of Fe(II) and precipitation of the iron as FeOOH. This would avoid the ‘Miller paradox’, Phil. Trans. R. Soc. A (2011) Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 Review. Organic matter in space 547 which refers to the side reaction of glycolonitrile (cyanohydrin of formaldehyde) formation from free HCN and ubiquitous formaldehyde [98]. Formaldehyde and HCN, if present in the same environment, tend to react to form stable glyconitrile. On the other hand, Schwartz & Goverde [92] have shown that admixture of solutions enriched in cyanohydrins (like glyconitrile) with solutions of HCN permits oligomerization of HCN to DAMN, even under dilute conditions. An alternative model to avoid the ‘Miller paradox’ involving alkaline hydrothermal mounds as flow reactors in which strongly polar compounds such as the cyanide ion is retained by fresh FeS/Fe3 S4 membranes has been presented by Russell et al. [99–102]. According to their model, the fluctuations in pH at the interface between hydrothermal fluid and sea water would determine adsorption and desorption of the cyanide. In natural environments, the occurrence of ferrocyanides in hydrothermal systems has so far been reported only from the Kurile Islands and the Kamchatka Peninsula in the northwest Pacific Ocean [103,104]. Cohn et al. [105] have shown that adenine is far displaced towards adsorption onto pyrite, quartz and pyrrhotite, which are all common minerals of hydrothermal environments. It would, therefore, normally be useless to search for the purine bases in the fluid phase of hydrothermal systems [106]. The observed coding effect of adsorbed purine bases [107] may indicate that the role of phosphate as a constituent of polynucleotides is a secondary property, and that phosphate was originally incorporated in prebiotic systems because of its energy-transfer capacity. A couple of decades ago, many scientists believed that the abiotic formation of ribose, a constituent of RNA, occurred through the formose reaction [87,108]. The formose reaction was discovered and first described by Butlerow [109]. In this reaction, pentoses like ribose can be formed under alkaline conditions from simple organic precursors (formaldehyde and glycolaldehyde) [87,88]. The condensation of formaldehyde to sugars is catalysed by divalent cations and layered minerals, such as clays. The reaction proceeds by the stepwise condensation of formaldehyde to dimer (glycolaldehyde), trimer, etc. Under experimental conditions, it has been possible to convert as much as 50 per cent of the original formaldehyde to glycolaldehyde [110]. However, this reaction has, for a while, been an outdated concept in prebiotic chemistry. A major reason for this is that the reaction, as we have known it, is non-selective and leads to a large variety of aldoses, ketoses and sugar alcohols with only small fractions of potentially bioactive compounds such as ribose [90,111,112]. A general opinion has been that if ribose were used in the first RNA, an unknown selection process must have operated to segregate ribose from the other sugars that were formed. A second reason why the formose reaction has been outdated is that the reaction proceeds at a significant rate only under naturally ‘improbable’ conditions, like under highly alkaline conditions [81,87,108,113]. Natural environments with the pH conditions required for the abiotic formation of carbohydrates have previously been considered to be relatively rare on the Earth. However, the recent discovery of alkaline hydrothermal systems in ultramafic rocks, such as the Lost City Hydrothermal Field on the Mid-Atlantic Ridge [97,114–116] and the Mariana Trench [94,84], indicates that alkaline environments may be much more common on the Earth than was thought just a few years ago. Phil. Trans. R. Soc. A (2011) Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 548 P. Ehrenfreund et al. Because of the postulated difference in requirements for the formation of the ribose and the nitrogen base, the spontaneous formation of RNA under prebiotic conditions on the Earth has been doubted [90]. The differences in required environment may, however, be illusive. It was mentioned earlier that formaldehyde is necessary for the formation of carbohydrates in the formose reaction. Schulte & Shock [117] have shown that aldehydes may be intermediates in the formation of carboxylic acids from hydrocarbons in sedimentary basin brines, as well as in hydrothermal systems. Furthermore, they concluded that the presence of aldehydes should normally be difficult to detect in natural systems if metastable equilibrium is reached between aldehydes and carboxylic acids at expected redox conditions. On the other hand, this suggests that aldehydes are always present as reaction intermediates in cases when organic acids and hydrocarbons both exist in natural hydrothermal systems. In fact, low concentrations of formaldehyde have been identified in hot-spring environments in Iceland, Mexico and southern California [118]. At equilibrium in hydrothermal systems, carboxylic acids, aldehydes and hydrocarbons will all be present in parallel, although at different levels of concentration. 4. Conclusion The cycle of birth and death of stars that is initiated by population III stars constantly increases the abundance of heavy elements in the interstellar medium. Observations of the oldest stars show that carbon has been formed already in the very early Universe. The central star of our Solar System, the Sun, was formed many billion years after this time, and therefore contains several generations of supernova-produced metals. Tracing the earliest stars provides important insights into the origin of the elements necessary for life. The wide range of organic molecules identified by astronomical observations, space probes and by laboratory analysis of carbonaceous meteorites, suggests that the basic building blocks of life, at least as recognized on the Earth, must be widespread in planetary systems in our Galaxy and beyond [119]. There is a consensus that both exogenous and endogenous carbon sources have provided the raw material for the first building blocks of life on the early Earth. The extra-terrestrial contribution arrived via comets, asteroids and small fragments during the LHB phase 3.9 Gyr ago. The large quantities of extraterrestrial material delivered to young terrestrial planetary surfaces provided organic material predominantly in the form of aromatic networks that could have been used in biochemical pathways on the young Earth. Endogenous prebiotic carbon compounds may have formed in the early oceans. The connection between plate tectonics, hydrothermal geochemistry and reduction of simple carbon and nitrogen compounds has shown to be very suitable for abiotic organic chemistry. The best location where such processes could occur would be at convergent margins during the early phases of subduction of oceanic plates. Understanding the early and active Universe is extremely relevant to the question of terrestrial-planet formation. How heavy elements assemble to complex molecules and evolve in interstellar and circumstellar regions and how they are incorporated into forming planetary systems and are used on young planets Phil. Trans. R. Soc. A (2011) Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 Review. Organic matter in space 549 to form life are major research avenues that are investigated under the interdisciplinary umbrella of astrobiology. Understanding the constraints when defining the chemical composition of life’s raw material from the viewpoints of different scientific disciplines is essential. P.E. is supported by NASA grant NNX08AG78G and the NASA Astrobiology Institute NAI. We thank Alain Blanchard and Jan Cami for help in preparing the manuscript. References 1 Hinshaw, G. et al. 2009 Five-year Wilkinson microwave anisotropy probe observations: data processing, sky maps, and basic results. Astrophys. J. Suppl. 180, 225–245. 2 Tegmark, M., Silk, J., Rees, M. J., Blandchard, A., Abel, T. & Palla, F. 1997 How small were the first cosmological objects? Astrophys. J. 474, 1. (doi:10.1086/303434) 3 Abel, T., Bryan, G. L. & Norman, M. L. 2002 The formation of the first star in the Universe. Science 295, 93–98. (doi:10.1126/science.1063991) 4 Schleicher, D. R. G., Spaans, M. & Glover, S. C. O. 2010 Black hole formation in primordial galaxies: chemical and radiative conditions. Astrophys. J. 712, L69–L72. (doi:10.1088/20418205/712/1/L69) 5 Bromm, V., Coppi, P. S. & Larson, R. B. 2002 The formation of the first stars. I. The primordial star-forming cloud. Astrophys. J. 564, 23–51. (doi:10.1086/323947) 6 Scannapieco, E., Schneider, R. & Ferrara, A. 2003 The detectability of the first stars and their cluster enrichment signatures. Astrophys. J. 589, 35–52. (doi:10.1086/374412) 7 Cherchneff, I. & Dwek, E. 2009 The chemistry of population III supernova ejecta. I. Formation of molecules in the early Universe. Astrophys. J. 703, 642–661. (doi:10.1088/0004637X/703/1/642) 8 Beers, T. C. & Christlieb, N. 2005 The discovery and analysis of very metal-poor stars in the galaxy. Ann. Rev. Astron. Astrophys. 43, 531–580. (doi:10.1146/annurev.astro.42. 053102.134057) 9 Iwamoto, N., Umeda, H., Tominaga, N., Nomoto, K. & Maeda, K. 2005 The first chemical enrichment in the Universe and the formation of hyper metal-poor stars. Science 309, 451–453. (doi:10.1126/science.1112997) 10 Ito, H., Aoki, W., Honda, S. & Beers, T. C. 2009 BD + 44◦ 493: a ninth magnitude messenger from the early Universe; carbon enhanced and beryllium poor. Astrophys. J. 698, L37–L41. (doi:10.1088/0004-637X/698/1/L37) 11 Cazaux, S. & Spaans, M. 2009 HD and H2 formation in low-metallicity dusty gas clouds at high redshift. Astron. Astrophys. 496, 365–374. (doi:10.1051/0004-6361:200811302) 12 Cazaux, S. & Spaans, M. 2004 Molecular hydrogen formation on dust grains in the highredshift Universe. Astrophys. J. 611, 40–51. (doi:10.1086/422087) 13 Spaans, M. & Silk, J. 2000 The polytropic equation of state of interstellar gas clouds. Astrophys. J. 538, 115–120. (doi:10.1086/309118) 14 Spaans, M. & Silk, J. 2005 The polytropic equation of state of primordial gas clouds. Astrophys. J. 626, 644–648. (doi:10.1086/430105) 15 Norman, C. A. & Spaans, M. 1997 Molecules at high redshift: the evolution of the cool phase of protogalactic disks. Astrophys. J. 480, 145–154. (doi:10.1086/303940) 16 Bertoldi, F. et al. 2003 High-excitation CO in a quasar host galaxy at z = 6.42. Astron. Astrophys. 409, L47–L50. (doi:10.1051/0004-6361:20031345) 17 Walter, F., Riechers, D., Cox, P., Neri, R., Carilli, C., Bertoldi, F., Weiss, A. & Maiolino, R. 2009 A kiloparsec-scale hyper-starburst in a quasar host less than 1gigayear after the Big Bang. Nature 457, 699–701. (doi:10.1038/nature07681) 18 Weiß, A. Downes, D., Neri, R., Walter, F., Henkel, C., Wilner, D. J., Wagg, J. & Wiklind, T. 2007 Highly-excited CO emission in APM 08279 + 5255 at z = 3.9. Astron. Astrophys. 467, 955–969. (doi:10.1051/0004-6361:20066117) Phil. Trans. R. Soc. A (2011) Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 550 P. Ehrenfreund et al. 19 Simcoe, R. A. 2006 High-redshift intergalactic C IV abundance measurements from the nearinfrared spectra of two z ∼ 6 QSOs. Astrophys. J. 653, 977–987. (doi:10.1086/508983) 20 Madau, P., Ferguson, H. C., Dickinson, M. E., Giavalisco, M., Steidel, C. C. & Fruchter, A. 1996 High-redshift galaxies in the hubble deep field: colour selection and star formation history to z ∼ 4. Mon. Not. R. Astron. Soc. 283, 1388–1404. 21 Spaans, M. & Norman, C. A. 1997 Cosmological evolution of dwarf galaxies: the influence of star formation and the multiphase interstellar medium. Astrophys. J. 483, 87. (doi:10.1086/304231) 22 García-Burillo, S., Fernández-García, S., Combes, F., Hunt, L. K., Haan, S., Schinnerer, E., Boone, F., Krips, M. & Márquez, I. 2009 Molecular gas in NUclei of GAlaxies (NUGA). XI. A complete gravity torque map of NGC 4579: new clues to bar evolution. Astron. Astrophys. 496, 85–105. 23 Meier, D. S. & Turner, J. L. 2005 Spatially resolved chemistry in nearby galaxies. I. The center of IC 342. Astrophys. J. 618, 259–280. (doi:10.1086/426499) 24 Pérez-Beaupuits, J. P., Spaans, M., van der Tak, F. S. S., Aalto, S., García-Burillo, S., Fuente, A. & Usero, A. 2009 Probing X-ray irradiation in the nucleus of NGC 1068 with observations of high-J lines of dense gas tracers. Astron. Astrophys. 503, 459–466. (doi:10.1051/00046361/200912350) 25 Loenen, A. F., Spaans, M., Baan, W. A. & Meijerink, R. 2008 Mechanical feedback in the molecular ISM of luminous IR galaxies. Astron. Astrophys. 488, L5–L8. (doi:10.1051/00046361:200810327) 26 Meijerink, R. & Spaans, M. 2005 Diagnostics of irradiated gas in galaxy nuclei. I. A farultraviolet and X-ray dominated region code. Astron. Astrophys. 436, 397–409. (doi:10.1051/ 0004-6361:20042398) 27 Spaans, M. & Meijerink, R. 2008 On the detection of high-redshift black holes with ALMA through CO and H2 emission. Astrophys. J. 678, L5–L8. (doi:10.1086/588253) 28 Desai, V. et al. 2009 Strong polycyclic aromatic hydrocarbon emission from z ≈ 2 ULIRGs. Astrophys. J. 700, 1190–1204. (doi:10.1088/0004-637X/700/2/1190) 29 Ormel, C. W., Spaans, M. & Tielens, A. G. G. M. 2007 Dust coagulation in protoplanetary disks: porosity matters. Astron. Astrophys. 461, 215–232. (doi:10.1051/0004-6361:20065949) 30 Spaans, M. 2004 The synthesis of the elements and the formation of stars. In Astrobiology: future perspectives, astrophysics and space science library, vol. 305 (eds P. Ehrenfreund et al.), pp. 1–16. Dordrecht, The Netherlands: Kluwer Academic Publishers. 31 Ehrenfreund, P. & Charnley, S. B. 2000 Organic molecules in the interstellar medium, comets, and meteorites: a voyage from dark clouds to the early earth. Ann. Rev. Astron. Astrophys. 38, 427–483. (doi:10.1146/annurev.astro.38.1.427) 32 Kwok, S. 2004 The synthesis of organic and inorganic compounds in evolved stars. Nature 430, 985–991. (doi:10.1038/nature02862) 33 van Dishoeck, E. F. & Blake, G. 1998 Chemical evolution of star-forming regions. Ann. Rev. Astron. Astrophys. 36, 317–368. (doi:10.1146/annurev.astro.36.1.317) 34 Cuppen, H. M. & Herbst, E. 2007 Simulation of the formation and morphology of ice mantles on interstellar grains. Astrophys. J. 668, 294–309. (doi:10.1086/521014) 35 Ehrenfreund, P. & Fraser, H. 2003 Ice chemistry in space. In Solid state astrochemistry, NATO ASI series (eds V. Pirronello, J. Krelowski & G. Manicó), pp. 317–356. Dordrecht, The Netherlands: Kluwer Academic Publishers. 36 Gibb, E., Whittet, D., Boogert, A. & Tielens, A. G. G. M. 2004 Interstellar ice: the infrared space observatory legacy. Astrophys. J. Suppl. Ser. 151, 35–73. (doi:10.1086/381182) 37 Boogert, A. et al. 2008 The c2d spitzer spectroscopic survey of ices around low-mass young stellar objects. I. H2 O and the 5–8 mm bands. Astrophys. J. 678, 985–1004. (doi:10.1086/533425) 38 Pontoppidan, K. M., Boogert, A. C. A., Fraser, H. J., van Dishoeck, E. F., Blake, G. A., Lahuis, F., Öberg, K. I., Evans II, N. J. & Salyk, C. 2008 The c2d spitzer spectroscopic survey of ices around low-mass young stellar objects. II. CO2 . Astrophys. J. 678, 1005–1031. (doi:10.1086/533431) Phil. Trans. R. Soc. A (2011) Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 Review. Organic matter in space 551 39 Oberg, K., Adwin Boogert, A. C., Pontoppidan, K. M., Blake, G. A., Evans, N. J., Lahuis, F. & van Dishoeck, E. F. 2008 The c2d spitzer spectroscopic survey of ices around low-mass young stellar objects. III. CH4 . Astrophys. J. 678, 1032–1041. (doi:10.1086/533432) 40 Snow, T. P. & McCall, B. J. 2006 Diffuse atomic and molecular clouds. Ann. Rev. Astron. Astrophys. 44, 367–414. (doi:10.1146/annurev.astro.43.072103.150624) 41 Liszt, H. & Lucas, R. 2000 The structure and stability of interstellar molecular absorption line profiles at radio frequencies. Astron. Astrophys. 355, 333–346. 42 Tielens, A. G. G. M. 2008 Interstellar polycyclic aromatic hydrocarbon molecules. Ann. Rev. Astron. Astrophys. 46, 289–337. (doi:10.1146/annurev.astro.46.060407.145211) 43 Mennella, V., Colangeli, L., Bussoletti, E., Palumbo, P. & Rotundi, A. 1998 A new approach to the puzzle of the ultraviolet interstellar extinction bump. Astrophys. J. 507, 177–180. (doi:10.1086/311693) 44 Henning, T. & Salama, F. 1998 Carbon in the Universe. Science 282, 2204–2210. (doi:10.1126/ science.282.5397.2204) 45 Pendleton, Y. J. & Allamandola, L. J. 2002 The organic refractory material in the diffuse interstellar medium: mid-infrared spectroscopic constraints. Astrophys. J. Suppl. 138, 75–98. (doi:10.1086/322999) 46 Genzel, R. et al. 1998 What powers ultraluminous IRAS galaxies? Astrophys. J. 498, 579–605. (doi:10.1086/305576) 47 Peeters, E., Allamandola, L. J., Hudgins, D. M., Hony, S. & Tielens, A. G. G. M. 2004 The unidentified infrared features after ISO in astrophysics of dust. ASP Conf. Ser. 309, 141. 48 Peeters, E., Spoon, H. & Tielens, A. G. G. M. 2004 Polycyclic aromatic hydrocarbons as a tracer of star formation? Astrophys. J. 613, 986–1003. (doi:10.1086/423237) 49 Smith, J. D. et al. 2007 The mid-infrared spectrum of star-forming galaxies: global properties of polycyclic aromatic hydrocarbon emission. Astrophys. J. 656, 770–791. (doi:10.1086/510549) 50 Chiar, J. E. & Pendleton, Y. 2008 The origin and evolution of interstellar organics. Organic Matter in Space, Proc. Int. Astronomical Union, IAU Symp., vol. 251, pp. 35–44. Cambridge, UK: Cambridge University Press. 51 Kwok, S. 2009 Delivery of complex organic compounds from planetary nebulae to the Solar System. Int. J. Astrobiol. 8, 161–167. (doi:10.1017/S1473550409004492) 52 Allamandola, L. J., Hudgins, D. M. & Sandford, S. A. 1999 Modeling the unidentified infrared emission with combinations of polycyclic aromatic hydrocarbons. Astrophys. J. 511, 115–119. (doi:10.1086/311843) 53 Salama, F. 1999 Polycyclic aromatic hydrocarbons in the interstellar medium: a review, solid interstellar matter. In The ISO revolution (eds L. d’Hendecourt, A. Jones & C. Joblin) p. 65. Les Ulis, France: EDP Sciences, Springer-Verlag. 54 Boss, A. P. 2004 From molecular clouds to circumstellar disks. In COMETS II (eds M. Festou, H. U. Keller & H. A. Weaver), pp. 67–80. Tuscon, AZ: University of Arizona Press. 55 Carr, J. & Najita, J. R. 2008 Organic molecules and water in the planet formation region of young circumstellar disks. Science 319, 1504–1506. (doi:10.1126/science.1153807) 56 Gorti, U., Dullemond, K. & Hollenbach, D. 2009 Time-evolution of viscous circumstellar disks due to photoevaporation by FUV, EUV and X-ray radiation from the central star. Astrophys. J. 705, 1237–1251. (doi:10.1088/0004-637X/705/2/1237) 57 Dullemond, C., Pavlyuchenkov, Y., Apai, D. & Pontoppidan, K. 2008 Structure and evolution of protoplanetary disks. Phys. Conf. Ser. 131, 012018. (doi:10.1088/1742-6596/131/1/012018) 58 Visser, R., Geers, V. C., Dullemond, C. P., Augereau, J., Pontoppidan, K. & van Dishoeck, E. F. 2007 PAH chemistry and IR emission from circumstellar disks. Astron. Astrophys. 466, 229–241. (doi:10.1051/0004-6361:20066829) 59 Brownlee, D. et al. 2006 Comet 81P/Wild 2 under a microscope. Science 314, 1711–1716. (doi:10.1126/science.1135840) 60 Cruikshank, D., Imanaka, H., Dalle, O. & Cristina, M. 2005 Tholins as coloring agents on outer Solar System bodies. Adv. Space Res. 36, 178–183. (doi:10.1016/j.asr.2005.07.026) 61 Raulin, F. 2008 Astrobiology and habitability of Titan. Space Sci. Rev. 135, 37–48. (doi:10.1007/s11214-006-9133-7) Phil. Trans. R. Soc. A (2011) Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 552 P. Ehrenfreund et al. 62 Sephton, M. A. & Botta, O. 2005 Recognizing life in the Solar System: guidance from meteoritic organic matter. Int. J. Astrobiol. 4, 269–276. (doi:10.1017/S1473550405002806) 63 Crovisier, J., Biver, N., Bockelée-Morvan, D., Boissier, J., Colom, P. & Dariusz, C. 2009 The chemical diversity of comets: synergies between space exploration and ground-based radio observations. Earth, Moon, Planets 105, 267–272. (doi:10.1007/s11038-009-9293-z) 64 Di Santi, M. & Mumma, M. 2009 Reservoirs for comets: compositional differences based on infrared observations, origin and early evolution of comet nuclei. Space Sci. Ser. 28, 127–145. (doi:10.1007/978-0-387-85455-7_8) 65 Jenniskens, P. et al. 2009 The impact and recovery of asteroid 2008 TC3 . Nature 458, 485–488. (doi:10.1038/nature07920) 66 Sephton, M. A. 2002 Organic compounds in carbonaceous meteorites. Nat. Prod. Rep. 19, 292–311. (doi:10.1039/b103775g) 67 Cronin, J. R. & Chang, S. 1993 Organic matter in meteorites: molecular and isotopic analyses of the Murchison meteorite. In The chemistry of life’s origin (eds J. M. Greenberg, C. X. Mendoza-Gómez & V. Pirronello), pp. 209–258. Dordrecht, The Netherlands: Kluwer Academic Publishing. 68 Ehrenfreund, P., Glavin, D., Botta, O., Cooper, G. & Bada, J. 2001 Extraterrestrial amino acids in Orgueil and Ivuna: tracing the parent body of CI type carbonaceous chondrites. Proc. Natl Acad. Sci. USA 98, 2138–2141. (doi:10.1073/pnas.051502898) 69 Martins, Z., Alexander, O. D., Orzechowska, G., Fogel, M. & Ehrenfreund, P. 2007 Indigenous amino acids and chiral excess identified in CR primitive meteorites. Meteorit. Planet. Sci. 42/12, 2125–2136. (doi:10.1111/j.1945-5100.2007.tb01013.x) 70 Martins, Z. et al. 2008 Extraterrestrial nucleobases in the Murchison meteorite. Earth Planet. Sci. Lett. 270, 130–136. (doi:10.1016/j.epsl.2008.03.026) 71 Alexander, C., Fogel, M., Yabuta, H. & Cody, G. D. 2007 The origin and evolution of chondrites recorded in the elemental and isotopic compositions of their macromolecular organic matter. Geochimica et Cosmochimica Acta 71, 4380–4403. (doi:10.1016/j.gca.2007.06.052) 72 Schmitt-Kopplin, P. Gabelica, Z., Gougeon, R. D., Fekete, A., Kanawati, B., Harir, M., Gebefuegi, I., Eckel, G. & Hertkorn, N. 2010 High molecular diversity of extraterrestrial organic matter in Murchison metoerite revealed 40 years after its fall. Proc. Natl Acad. Sci. USA 107, 2763–2768. (doi:10.1073/pnas.0912157107) 73 Chyba, C. & Sagan, C. 1992 Endogenous production, exogenous delivery and impact-shock synthesis of organic molecules: an inventory for the origins of life. Nature 355, 125–132. (doi:10.1038/355125a0) 74 Gomes, R., Levison, H. F., Tsiganis, K. & Morbidelli, A. 2005 Origin of the cataclysmic Late Heavy Bombardment period of the terrestrial planets. Nature 435, 466–469. (doi:10.1038/ nature03676) 75 Ehrenfreund, P. et al. 2002 Astrophysical and astrochemical insights into the origin of life. Rep. Prog. Phys. 65, 1427–1487. (doi:10.1088/0034-4885/65/10/202) 76 Shirey, S. B., Kamber, B. S., Whitehouse, M. J., Mueller, P. A. & Basu, A. R. 2008 A review of the isotopic and trace element evidence for mantle and crustal processes in the Hadean and Archean: implications for the onset of plate tectonic subduction. In When did plate tectonics begin on Earth? (eds K. C. Condie & V. Pease), Special paper 440, pp. 1–31. Boulder, CO: Geological Society of America. 77 Derenne, S., Robert, F., Skrzypczak-Bonduelle, A., Gourier, A., Binet, L., & Rouzaud, J. N. 2008 Molecular evidence for life in the 3.5 billion year old Warrawoona Chert. Earth Planet. Sci. Lett. 272, 476–480. (doi:10.1016/j.epsl.2008.05.014) 78 Westall, F. 2009 Life on an anaerobic planet. Science 232, 471–472. (doi:10.1126/science. 1167220) 79 Lammer, H. et al. 2009 What makes a planet habitable? Astron. Astrophys. Rev. 17, 181–249. (doi:10.1007/s00159-009-0019-z) 80 Smirnov, A. Hausner, D., Laffers, R., Strongin, D. R. & Schoonen, M. A. A. 2008 Abiotic ammonium formation in the presence of Ni–Fe metals and alloys and its implications for the Hadean nitrogen cycle. Geochem. T. 9, 5. (doi:10.1186/1467-4866-9-5) Phil. Trans. R. Soc. A (2011) Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 Review. Organic matter in space 553 81 Arrhenius, G. O. 2003 Crystals and life. Helv. Chim. Acta 86, 1569–1586. (doi:10.1002/ hlca.200390135) 82 Honma, H. 1996 High ammonium contents in the 3800 Ma Isua supracrustal rocks, central West Greenland. Geochim. Cosmochim. Acta 60, 2173–2178. (doi:10.1016/0016-7037 (96)00083-X) 83 Ward, P. D. & Brownlee, D. 2000 Rare earth: why complex life is uncommon in the Universe. New York, NY: Copernicus. 84 Holm, N. G. & Neubeck, A. 2009 Reduction of nitrogen compounds in oceanic basement and its implications for HCN formation and abiotic organic synthesis. Geochem. T. 10, 9. (doi:10.1186/1467-4866-10-9) 85 Ferris, J. P. 1992 Chemical markers of prebiotic chemistry in hydrothermal systems. Orig. Life Evol. Biosh. 22, 109–134. (doi:10.1007/BF01808020) 86 Brandes, J. A., Boctor, N. Z., Cody, G. D., Cooper, B. A., Hazen, R. M. & Yoder Jr, H. S. 1998 Abiotic nitrogen reduction on the early Earth. Nature 395, 365–367. (doi:10.1038/26450) 87 Ferris, J. P. 2005 Catalysis and prebiotic synthesis. Rev. Miner. Geochem. 59, 187–210. (doi:10.2138/rmg.2005.59.8) 88 Ferris, J. P. & Usher, D. A. 1988 Origins of life. In Biochemistry (ed. G. Zubay), pp. 1120–1151. New York, NY: Macmillan. 89 Levy, M., Miller, S. L., Brinton, K. & Bada, J. L. 2000 Prebiotic synthesis of adenine and amino acids under Europa-like conditions. Icarus 145, 609–613. (doi:10.1006/icar.2000.6365) 90 Shapiro, R. 1988 Prebiotic ribose synthesis: a critical analysis. Orig. Life Evol. Biosph. 18, 71–85. (doi:10.1007/BF01808782) 91 Franiatte, M., Richard, L., Elie, M., Nguyen-Trung, C., Perfetti, E. & LaRowe, D. E. 2008 Hydrothermal stability of adenine under controlled fugacities of N2 , CO2 , and H2 . Orig. Life Evol. Biosph. 38, 139–148. (doi:10.1007/s11084-008-9126-5) 92 Schwartz, A. W. & Goverde, M. 1982 Acceleration of HCN oligomerization by formaldehyde and related compounds—implications for prebiotic synthesis. J. Mol. Evol. 18, 351–353. (doi:10.1007/BF01733902) 93 Hennet, R.-J. C., Holm, N. G. & Engel, M. H. 1992 Abiotic synthesis of amino acids under hydrothermal conditions and the origin of life: a perpetual phenomenon? Naturwissenschaften 79, 361–365. (doi:10.1007/BF01140180) 94 Holm, N. G., Dumont, M., Ivarsson, M. & Konn, C. 2006 Alkaline fluid circulation in ultramafic rocks and formation of nucleotide constituents: a hypothesis. Geochem. T. 7, 7. (doi:10.1186/1467-4866-7-7) 95 Arrhenius, T., Arrhenius, G. & Paplawski, W. 1994 Archean geochemistry of formaldehyde and cyanide and the oligomerization of cyanohydrin. Orig. Life Evol. Biosph. 24, 1–17. (doi:10.1007/BF01582036) 96 Keefe, A. D. & Miller, S. L. 1996 Was ferrocyanide a prebiotic reagent? Orig. Life Evol. Biosph. 26, 111–129. (doi:10.1007/BF01809851) 97 Kelley, D. S. et al. 2005 A serpentinite-hosted ecosystem: the Lost City hydrothermal field. Science 307, 1428–1434. (doi:10.1126/science.1102556) 98 Schlesinger, G. & Miller, S. L. 1973 Equilibrium and kinetics of glyconitrile formation in aqueous-solution. J. Am. Chem. Soc. 95, 3729–3735. (doi:10.1021/ja00792a043) 99 MacLeod, G., McKeown, C., Hall, A. J. & Russell, M. J. 1994 Hydrothermal and oceanic pH conditions of possible relevance to the origin of life. Orig. Life Evol. Biosph. 24, 19–41. (doi:10.1007/BF01582037) 100 Martin, W. & Russell, M. J. 2007 On the origin of biochemistry at an alkaline hydrothermal vent. Phil. Trans. R. Soc. B 362, 1887–1926. (doi:10.1098/rstb.2006.1881) 101 Russell, M. J. & Hall, A. J. 1997 The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front. J. Geol. Soc. Lond. 154, 377–402. (doi:10.1144/ gsjgs.154.3.0377) 102 Russell, M. J., Hall, A. J., Boyce, A. J. & Fallick, A. E 2005 On hydrothermal convection systems and the emergence of life. Econ. Geol. 100, 419–438. (doi:10.2113/100.3.419) 103 Mukhin, L. M. 1974 Evolution of organic compounds in volcanic regions. Nature 251, 50–51. (doi:10.1038/251050a0) Phil. Trans. R. Soc. A (2011) Downloaded from rsta.royalsocietypublishing.org on March 12, 2014 554 P. Ehrenfreund et al. 104 Mukhin, L. M., Bondarev, V. B. & Safonova, E. N. 1978 The role of volcanic processes in the evolution of organic compounds on the primitive Earth. Mod. Geol. 6, 119–122. 105 Cohn, C. A., Hansson, T. K., Larsson, H. S., Sowerby, S. J. & Holm, N. H. 2001 Fate of prebiotic adenine. Astrobiology 1, 477–480. (doi:10.1089/153110701753593874) 106 Holm, N. G. & Andersson, E. 2005 Hydrothermal simulation experiments as a tool for studies of the origin of life on Earth and other terrestrial planets: a review. Astrobiology 5, 444–460. (doi:10.1089/ast.2005.5.444) 107 Sowerby, S. J., Petersen, G. B. & Holm, N. G. 2001 Primordial coding of amino acids by adsorbed purine bases. Orig. Life Evol. Biosph. 32, 35–46. (doi:10.1023/A:1013957812213) 108 Joyce, G. F. 1989 RNA evolution and the origins of life. Nature 338, 217–224. (doi:10.1038/ 338217a0) 109 Butlerow, A. 1861 Formation synthetique d’une substance sucrée. Comp. Rend. Acad. Set. 53, 145–147. 110 Breslow, R. 1959 On the mechanism of the formose reaction. Tetrahedron Lett. 21, 22–26. (doi:10.1016/S0040-4039(01)99487-0) 111 Saladino, R., Crestini, C., Costanzo, G. & DiMauro, R. 2005 On the prebiotic synthesis of nucleobases, nucleotides, oligonucleotides, pre-RNA and pre-DNA molecules. Top. Curr. Chem. 259, 29–68. (doi:10.1007/b136152) 112 Shapiro, R. 1986 Origins: a skeptics guide to the creation of life on earth. London, UK: Heinemann. 113 Springsteen, G. & Joyce, G. F. 2004 Selective derivation and sequestration of ribose from a prebiotic mix. J. Am. Chem. Soc. 126, 9578–9583. (doi:10.1021/ja0483692) 114 Früh-Green, G. L., Kelley, D. S., Bernasconi, S. M., Karson, J. A., Ludwig, K. A., Butterfield, D. A., Boschi, C. & Proskurowski, G. 2003 30,000 years of hydrothermal activity at the Lost City vent field. Science 301, 495–498. (doi:10.1126/science.1085582) 115 Kelley, D. S. et al. & AT3-60 Shipboard Party. 2001 An off-axis hydrothermal vent field near the mid-Atlantic ridge at 30◦ N. Nature 412, 145–149. (doi:10.1038/35084000) 116 Proskurowski, G., Lilley, M. D., Seewald, J. S., Früh-Green, G. L., Olson, E. J., Lupton, J. E., Sylva, S. P. & Kelley, D. S. 2008 The abiotic production of hydrocarbons at the Lost City hydrothermal field. Geochim. Cosmochim. Acta 72, A764–A764. 117 Schulte, M. D. & Shock, E. L. 1993 Aldehydes in hydrothermal solution: standard partial molal thermodynamic properties and relative stabilities at high temperatures and pressures. Geochim. Cosmochim. Acta. 57, 3835–3846. (doi:10.1016/0016-7037(93)90337-V) 118 Ingmanson, D. E. 1997 Formaldehyde in hot springs. Orig. Life Evol. Biosph. 27, 313–317. (doi:10.1023/A:1006593802507) 119 Ehrenfreund, P., Rasmussen, S., Cleaves, J. H. & Chen, L. 2006 Experimentally tracing the key steps in the origin of life: the aromatic world. Astrobiology 6, 490–520. (doi:10.1089/ ast.2006.6.490) Phil. Trans. R. Soc. A (2011)