Phil. Trans. R. Soc. A (2011) 369, 538–554doi:10.1098/rsta.2010.0231

REVIEW

The evolution of organic matter in spaceBY PASCALE EHRENFREUND1,2,*, MARCO SPAANS3 AND NILS G. HOLM4

1Space Policy Institute, 1957 E Street, Suite 403, 20052, Washington DC, USA2Leiden Institute of Chemistry, Astrobiology Laboratory, 2300 RA Leiden,

The Netherlands3Kapteyn Astronomical Institute, PO Box 800, 9700 AV Groningen,

The Netherlands4Department of Geological Sciences, Stockholm University, Stockholm, Sweden

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, duringwhich heavy elements like carbon, oxygen, nitrogen, silicon and iron are produced. Also,many complex molecules, from carbon monoxide to polycyclic aromatic hydrocarbons, aredetected in these systems, like they are for our own Galaxy. Interstellar molecular cloudsand circumstellar envelopes are factories of complex molecular synthesis. A surprisinglyhigh number of molecules that are used in contemporary biochemistry on the Earth arefound in the interstellar medium, planetary atmospheres and surfaces, comets, asteroidsand meteorites and interplanetary dust particles. Large quantities of extra-terrestrialmaterial were delivered via comets and asteroids to young planetary surfaces duringthe heavy bombardment phase. Monitoring the formation and evolution of organicmatter in space is crucial in order to determine the prebiotic reservoirs available tothe early Earth. It is equally important to reveal abiotic routes to prebiotic moleculesin the Earth environments. Materials from both carbon sources (extra-terrestrial andendogenous) may have contributed to biochemical pathways on the Earth leading tolife’s origin. The research avenues discussed also guide us to extend our knowledge toother 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]. DuringBig-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, coolingand decreasing in density, heavier elements (called metals by astronomers) couldnot 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 andthe consequences for science and society’.

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triple-a process (3 × 4He → 12C) in the cores of stars is the fundamental sourceof carbon, the basis of organic chemistry. After hydrogen is exhausted, furthernuclear reactions start in the core of stars with masses greater than half a solarmass leading to carbon and heavier elements, and up to 56Fe for the more massivestars. Heavier elements than iron are formed during the final stages of stars instellar explosions by neutron absorption (s and r processes). In this phase, noequilibrium can be reached: the stars undergo mass loss either in a smoothway or in violent way, leading to the enrichment of the interstellar medium.Analytical arguments [2], as well as numerical simulations [3], showed that asignificant amount of star formation could have occurred when the Universe wasonly 100 Myr old in the standard cold dark matter theory. The high opacityto Thomson scattering of the Universe found by the Wilkinson MicrowaveAnisotropy Probe provides support for this theory. The first stars (so calledpopulation III or zero metallicity stars) are expected to form in dark matterhalos, growing from primordial fluctuations, in which the baryonic gas couldcool efficiently enough. Although atomic cooling can ensure temperatures downto 10 000 K, molecular cooling is necessary to reach lower temperatures. Thedominant 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 H2cooling could not decrease the temperature as low as metals do. The Jeans massis therefore higher, up to 100–1000 solar masses [5]. These massive stars are veryshort 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 theUniverse [6]. There is evidence that a copious amount of molecules, such asO2, CO, SiS, SO, CO and SiO, may form in the ejecta of Pop III progenitorsupernovae [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 haloalso provides important constraints for early star formation processes [8,9]. Theobserved 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 lessmassive than the Sun. Their modest masses allow them to exist for longer than10 Gyr, and thus to act as ‘fossil’ record. Investigations of those stars may provideclues regarding the properties of the initial generation of stars and supernovaethat distributed the first heavy elements in the early Universe. The star BD+44493 has been recently identified as the brightest extremely low-metallicity staramong all objects reported [10]. Carbon appears to be favoured as a formationproduct of the first generation of stars. Molecules like CO and water, formed onceoxygen and carbon atoms were present (less than 1 Gyr after the Big Bang), aswell as very small grains, cool interstellar gas much more efficiently than H2. Thisstimulates cloud fragmentation and triggers the formation of low-mass stars likeour Sun [11–14].

Low-mass stars live much longer, approximately 10 Gyr for the Sun, a durationthat enables the formation of terrestrial planets and possibly the emergenceof life.

Once the first generation of population III stars had formed and explodedas supernovae about 500 Myr after the Big Bang, the subsequent existence ofmetals and dust is expected to lead to the efficient formation of molecules like

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10

1

0.12 4 6

redshift

WC

IV

(×

10–8

)

Figure 1. The evolution of the intergalactic ion C IV (C3+) abundance as a function of redshift, inunits of its contribution to the closing density. The constancy of the curve indicates that vigorousstar formation was already underway when the Universe was only 7% (at redshift z = 6) of itspresent age. Reproduced with permission from Simcoe [19].

CO, water, hydrides and carbon chains [15]. Indeed, high excitation CO emissionsfrom the distant quasar SDSS 114816.64 + 525150.3 at redshift z = 6.4 have beendetected, indicating that CO, one of the most important coolants of interstellargas, has been present in the Universe since approximately 800 Myr after the BigBang [16]. Furthermore, detections of C and C+ have been made and upper limitson 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 thegalaxy to be probed. Large amounts of warm (100 K) CO gas and warm dust(assuming a frequency squared absorption-coefficient dependence) appear to bepresent, indicative of active star formation [18]. Clearly, carbon and dust surfacechemistry was occurring already in the earliest epochs of the Universe. That theseobjects 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. Inthis, redshifts of 1 and 6 mean 35 and 7 per cent of the present age of theUniverse, respectively. Clearly, carbon and thus star formation was already verymuch present in the young Universe [19]. This fits well with the star formationand metal-production history of the Universe [20], where the metals produced bymassive stars lead to the formation of molecular gas and thus more stars. For ametallicity of 1 per cent of solar and up, one develops a multi-phase interstellarmedium (ISM) that supports a cool dense phase, with a density larger than100 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 certainlyreached in the quasar sources mentioned above, and an active carbon chemistrytherefore 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 carbonchemistry, as exemplified by species such as CO, HCN, HNC, HCO+, CH3OH,H2CO, C2H and polycyclic aromatic hydrocarbons (PAHs; e.g. [22–24]). Somegalaxies form stars with a very high rate, so-called starburst galaxies like Arp 220

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and M82. Carbonaceous molecules are detected in those systems as well, even inthe presence of strong mechanical feedback owing to supernova explosions andoutflows [25]. UV radiation produced by stars or X-ray photons created by anaccreting supermassive black hole can destroy complex molecules in the nucleiof galaxies [26]. Nevertheless, species like CO may survive even such extremeenvironments, already in the early Universe at metal-enrichment levels of only afew 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 bypopulation III stars constantly increases the abundance of heavy elements inthe interstellar medium, a crucial prerequisite for rocky-planet formation [29,30].Understanding the early and active Universe is thus extremely relevant to thequestion 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 complexmolecular synthesis [31–33]. Interstellar clouds constitute a few per cent ofgalactic mass and are composed primarily of H and He. They are enrichedprimarily by matter ejected from evolved stars and can vary strongly in theirfundamental physical parameters such as temperature and density. Dominatedby gas, interstellar material also contains approximately 1 per cent of smallmicron-sized particles. Gas-phase and gas–grain interactions lead to the formationof complex molecules. Surface catalysis on solid interstellar particles enablesmolecule formation and chemical pathways that cannot proceed in the gasphase owing to reaction barriers [34,35]. H2 is by far the most abundantmolecule in cold interstellar regions, followed by CO, the most abundantcarbon-containing species, with CO/H2 ∼ 10−4. CO is characterized by a highbinding energy (11.2 eV) and strongly influences the chemistry in interstellarclouds. Two main types of interstellar clouds drive molecular synthesis. In colddark clouds, the temperature is low (approx. 10 K) and therefore the stickingcoefficients of most atoms and molecules are close to unity, leading to a freezeout of practically all species (except H2 and He). The high density in darkclouds (up to approx. 106 cm−3) attenuates UV radiation and offers a protectedenvironment for the formation of larger molecules by gas-phase reactions andice chemistry on grains. A large number of complex organic gas-phase moleculeswas 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 long-chain hydrocarbons. The main species observed in interstellar ice mantles areH2O, CO2, CO and CH3OH, with smaller admixtures of CH4, NH3, H2CO andHCOOH [36]. A recent c2d (core to disks) Spitzer survey of ices investigatedthe 6–8 mm region that displays the prominent bending mode of water ice. Fiveindependent components that can be attributed to eight different carriers [37]have been identified. Observations of CO2 in low-mass protostars showed highabundances (average of 32% relative to water ice) [38]. CH4 ice was detected in25 out of 52 targets, with abundances ranging from 2 to 8 per cent relative towater ice and reach 13 per cent in a few sources [39].

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Diffuse interstellar clouds are characterized by a low density (approx.103 atoms cm−3) and temperatures less than or equal to 100 K. Ion–moleculereactions, dissociative recombination with electrons, radiative associationreactions and neutral–neutral reactions contribute to gas-phase processes andinfluence interstellar chemistry [40]. A variety of small molecules, including CO,CH, CN, OH, C2, C3 and others, are observed [41]. Gaseous PAHs are highlyabundant, with fractions of about 10−7 [42]. Carbonaceous grains composed ofmacromolecular aromatic networks account for most of the molecular carbonfraction in these clouds as evidenced by a ubiquitous strong UV absorption bandat 2175 Å [43].

Amorphous carbon, hydrogenated amorphous carbon, diamonds, refractoryorganics and carbonaceous networks such as coal, soot, graphite and quenched-carbonaceous condensates have been proposed as possible carbon compounds[31,42,44,45]. PAHs are observed to be widely distributed in galactic andextragalactic regions [42,46–49]. In diffuse interstellar clouds, dust interactswith hot gas, UV radiation and cosmic rays, and evolves or gets destroyed inshocks and by sputtering. Strong differences in the dust component of denseand 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 molecularsynthesis [32]. Figure 2 shows a route to the formation of PAHs and soot materialthat has been proposed over two decades to occur in the shielded environment ofstellar envelopes.

(b) Solar-System materials

The gravitational collapse of an interstellar cloud led to the formation ofthe protosolar nebula from which planets and small bodies of our Solar Systemformed [54]. Observations of protoplanetary disks show that gas and solids driftinward in time. Solids migrate inwards faster than gas, and small particles growto kilometre-sized bodies that accrete to planets. The chemical composition ofprotoplanetary disks is expected to hold clues to the physical and chemicalprocesses that influence the formation of planetary systems. Recently, it hasbeen reported that the protoplanetary disks of AA Tauri possess a rich molecularemission spectrum in the mid-infrared, indicating a high abundance of simpleorganic molecules (HCN, C2H2 and CO2), water vapour and OH [55]. Data fromrecent space missions, such as the Spitzer telescope, Stardust and Deep Impact,show that the dynamic environment of the solar nebula with the simultaneouspresence of gas, particles and energetic processes, including shock waves, lightningand radiation (e.g. [56]) can trigger a rich organic chemistry. Turbulent motionleads to radial mixing of the products within the disk [57,58], which has beenconfirmed by Stardust data [59]. The carbonaceous inventory of our Solar Systemtherefore contains a mixture of material that was (i) highly processed by exposureto 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

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Figure 2. Acetylene chemistry leading to the formation of benzene and small PAHs thatsubsequently build up larger structures has been proposed to occur in the shielded environmentsof 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 asteroidchemistry. Carbonaceous chondrites (meteorites) and micrometeorites, whichrepresent fragments of cometary and asteroidal bodies, do contain a variety oforganics (e.g. see [62,66] for reviews).

In the soluble fraction of the Murchison meteorite, more than 70 extra-terrestrial amino acids have been identified in addition to many other organiccompounds, including N-heterocycles, carboxylic acids, sulphonic and phosphonicacids, and aliphatic and aromatic hydrocarbons [67–70]. However, the majorcarbon component in meteorite samples is composed of a macromolecular organicfraction [71]. A recent study using ultra-high resolution molecular analysisof the solvent-accessible organic fraction of Murchison shows high moleculardiversity [72].

The remaining population of planetesimals not incorporated into planets existsuntil today as asteroids and comets. Most of the asteroids and comets are confinedto stable orbits (such as the asteroid belt between Mars and Jupiter) or reservoirsin 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

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and asteroids, and their fragments impacted the young planets [73]. A destabilizedplanetesimal disk caused a massive delivery of planetesimals to the inner SolarSystem at 3.9 Gyr ago. This so-called Late Heavy Bombardment (LHB) phase waslikely triggered by rapid migration of giant planets [74]. The large quantities ofextra-terrestrial material delivered to young terrestrial planetary surfaces duringthis period may have provided raw material useful for protocell assembly on theEarth [73,75]. The analysis of extra-terrestrial matter in the Earth laboratoriesindicates that the dominant form of carbonaceous material that was delivered toyoung 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 inthe last decade, we still have limited knowledge regarding the exact atmosphericcomposition, the temperature of the oceans and geological activity. Considerablegeochemical evidence supports an initiation of plate tectonics on the Earth shortlyafter the end of the Hadean about 3.9 Gyr ago. It is unclear if the transitionto plate tectonics resulted from radioactive decay-driven mantle heating orfrom cooling to the extent that large lithospheric plates stabilized [76]. Anyexisting carbon material from the solar nebula (volatile and refractory) wasdestroyed during the Earth’s formation. Therefore, organic molecules foundon terrestrial planets must have formed after the planetary surface cooled, orhave been delivered via impacts by small bodies in the young Solar System.All terrestrial planets have been seeded with organic compounds through theimpact of small bodies during Solar-System formation. There is a consensusthat a combination of exogenous and endogenous sources has provided thefirst precursor molecules for life on the young Earth. These simple moleculesreacted and assembled on catalytic surfaces (such as minerals) and formedmore complex structures that later developed into primitive cells (protocells).The endogenous synthesis of prebiotic organic compounds (molecules that areinvolved in the processes leading to the origin of life) may have been limited toprotective environments such as the oceans, owing to the hostile conditions onthe young Earth, including volcanism, radiation and bombardment by cometsand asteroids.

Whatever the inventory of endogenous organic compounds on the ancient Earthwas, it would have been augmented by extra-terrestrial material. It is estimatedthat these sources delivered approximately 109 kg of carbon per year to the Earthduring 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 ourSolar System and has adapted to every possible environment on planet Earth.Life on Earth can be found in extreme environments, such as hydrothermalvents, in dry deserts, the Earth atmosphere and in polar regions. These findingschallenge the definition of the ‘planetary habitable zone’. Primitive life, in theform of bacteria, emerged approximately 3.5 Gyr ago [77,78]. The homologousseries of long-chain aliphatic hydrocarbons found in old sedimentary rocks

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characterized by odd-over-even carbon-number predominance is only consistentwith a biological origin and indicates that, despite the hostile conditions, planetEarth was habitable in its early history [79].

Today, the Earth provides an ideal environment for life to sustain. Dynamicprocesses in the interior of the Earth have established a magnetosphere thatprotects the Earth from harmful cosmic radiation. Oceans and atmosphere enablea 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 temperatureof −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, energytransfer) and proteins. Systems containing NH3/NH+

4 are more efficient in abioticorganic synthesis than those dominated by N2 in both aqueous and and gaseousenvironments [80]. The reason is that the triple bond between the atoms inmolecular nitrogen is very stable and hard to break. Geochemically plausibleabiotic synthesis pathways of prebiotic molecules and concentration mechanismsfor nitrogen-containing molecules must eventually be found since nitrogen-basedlife is likely to have existed on the Earth from early Archean about 3.8 Gyr agoand onwards [81]. High ammonium contents (54–95 ppm) have been found inauthigenic clays of the Isua supracrustal rocks of western Greenland, suggestingthat clays were major sinks of NH+

4 or other nitrogen compounds on the Earth’ssurface already at 3.8 Gyr ago [82]. Ward & Brownlee [83] have argued that platetectonics is necessary for the origin of life on terrestrial planets and have listed anumber of reasons in support of their opinion. However, one argument that theyhave never mentioned is the connection between plate tectonics, hydrothermalgeochemistry, and reduction of simple carbon and nitrogen compounds suitablefor abiotic organic chemistry. The best location where such processes could occurwould be at convergent margins during the early phases of subduction of oceanicplates. As a plate descends, fluids distilled from the plate influence, and evencontrol, fundamental processes in the subduction zone [84]. The subducting plate,along with its fluids and altered igneous rock, interact with the over-riding platealong the subduction zone. Fluids originating in the subducting plate will risethrough the upper plate containing hydrated ultramafic mantle material in itslower parts. The fluids may thus move from a relatively acidic environment inweathered basalt into an alkaline environment in serpentinized peridotite.

The strong pH increase promotes the formation of carbohydrates like ribosefrom simple organic compounds. It also supports the synthesis of amino acids andpurine nitrogen bases, as well as their condensation to nucleotides in the presenceof 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 normallypresent in trace amounts [85]. HCN is, for instance, readily formed by the reactionof CO or CH4 with NH3 (figure 3) [84]. Hydrothermal systems represent regions ofthe 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

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over-riding plate

accretionary prism

oceanic lithosphere

dehydrat

ion

subducti

on

hydrated

mantle

pH 9–12HCN

amino ac

ids,

purines

oxidation

reduction

Fe(II) Fe(III)

(Fe(II)(Ni(II)

H2O

CO2

CH4

CO

CO, CH4NO3

–, NO2–

NH3+ HCN

NH4+ adsorption on smectites and zeolites

H2

Fe)Ni)

off-axishydrothermalismand fluid flow

spreading centremid-oceanic ridge

pH 3–5

spreading

magmachamber

seafloor

Figure 3. Cartoon showing a cross-section of oceanic lithosphere, extending from the spreadingcentre to the subduction zone. Off-axis hydrothermal flow in the oceanic lithosphere causesoxidation of Fe(II) to Fe(III) and reduction of water to molecular hydrogen. Some Fe(II) andNi(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 likesmectite 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 intohydrated mantle rock of high pH. At the high pH hydrogen cyanide may form HCN oligomers aswell as amino acids, purine bases, nucleosides and, perhaps, nucleotides (adapted from [84]).

synthesized in the same abiotic reactions that yield amino acids [87–90]. Adenineis likely to have been the first nucleobase formed abiotically, and has beenshown to remain in detectable concentrations still after 200 h at 300◦C underfugacities of CO2, N2 and H2 that are supposedly representative of those inmarine hydrothermal systems on the early Earth [91]. The purines are formedfrom HCN via two routes. One route is via HCN oligomers, which may alsoform amino acids; the second one is via the HCN tetramer diaminomaleonitrile(DAMN) [87,88]. DAMN formation is accelerated by the presence of formaldehydeunder mildly alkaline conditions (pH 9.2) [92]. Amino acids can be released byhydrolysis of HCN oligomers that form by the self-condensation of hydrogencyanide in aqueous solution [88]. Furthermore, amino acids may be synthesizedin putative prebiotic chemistries like Strecker-type reactions (synthesis of aminoacids from cyanide and aldehyde in the presence of ammonia) in hydrothermalenvironments at fairly low temperatures (150◦C) [93,94]. In order to participate inabiotic organic reactions, HCN must first be concentrated. One possibility is theconcentration to a reservoir of ferrocyanide at relatively low pH from which freeHCN can be released upon local elevation of the pH [81,95]. HCN reacts withferrous ions to give ferrocyanide, provided that the concentration of hydrogensulphide is low [96], like in the Lost City serpentinite-hosted hydrothermal field offthe 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’,

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which refers to the side reaction of glycolonitrile (cyanohydrin of formaldehyde)formation from free HCN and ubiquitous formaldehyde [98]. Formaldehyde andHCN, if present in the same environment, tend to react to form stable glyconitrile.On the other hand, Schwartz & Goverde [92] have shown that admixture ofsolutions enriched in cyanohydrins (like glyconitrile) with solutions of HCNpermits oligomerization of HCN to DAMN, even under dilute conditions.

An alternative model to avoid the ‘Miller paradox’ involving alkalinehydrothermal mounds as flow reactors in which strongly polar compounds suchas the cyanide ion is retained by fresh FeS/Fe3S4 membranes has been presentedby Russell et al. [99–102]. According to their model, the fluctuations in pHat the interface between hydrothermal fluid and sea water would determineadsorption and desorption of the cyanide. In natural environments, the occurrenceof ferrocyanides in hydrothermal systems has so far been reported only fromthe Kurile Islands and the Kamchatka Peninsula in the northwest PacificOcean [103,104].

Cohn et al. [105] have shown that adenine is far displaced towardsadsorption onto pyrite, quartz and pyrrhotite, which are all common mineralsof hydrothermal environments. It would, therefore, normally be useless to searchfor the purine bases in the fluid phase of hydrothermal systems [106]. Theobserved coding effect of adsorbed purine bases [107] may indicate that the roleof phosphate as a constituent of polynucleotides is a secondary property, andthat phosphate was originally incorporated in prebiotic systems because of itsenergy-transfer capacity.

A couple of decades ago, many scientists believed that the abiotic formationof ribose, a constituent of RNA, occurred through the formose reaction [87,108].The formose reaction was discovered and first described by Butlerow [109]. In thisreaction, pentoses like ribose can be formed under alkaline conditions from simpleorganic precursors (formaldehyde and glycolaldehyde) [87,88]. The condensationof formaldehyde to sugars is catalysed by divalent cations and layered minerals,such as clays. The reaction proceeds by the stepwise condensation of formaldehydeto dimer (glycolaldehyde), trimer, etc. Under experimental conditions, it hasbeen possible to convert as much as 50 per cent of the original formaldehydeto glycolaldehyde [110]. However, this reaction has, for a while, been an outdatedconcept 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 bioactivecompounds such as ribose [90,111,112]. A general opinion has been that if ribosewere used in the first RNA, an unknown selection process must have operatedto segregate ribose from the other sugars that were formed. A second reasonwhy the formose reaction has been outdated is that the reaction proceeds at asignificant rate only under naturally ‘improbable’ conditions, like under highlyalkaline conditions [81,87,108,113].

Natural environments with the pH conditions required for the abiotic formationof carbohydrates have previously been considered to be relatively rare onthe Earth. However, the recent discovery of alkaline hydrothermal systems inultramafic rocks, such as the Lost City Hydrothermal Field on the Mid-AtlanticRidge [97,114–116] and the Mariana Trench [94,84], indicates that alkalineenvironments may be much more common on the Earth than was thought just afew years ago.

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Because of the postulated difference in requirements for the formation of theribose and the nitrogen base, the spontaneous formation of RNA under prebioticconditions on the Earth has been doubted [90]. The differences in requiredenvironment may, however, be illusive. It was mentioned earlier that formaldehydeis necessary for the formation of carbohydrates in the formose reaction. Schulte &Shock [117] have shown that aldehydes may be intermediates in the formationof carboxylic acids from hydrocarbons in sedimentary basin brines, as well asin hydrothermal systems. Furthermore, they concluded that the presence ofaldehydes should normally be difficult to detect in natural systems if metastableequilibrium is reached between aldehydes and carboxylic acids at expected redoxconditions. On the other hand, this suggests that aldehydes are always present asreaction intermediates in cases when organic acids and hydrocarbons both existin natural hydrothermal systems. In fact, low concentrations of formaldehydehave been identified in hot-spring environments in Iceland, Mexico and southernCalifornia [118].

At equilibrium in hydrothermal systems, carboxylic acids, aldehydes andhydrocarbons will all be present in parallel, although at different levelsof concentration.

4. Conclusion

The cycle of birth and death of stars that is initiated by population III starsconstantly increases the abundance of heavy elements in the interstellar medium.Observations of the oldest stars show that carbon has been formed already in thevery early Universe. The central star of our Solar System, the Sun, was formedmany billion years after this time, and therefore contains several generations ofsupernova-produced metals. Tracing the earliest stars provides important insightsinto the origin of the elements necessary for life. The wide range of organicmolecules identified by astronomical observations, space probes and by laboratoryanalysis of carbonaceous meteorites, suggests that the basic building blocks of life,at least as recognized on the Earth, must be widespread in planetary systems inour Galaxy and beyond [119]. There is a consensus that both exogenous andendogenous carbon sources have provided the raw material for the first buildingblocks of life on the early Earth.

The extra-terrestrial contribution arrived via comets, asteroids and smallfragments during the LHB phase 3.9 Gyr ago. The large quantities of extra-terrestrial material delivered to young terrestrial planetary surfaces providedorganic material predominantly in the form of aromatic networks that could havebeen used in biochemical pathways on the young Earth. Endogenous prebioticcarbon compounds may have formed in the early oceans. The connection betweenplate tectonics, hydrothermal geochemistry and reduction of simple carbon andnitrogen compounds has shown to be very suitable for abiotic organic chemistry.The best location where such processes could occur would be at convergentmargins during the early phases of subduction of oceanic plates.

Understanding the early and active Universe is extremely relevant to thequestion of terrestrial-planet formation. How heavy elements assemble to complexmolecules and evolve in interstellar and circumstellar regions and how they areincorporated into forming planetary systems and are used on young planets

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to form life are major research avenues that are investigated under theinterdisciplinary umbrella of astrobiology. Understanding the constraints whendefining the chemical composition of life’s raw material from the viewpoints ofdifferent scientific disciplines is essential.

P.E. is supported by NASA grant NNX08AG78G and the NASA Astrobiology Institute NAI. Wethank Alain Blanchard and Jan Cami for help in preparing the manuscript.

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