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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 ([email protected]).
One contribution of 17 to a Discussion Meeting Issue ‘The detection of extra-terrestrial life and
the consequences for science and society’.
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This journal is © 2011 The Royal Society
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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
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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
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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].
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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–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
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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
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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
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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
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accretionary prism
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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’,
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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.
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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)
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Review. Organic matter in space
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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.
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