Phil. Trans. R. Soc.

B (2006) 361, 1689–1702

doi:10.1098/rstb.2006.1913
Published online 11 September 2006

Prebiotic materials from on and off

the early Earth
Max Bernstein*
NASA Ames Research Center, Mail Stop 245-6, Moffett Field, CA 94035-1000, USA
One of the greatest puzzles of all time is how did life arise? It has been universally presumed that life arose
in a soup rich in carbon compounds, but from where did these organic molecules come? In this article,
I will review proposed terrestrial sources of prebiotic organic molecules, such as Miller–Urey synthesis
(including how they would depend on the oxidation state of the atmosphere) and hydrothermal vents
and also input from space. While the former is perhaps better known and more commonly taught in
school, we now know that comet and asteroid dust deliver tons of organics to the Earth every day,
therefore this flux of reduced carbon from space probably also played a role in making the Earth
habitable. We will compare and contrast the types and abundances of organics from on and off the Earth
given standard assumptions. Perhaps each process provided specific compounds (amino acids, sugars,
amphiphiles) that were directly related to the origin or early evolution of life. In any case, whether
planetary, nebular or interstellar, we will consider how one might attempt to distinguish between abiotic
organic molecules from actual signs of life as part of a robotic search for life in the Solar System.
Keywords: prebiotic chemistry; exogenous delivery; endogenous synthesis; impact;
hydrothermal vents; IDP (interplanetary dust particle)

1. INTRODUCTION interstellar cloud. Stars like the Sun and the clouds that
Following Professor Thaddeus’s gas-phase interstellar precede them are composed primarily of the ‘light and
molecules and preceding Professor Grady’s planetary transparent’ elements, hydrogen and helium, which
carbon cycle means that, in a way, I stand between the escape (at least from the forming terrestrial planets)
Earth and the sky. It may sound rather mythic to say it leaving behind the heavier elements that comprise the
that way, but given that the question of how life rocky planets of the inner Solar System. However,
emerged on Earth is a subject that has inspired a great exactly how and when the ‘something light and
deal of myth, both scientific and otherwise, it is difficult transparent rose up’—which I interpret to mean ‘when
to resist the temptation to be just a bit fabulous. In fact, did the hydrogen escape if it ever was there to begin
I am going to start with a creation story from the with?’ or ‘What was the oxidation state of the early
Kojiki—Japan’s eighth century chronicle that starts Earth’s atmosphere?’—has important consequences for
with the formation of the world, deities, and Japan. how complex and profuse one expects organic
I will leave the specifics of the island of Japan to the compounds to be on the early Earth.1 The abundance
geologists and the deities to subsequent speakers who of organic molecules on the early Earth is the first crucial
are even more outrageous than I, and restrict myself in matter we must address this week in our discussions of
this talk to the world. conditions for emergence of life on the early Earth
because, as we shall see, all non-magical notions of how
Before the heavens and the Earth came into existence,
life emerges are predicated on the basis of the presence
all was a chaos, unimaginably limitless and without
definite shape or [Link] of this boundless, shapeless
of organic compounds, as well as some other substances
mass something light and transparent rose up and that we know make up living things today.
formed the heaven.(and a god emerges here). In the My apologies to the impatient chemists for not just
meantime what was heavy and opaque in the void jumping right into the organic chemistry here, but I can
gradually precipitated and became the Earth, but it had hardly discuss the conditions necessary for the
taken an immeasurably long time before it condensed emergence of life on the early Earth (in my case,
sufficiently to form solid ground.. chemical conditions) without at least briefly presenting
(Brains et al. 1999) some of the ideas about how life emerged on Earth,
which will set the requirements. Incidentally, it seems
All things considered, this excerpt from the Isobe to me that the conditions under which life first
translation of the Kojiki is remarkably similar to how we developed might well be more restricted than those
currently describe the formation of the Earth within the under which life can survive or thrive thereafter; hence,
Solar nebula that came from the collapse of a vast, dense I am going to assume that terrestrial life did, in fact,
first begin here on the Earth and was not transported
*mbernstein@[Link] (or deliberately set down) here. Presumably, if any of
One contribution of 19 to a Discussion Meeting Issue ‘Conditions for you favour some kind of panspermia, at least you will
the emergence of life on the early Earth’. find my conditions hospitable, if a bit provincial.

1689 This journal is q 2006 The Royal Society

1690 M. Bernstein Sources of prebiotic matter

So, let us briefly consider the first of these non- connected by a tube to a reservoir of warm liquid
mythological conceptions of how life emerged as an water (the ocean).
example, and then proceed to experimental tests of that The results were breathtaking. When Miller ana-
concept. The prototypical example comes from a lysed the organic matter that was made in that and
private letter written by Charles Darwin in 1871 in subsequent experiments, he found certain amino acids,
which he speculated about how just the kind of thing that would have delighted
Darwin. Starting with some simple common gases, a
.we could conceive in some warm little pond with all
fairly minimal apparatus and a little energy, the
sorts of ammonia and phosphoric salts, light, heat,
electricity, etc. present, that a protein compound was fundamental components of proteins had formed
chemically formed, ready to undergo still more complex rapidly. Although he was among the first to tackle the
changes. At the present day, such matter would be problem experimentally, and had only just begun,
instantly devoured or absorbed which would not have Miller had already made tremendous progress. Given
been the case before living creatures were formed. that it was also the year that the structure of DNA was
(Darwin 1898) published, I am told that it seemed as if the secrets of
life were being revealed and that very soon scientists
It need not be a protein of course, but it was a logical would understand how life had come about. It turns
choice since Strecker had shown in the 1850s that one out, of course, that the situation is not as straightfor-
could make amino acids by heating an aqueous solution ward as it may have appeared at that time. For one
of simple starting materials (Strecker 1854). It is easy reason, the assumption that a mixture of reduced gases
to forget that they did not know about nucleic acids, accurately represents the atmosphere of the early Earth
and besides, the kind of molecule does not matter here has since been called into question.
in Session 1 on Monday. The important part is that one At that time, scientists believed that Jupiter was a
goes from a random mix of essential but disordered good model for how planets began and that the early
components to the first self-replicating molecule, and Earth formed warm and wet and had a thick
from there to the last common ancestor is a simple atmosphere composed of reduced gases like hydrogen,
matter of natural selection. From the 1920s onward, A. methane and ammonia left over from the formation of
Oparin and J. B. S. Haldane publicly presented and the Solar System. They figured that Earth’s atmos-
more fully developed similar ideas of a primordial soup phere, and that of all the planets, essentially started
(Oparin 1938) but the kernel of the idea was there back with solar abundances of gases, which gradually
in that private letter of Darwin’s in 1871. In other escaped, as described in the Kojiki, leaving behind
words, scientific origins of life scenarios tend to put the the N2 that makes up most of our atmosphere today.
pieces of life in proximity to one another, add some Our oxygen came later, of course, as a waste product of
kind of energy and figure that eventually something or life. Apparently, part of the appeal of this reduced
some process that can reproduce itself will arise. In atmosphere for the early Earth was that it would have
Session 3, I think, Profs. Szathmáry and Ferris will been a greenhouse mixture, keeping the Earth from
speak about how a self-replicating molecule may have freezing over during a period when the Sun was
arisen, and Profs. Wächtershäuser and Deamer on dimmer than it is today (Sagan & Chyba 1997).
alternatives to focusing on such a molecule; indeed I Jupiter retained its original gases because it is so
am keenly looking forward to all of those lectures. My massive that the molecules could never escape.
job, thankfully, is much easier than theirs. What I want However, size is not the only difference between Jupiter
to consider in my talk is from where those pieces might and Earth; the Earth is much closer to the Sun. The
have come. notion that, from the time of formation, the Earth
started with a thick Jupiter-like atmosphere was
seriously undermined by models showing that the
2. SPARK DISCHARGE—LIGHTNING IN A temperature in the Solar nebula here at 1 AU exceeded
REDUCING ATMOSPHERE 1000 K (Bell et al. 2000). If true then the Earth formed
It is presumed that the early Earth would have had an hot and relatively devoid of atmosphere as a result, and
atmosphere of simple gases of the type seen in space, subsequent impacts did not help any either (Sleep et al.
or other planetary atmospheres, and/or predicted to 2001). Instead of being a kind of gaseous placenta, our
be present based on models of how the Earth formed. atmosphere is thought to have accumulated about the
Then, with these simple gases, you see if you can planet thereafter by outgassing (Allegre et al. 1987;
make biotic or prebiotic monomers by adding energy. Turner 1989; Farley & Neroda 1998) from the Earth.
Miller’s spark discharge experiments (Miller 1953) When a Mars-sized object collided with the Earth
were probably the first and certainly the most famous leading to the formation of the Moon (Palme 2004),
modern experimental attempt of that kind to make that must have blown away any atmosphere or ocean
the primordial soup about which Darwin, Oparin and that the Earth had built up during those tens of millions
Haldane had written. The landmark Miller–Urey of years after planet formation (Sleep et al. 2001).
experiments showed how those first components of Continued outgassing punctuated by the occasional
the first self-replicating molecule could easily be giant impact led to an atmosphere, but very different
made by cooking up a little early Earth in a flask. from that of Jupiter in both the manner of formation
The experiment consisted of running sparks (light- and the composition.
ning) into a glass sphere (see figure 1) containing a Geologic data suggested that the Earth has been at
reduced1 gas mixture of simple molecules, such as or near its current oxidation state for over 3 and
hydrogen, ammonia and methane (the atmosphere), probably close to 4 billion years (Delano 2001),

Phil. Trans. R. Soc. B (2006)

 Sources of prebiotic matter M. Bernstein 1691

implying an atmosphere composed of neutral or wonderful place to make or maintain things that are not
perhaps even oxidized gases, such as H2O, CO2 and really stable in the thermodynamic big-long-run-
SO2. Such an oxidizing mixture on the early Earth picture, like us or anything else alive. By all thermo-
would make it more difficult to make organic dynamic rights we should all really be CO2 and H2O,
compounds like amino acids, by spark discharge rather than what we are, and it is under such temporary
(Stribling & Miller 1987). My understanding is that kinetic conditions that organic molecules and life
while most agree that the atmosphere was not reducing survive. Like a scalding kiln against the far wall of a
(Abelson 1966; Walker 1977; Kasting & Eggler 2002; pottery studio where things can be heated until set, but
Chyba 2005), on the other hand, there is no consensus then are removed and put aside to cool, the hot interior
that it was oxidizing either. Last year, there was a report of the vent is an enclosed hot place where molecules are
asserting that even if the early atmosphere were presumably made and then flow out into the surround-
dominated by CO2, the rate of escape of hydrogen ing water to cool. Avoiding an extended stay in the hot
from the Earth had been overestimated; therefore, water that would surely hydrolyse our putative newly
more molecular hydrogen would have accumulated in formed protein (or whatever) is important to the
the Earth’s atmosphere than was previously thought success of the laboratory experiments that demonstrate
(Tian et al. 2005). This hydrogen in turn would have the potential of hydrothermal vents for prebiotic
allowed for some terrestrial synthesis of organic chemical synthesis. In practice, building up oligomers
compounds (as simulated by spark discharge) albeit in the laboratory involves cycling the solution round
less efficiently than with the original Miller gas mixture and round through the heated synthetic chamber and
(Stribling & Miller 1987). the cooled quench, and presumably this is representa-
tive of the cycle of water around hydrothermal vent
systems (figure 2).
3. HYDROTHERMAL VENTS The cycling of synthesized organics into a cooler
In any case, if the spark discharge method of making environment where they are more stable deals nicely
organic molecules is not as important as it was with one of the objections that has been raised to a
originally thought to be, there are many other ways in static warm pond: that while one might be able to build
which organic molecules may have formed on the early up a biopolymer like a protein there, the abundant
Earth. One very logical approach is to follow the water that is all around this protein will, eventually and
hydrogen. After all, even if it turns out that the early inevitably, add to the peptide bonds and break it down,
atmosphere was not Jupiter-like, one might still find a and the warmer the faster (Cronin & Chang 1993).
place where the conditions are fairly reducing and Putting proteins in warm water is, after all, what we do
therefore organic synthesis should be possible. Perhaps to cook them, and keeping them cool in the fridge is
the most popular sites for potential organic synthesis in what we do to preserve them.
this vein are hydrothermal vents (figure 2), and with Taking this to the logical extreme, we should consider
good reason. Reducing gases emerge there, at least organic synthesis at very low temperatures, since our
today, and presumably the early Earth was even more prebiotic organics will survive there. As water freezes it
tectonically active than today, so, there would have concentrates solutes just like an evaporating pond, but
been a great many of them early on. avoiding the break down of potential biopolymers that
Personally, I think that hydrothermal synthesis automatically comes with elevated temperature. The
enjoys a certain psychological advantage over gas- problem, of course, is that while the molecules that you
phase syntheses since humans are used to thinking have made do last longer, the reactions that synthesize
about reactions in hot liquid, and hence the notion of these molecules go slower at low temperature too,
the primordial ‘soup’ is so popular. Be that as it may, hence, one must be patient. The chemist’s rule of thumb
the laboratory experiments simulating the conditions in is a factor of 2 or 3 for every 108C, so, between boiling
hydrothermal vents have been highly promising, and freezing pure water the difference in rate should be
yielding lipids and related compounds (McCollom in the range 210–310 (approx. 103–105). In what must
et al. 1999; Rushdi & Simoneit 2001), amino acid hold the record for the longest experiment ever
formation (Hennet et al. 1992) and oligomerization performed, Stanley Miller and co-workers published a
(Islam et al. 2003; Yokoyama et al. 2003; Imai et al. report on the prebiotic synthesis of purine and
1999), nucleotide oligomerization (Ogasawara et al. pyrimidine bases from a dilute solution of ammonium
2000) and pyruvate (Cody et al. 2000, 2001, 2004). A cyanide solution frozen at K788C for 27 years! (Levy
caveat on this subject: Smirnov & Schoonen (2003) et al. 2000; Miyakawa et al. 2002). Similarly, however,
warn that stainless steel, which has sometimes been less dramatically, it had been shown previously that
part of these laboratory equipment, can act as a catalyst hydroxy, amino and carboxylic acids can be formed in
for certain reactions under hydrothermal conditions; aqueous solutions at K108C (Lerner 1995). Not only
hence, one has to pay attention to experimental details. can starting materials be made under these conditions,
This is obviously only a cursory glance at this subject, but template-directed RNA oligomerization was
please see Holm & Andersson 2005 for a recent review. recently shown to be remarkably effective in frozen
In addition to being a potential locally reducing seawater with temperature variation, yielding chain
environment, hydrothermal vents are also good sites for lengths of up to 400! (Trinks et al. 2005).
prebiotic organics owing to the way that they are Regardless of whether it is spark discharge experi-
perched upon gradients. I suspect that subsequent ments intended to simulate lightning in the atmos-
speakers may touch on this and probably could explain phere, evaporating ponds, hydrothermal vents or
this far better than I but, briefly, a gradient is a freezing solutions, there are various ways to make

Phil. Trans. R. Soc. B (2006)

1692 M. Bernstein Sources of prebiotic matter

Figure 2. (a) An image of a smoker from the Lost City

hydrothermal vent field from the University of Washington
([Link]/newsroom/news/images/lostcity/).
(b) Schematic of circulation of seawater through a hydro-
thermal vent. Image from Yvonne Ibarra (NASA Ames).

impacts will oligomerize amino acid monomers (Blank

et al. 2001) and make other organic molecules (Mimura
1995; Gerasimov et al. 2000; Managadze et al. 2003).
Despite the drama of the aforementioned big bolide
impacts, most matter from space that comes to the
surface of the Earth is in the form of micrometre-sized
comet and asteroidal dust (also known as interplanetary
dust particles, IDPs; figure 3). Since there was a lot more
Figure 1. The kind of experimental apparatus used by Stanley debris floating around the early Solar System, there was,
Miller to perform his landmark early Earth simulation perhaps, a million times more matter falling onto the
experiments involving the spark discharge of a reducing gas
early Earth than there is today (Chyba & Sagan 1992).
mixture. Reproduced with permission of Prof. S. Miller of
UCSC (Miller 1953).
This would imply a prebiotic source of organic
compounds that would rival or exceed that produced
prebiotic organic molecules, and they all seem to be by a Miller-type synthesis using a CO2–H2 atmosphere
reasonable, to various extents, depending on what one (Stribling & Miller 1987; Tian et al. 2005), but it
believes of the early Earth. Depending on the depends on how much dust one thinks there was
oxidation state of the atmosphere, the prevalence of 4 billion years ago, and this is rather unconstrained. In
hydrothermal vents, or whether or not the Earth had any case, this suggests a different scenario for making the
enough greenhouse gases to avoid freezing over, either Earth habitable where important inputs came from off
one or another of the processes mentioned will allow the Earth. Since the primordial soup was such a
for the synthesis of some organic molecules. In memorable image, I have come up with a gustatory
addition to all these terrestrial sources of organics, metaphor for this exogenous delivery; please think of it
there is another one too; we know that tons of organic as the cake mix theory (figure 4). The idea is that unlike a
molecules from space are swept up by the Earth every soup from a can that comes containing everything and
day (Love & Brownlee 1995), and perhaps these needs only to be warmed up, a cake mix has most of what
molecules played a role in making the planet habitable you need but usually requires that something be added,
(Oró et al. 1991). such as some milk or butter. Similarly, our forming
Earth too has most of what it needs, but perhaps not all
of the moisture and organic matter that would be helpful
4. EXTRATERRESTRIAL INPUT to make the planet habitable. It is probable that much of
In Hollywood and among dinosaur-obsessed children, the organic matter delivered to the early Earth was
the best known way that extraterrestrial matter comes destroyed, and hence it may not matter what molecules
to Earth is in the form of a large comet or asteroid that arrived, only that it included organic carbon. On the
has to be deflected by Bruce Willis else it will release a other hand, perhaps there is more to it than just reduced
tremendous amount of energy leaving mayhem and carbon; maybe the compounds that are delivered
thermal decomposition of organic molecules in its actually matter, since as we shall see, the list of
wake. One’s intuition might suggest that such events extraterrestrial organics includes nearly everything a
are only destructive, but that is not the case. Not only prebiotic chemist could want.
can compounds survive such impacts (Pierazzo & Some infrared (Flynn et al. 2004) and mass spectra
Chyba 1999), but such cataclysms too are an (Clemett et al. 1993) of IDPs exist, and new techniques
opportunity for organic synthesis. Calculations suggest are being developed for the analysis of comet dust from
that, locally, an impactor can create an environment the Stardust mission, but our knowledge of the organics
conducive to the synthesis of reduced carbon in IDPs is limited by their microscopic size. Far more is
compounds by Fischer–Tropsch (F–T)-type reactions known about the carbon compounds in meteorites, and
(Chyba & Sagan 1992; Kress & McKay 2004). In they are also thought to derive from comets and
addition, experiments have shown that hypervelocity asteroids; hence, it is assumed that the organic

Phil. Trans. R. Soc. B (2006)

 Sources of prebiotic matter M. Bernstein 1693

(a) (b)
0.5
oxygen-XANES spectrum of a
C-rich region of an IDP
0.4

C=O
0.3

–ln (I/IO)
0.2

0.1

0.0
510 520 530 540 550 560
energy (eV)
Figure 3. (a) A Scanning electron microscope image of L2021C5, an ca 10 mm IDP, and (b) an oxygen Xanes spectrum showing
the presence of carbonyl functional groups estimated at the per cent level. These particles can contain over 90 vol% of carbon.
Reprinted from Flynn et al. 2004, with permission from Elsevier and the author.

molecules in IDPs resemble those in meteorites. Thus,

when people talk about the organic matter delivered to
the early Earth, they inevitably quote lists of molecules
from meteorites rather than in IDPs, even though this
may not be quite correct.
Let us do a quick comparison of some of the
similarities and differences in the organic matter in
meteorites and IDPs. In both IDPs and meteorites,
most of the carbon is in the form of a complex, insoluble,
coal-like macromolecular network of reduced carbon,
sometimes called ‘kerogen’ in analogy with terrestrial
biotic detritus for which this name is generally reserved.
This macromolecular matter is dominated by hydro-
carbons, both aromatic and aliphatic, but not composed
solely of carbon and hydrogen. Oxygen is common,
nitrogen is present, and there are often deuterium
enrichments and other isotopic anomalies.
There are some known differences between the
organics in IDPs and meteorites, however. For one
thing, carbon-rich meteorites have just a few per cent
organic carbon, a factor of 10 less than IDPs, which can
be up to 50% organic carbon by mass. For another, the
distribution of functional groups in meteoritic kerogen
seems to be different than that in IDPs. I base this on Figure 4. A cake mix as the new gustatory metaphor to
solid-state NMR data (figure 5) indicating that roughly replace the primordial soup as a way to think of what was
one in 10 carbon atoms in meteoritic kerogen has a needed for life to arise. Unlike a can of soup that has
double bond to oxygen (CaO) such as a ketone or acid everything already inside, the early Earth may have been more
like a boxed cake mix that requires the addition of some
(Cody & Alexander 2005), whereas IR spectra of IDPs
moisture and fat. The forming Earth acquired moisture and
(figure 3) are consistent with only one or two per cent organic matter from asteroids and comets and it is thought
CaO (Oró et al. 1991). Perhaps the measurements of this helped to make life possible. Image credit: (NASA Ames)
IDPs and meteorites, which rely on different methods, and Karen Harpp (Colgate).
are not really comparable, i.e. there is no real
difference. I had presumed that this greater abundance very differently on IDPs versus meteorites given the
of CaO in meteorites was real and representative of the difference in size (centimetres versus micrometres).
C/O ratio in general, that the carbon in meteorites was Regardless of whether these differences between them
more oxidized than in IDPs. are significant or not in terms of the inventory of
Rumours of results from the analysis of Stardust prebiotic organic compounds, I will now blithely treat
samples of cometary dust suggest that I have probably meteoritic molecules as representative of what was
oversimplified in extrapolating in this manner. In any available on the early Earth.
case, it is probable that although the suite of organics in Extractions have shown that carbon-rich meteorites
IDPs and meteorites is somewhat different they do contain abundant individual soluble molecules of
share a common source. It would not be surprising if prebiotic interest, including hydroxy-, imino-, keto- and
something in formation preferentially depleted meteor- amino acids (Pizzarello & Cooper 2001; Kminek
ites of hydrocarbons, or subsequent processing acted et al. 2002), nucleobases and other N-heterocycles

Phil. Trans. R. Soc. B (2006)

1694 M. Bernstein Sources of prebiotic matter

(a) (b) 100

VACP 13C MAS NMR

normalized spectral intensity (%)

aromatic carbon
80 C=O + COOH, R
CHxO
CR2 aromatic CHx
(EET92042)
CH2+CH
CH3

COOR CHxO
C=O
SB
SB 20

400 300 200 100 0 –100 –200 0

CR2 CI1 CM2 C2
(EET92042) (Orgueil) (Murchison) (Tagish lake)

Figure 5. (a) NMR spectrum and (b) bar graph indicating a substantial amount (i.e. approx. 8% of the total) of the insoluble
carbon in meteorites is in the form of a carbonyl (CaO). Reprinted from reference Cody & Alexander 2005, with permission
from Elsevier and the author.

(Stoks & Schwartz 1982; Basile et al. 1984; Pizzarello

diffuse medium dense cloud
2001), simple sugar-like polyols (Cooper et al. 2001) and
fatty acids (Deamer 1985; Deamer et al. 2002), as well as
many other classes of compounds (Cronin & Chang
1993; Pizzarello et al. 2001; Sephton 2002). These are
exactly the kinds of species that Darwin, Oparin and stellar death and
Haldane would have been happy to use to flavour the mass ejection star and planet formation
primordial soup, and they come ready made to the
Earth from space. It is possible that all these
exogenous delivery
extraterrestrial molecules are subducted, torn apart or
otherwise recast by terrestrial processes, and this
organic matter from space is simply a source of
asteroids
reduced carbon. However, it is equally possible that
comets
the delivery of a particularly rich meteorite to a small interplanetary
pond, or a heavy shower of IDPs at an opportune time dust
particles meteorites
provided a compound that survived and was useful in
some way. For example, the fact that more than one volcanic outgassing
(non-biological) amino acid in more than one meteor- endogenous synthesis
ite shows a bias towards the left-handed form (Cronin hydrothermal vents Miller–Urey syntheses
& Pizzarello 1997; Pizzarello et al. 2004) inevitably image by planet hydrosphere
Jason Dworkin
makes me wonder whether there might have been
some direct connection between the meteoritic Figure 6. From the outflows of dying stars, reactions and
tendency for left and the fact that left-handed amino radiation in the interstellar medium, through nebular and
acids dominate in living things. Or, perhaps, the fatty Solar System chemistry, to impacts and planetary processes
acids from Murchison that self-assemble into bi-layer like lightning and hydrothermal vents, there are myriad ways
vesicles (Deamer 1985; Deamer et al. 2002) provided to make and modify carbon compounds as long as conditions
the first self-replicating molecule with the sequestration are not terminally oxidizing. This image is reproduced
that it needed to avoid being taken advantage of by with perimission from the creator Dr Jason Dworkin of
NASA GSFC.
cheaters (Szabo et al. 2002).
where liquid water is stable, which could have impor-
5. EXTRATERRESTRIAL SYNTHESIS tant implications for organic chemistry (Cohen &
Regardless of the role they played, a rich suite of Coker 2000). Indeed, it is thought that most of the
organic molecules was and is brought to the Earth from amino acids found in meteorites are derived from
space by bits of asteroids and comets, large and small. reactions in liquid water on the parent body (Peltzer
Where do these compounds come from? A meteorite is et al. 1984; Ehrenfreund et al. 2001).
a complex object with materials and modifications However, one cannot explain all the compounds in
overlaid from a series of different eras (figure 6). meteorites in this way; some do not look like the kind of
Proceeding in reverse chronological order, first of all thing that forms in liquid water—hydrocarbons for
many extraterrestrial materials show evidence of having instance. The abundance of surfaces, high tempera-
seen liquid water before they arrived at Earth (Robert & tures and the abundance of hydrogen in the solar
Epstein 1982). This is consistent with models that nebula should drive F–T-type chemistry that would
show that if the parent asteroid or comet from which reduce CO or CO2 to CH4 and N2 to NH3 (Prinn
the meteorite comes was large enough, the heating 1993; Kress & Tielens 2001). CH4 and NH3 are great
from decay of radionuclides could lead to long periods starting materials for making more complex organics,

Phil. Trans. R. Soc. B (2006)

 Sources of prebiotic matter M. Bernstein 1695

Murchison presolar
graphite grain

graphite

C2

scalebars are one micron

C atoms 12 C / 13C
ratio up to 7000

C3

Murchison presolar
SiC crystal
(images by S. Amari)
Figure 7. Carbon molecules first form around dying carbon rich stars, and some of this material survives incorporation into
carbonaceous meteorites as indicated by the presence of isotopic anomalies. The Murchison grains are reproduced with
permission from Dr Sachiko Amari.

but the highly branched structures that are common completeness but instead am just mentioning a few of
among meteoritic carbon compounds seem to be the paths leading to prebiotically more interesting
inconsistent with F–T being the dominant source of molecules here. For those who are interested in knowing
higher molecular weight organic matter. These meteor- more, I offer to lend you any of the books on my shelves
ites contain inorganic and graphitic inclusions that are that give greater detail (Hollenbach & Thronson 1987;
accepted as pre-solar (Ott 1993) and as Dr Thaddeus Bakes 1997; Minh & van Dishoeck 2000).
has told us, rotational spectroscopy has revealed a However, even with all these options, some
plethora of interstellar molecules, some fairly large; so, problem structures still remain. While our laboratory
why not assume there is an interstellar contribution to experiments suggest that interstellar chemistry can
the organic material as well? Figure 6 represents the explain why so many of the meteoritic aromatics bear
complex history of the matter arriving on the early oxygen atoms (Bernstein et al. 1999, 2002a,b, 2003),
Earth, having components contributed from not only and thus why the polar hydrocarbon fractions that
our Solar nebula but also from the interstellar medium contain them are deuterium-enriched (Sandford et al.
and previous generations of stars as well. 2001), the basic carbon skeleton is probably older. It
Perhaps, the most convincing molecular evidence seems that the initial carbon–carbon bonds, molecules
for the interstellar heritage of meteoritic molecules is and carbonaceous dust formed around dying carbon-
their high deuterium (D) enrichment (Cronin & Chang rich stars (Frenklach & Feigelson 1997; Jones 1997)
1993, Kerridge 1999). At low temperatures in dense where the carbon atoms had been made in the first
molecular clouds, deuterium fractionation is expected place (figure 7). Thus, the oldest chemical structures
to be efficient and elevated D/H ratios have been seen in in meteorites date back, with interstellar or nebular
grain mantles (Teixeira et al. 1999) and several gas- modifications, to the previous generation of stars.
phase interstellar molecules, including amino acid Others formed in the interstellar medium, or in the
precursors, such as formaldehyde and ammonia solar nebula, or subsequently in the Solar System in an
(Turner 2001). A reported observation of interstellar asteroid, an impact, etc.
glycine in the interstellar medium (ISM) (Kuan et al. The relative contributions of organic matter to the
2003) and experiments showing the viability of a prebiotic environment from on and off the early Earth
condensed-phase interstellar synthesis (Bernstein are hard to assess because each of the processes we have
et al. 2002a,b; Munoz-Caro et al. 2002) suggest that mentioned are rather unconstrained. Terrestrial,
some meteoritic amino acids formed before the Solar Miller-type synthesis (represented by yellow lightning
System, or perhaps a precursor amino-nitrile was bolts in figure 8) depends on the oxidation state of the
converted to the amino acid in liquid water (Bernstein atmosphere, but, depending on how much hydrogen
et al. 2004). In addition, the vesicle forming (Deamer was present (Stribling & Miller 1987), the predicted
1985; Deamer et al. 2002) meteoritic fatty acids quantities of organic matter would be roughly in the
(Huang et al. 2005) may also be of interstellar origin same very wide range as what might have come from
(Dworkin et al. 2001). comets (Chyba & Sagan 1992), i.e. the equivalent of
There are too many small interstellar molecules and 107–109 kg yrK1.
too much work, both theoretical and experimental, on The amount of organic carbon on the early Earth
processes that lead to them (such as ion molecule was contributed by hydrothermal vents (represented by
reactions) for me to possibly review them here. This is the smoker in figure 8) is unclear to me both owing to
a very limited and personal view, I make no claims at uncertainties in flux and because the only molecule

Phil. Trans. R. Soc. B (2006)

1696 M. Bernstein Sources of prebiotic matter

1012 (a) (b)

O O
UV light,
reducing N
1011 atmosphere NH NH
thymine
organic material provided (kg yr –1)

lightning, nucleotide
1010 reducing N N O (in DNA)
O N O
atmosphere
–O P O
109 hydrothermal OH O
UV light,
HO H H
neutral O–
108 input atmosphere OH H H
from com vents OH H
and asteroetary
107 idal dust OPO3H
particles (ID
Ps)
106 Figure 9. (a) The chemical structure of a base-like molecule
(a flavin) and a sugar covalently bonded together in analogy to
lightning in a that of the bases and sugars in our DNA such as that seen in
105 CO2/H2 = 10 atmosphere the nucleotide of thymine (b). The sugar and base at (a) are
different than those on the right, but the basic classes are the
104 same, as are the arrangement of the ketones in the upper right
4.4 4.2 4.0 3.8 3.6 and the way the sugar is connected, so, would it be a
GA in the past biomarker?
Figure 8. A visual representation summarizing the relative different molecules at different wavelengths and vary by
contributions of some major sources of organic molecules, four orders of magnitude.
both domestic and imported. The numbers are from citations As summarized in figure 8, there were a number of
30 and 60, and the basic layout from a figure by S. L. Miller.
different sources of complex organics on the early Earth
Placing these on the same graph has required some significant
assumptions, and especially in the case of hydrothermal vents
making all kinds of interesting organic molecules.
the comparison is questionable (see text). Clearly, these different organic syntheses contributed
different kinds of compounds depending on the
that we can use as a proxy is methane. Let us consider conditions. However, it does seem inevitable that
the flux first. The position on the figure corresponds certain kinds of molecules, such as simple amino
to an estimate of ca 1–3!108 kg yrK1 (value from acids and fatty acids, must have been present because
Elderfield & Schultz 1996, Table 14) of methane that is we see them arise repeatedly from divergent settings
probably out of date largely owing to the relatively like meteorites, spark discharges and hydrothermal
recent discovery of off-axis sites such as Lost City (an vents. Having made these molecules, I am now looking
old, large, Atlantic hydrothermal vent depicted in forward to seeing what the following speakers will be
figure 2). If such off-axis sites were very common, able to do with them. But before that I would like to
then the above CH4 estimate might be too low take you on a brief exobiology interlude.
(K. Hand 2006, personal communication). On the
other hand, it assumes that this extra CH4 is not 6. CODA: THE SEARCH FOR LIFE IN THE
biological in origin, which it may be. Therefore, in the SOLAR SYSTEM
end, I opted for the more conservative approach and While I know that this is a side path off the main
used the lower older number. Presumably, this value route that we are to take this week, it is hard for a
too would also vary greatly depending on the oxidation NASA scientist to resist trying to use some of what
state of the early ocean and how active one thinks the has been learned from studies of the origin of life for
Earth’s surface and the hydrothermal flux was at the search for life in the Solar System. Many current
that time. approaches to the robotic search for life seem to be
The second problem (alluded to just a moment ago) instrument driven, with proposals to employ ever
with putting vents where they are in figure 8 is that the more sophisticated but off the shelf biotechnology on
form of carbon is methane, an assumed starting landers and rovers to detect proteins and nucleic
material for the other processes, such as lightning, acids. However, the structures of terrestrial biomole-
UV, etc. In other words, in a way, vents are built into cules were almost certainly different in the past, e.g.
the graph inherently since the quantity of complex DNA seems to be modern (Gilbert 1986; Joyce et al.
organics from the other processes depend on methane, 2002; Dworkin et al. 2003), hence there is no reason
at least indirectly via the oxidation state of the to think that alien biomolecules will be so similar to
atmosphere. The vertical position of the vent in this our own that devices designed for earthly life will
diagram really should be determined by the quantity of work at all. The alternative bases (Horlacher et al.
higher molecular weight organics, such as fatty acids or 1995; Liu et al. 2003), sugars (Eschenmoser 1999)
amino acids, but I do not know what that is. and backbones (Schwartz 1986; Nielsen 1993; Orgel
Chyba & Sagan (1992) suggest that synthesis of 1998) that have come out of this community suggest
organics by UV photolysis (represented in figure 9 by how different life may have been on Earth and can
Sun symbols) should actually be the largest source, but help us keep an open mind when thinking about
these numbers also seem to be very uncertain. They are the most difficult cases we may face in the search for
based on estimates of absorption cross-sections of alien life.

Phil. Trans. R. Soc. B (2006)

 Sources of prebiotic matter M. Bernstein 1697

What I mean by this is while we may get lucky and REFERENCES

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Evol. Biosph. 23, 323–327. (doi:10.1007/BF01582083) Smirnov, A. & Schoonen, M. A. A. 2003 Evaluating
Ogasawara, H., Yoshida, A., Imai, E.-i., Honda, H., Hatori, experimental artifacts in hydrothermal prebiotic synthesis
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Publications. (transl. with annotations by S. Morgulis 0016-7037(82)90222-8)
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1700 M. Bernstein Sources of prebiotic matter

Teixeira, T. C., Devlin, J. P., Buch, V. & Emerson, J. P. 1999 in-law, Ken, who is a native speaker of Japanese,
Discovery of solid HDO in grain mantles. Astron. assures me that this translation of the Kojiki is
Astrophys. 347, L19–L22. representative of the original text, so, the agreement
Tian, F., Toon, O. B., Pavlov, A. A. & de Sterck, H. 2005 A does seem to be real. It could be, as you suggest, that
hydrogen-rich early earth atmosphere. Science 308,
there was some exchange of mythology between the
1014–1017. (doi:10.1126/science.1106983)
Trinks, H., Schroder, W. & Biebricher, C. K. 2005 Ice and
Greco-Roman culture and Far East. I do not know if
the origin of life. OLEB 35, 429–445. (doi:10.1007/ this is the case, but others have noted some similarities
s11084-005-5009-1) between Greek myths and the Kojiki. See, for example,
Turner, G. 1989 The outgassing history of the Earth’s Matsumura Kazuo’s essay on Amaterasu versus Athena
atmosphere. J. Geol. Soc. 146, 147–154. at [Link]
Turner, B. E. 2001 Deuterated molecules in translucent and [Link].
dark clouds. Astrophys. J. Suppl. Ser. 136, 579–629. F. Westall (Centre de Biophysique Moleculaire, CNRS,
(doi:10.1086/322536) Orleans, France). Regarding the formation of prebiotic
Walker, J. C. G. 1977 Evolution of the atmosphere. New York, molecules in hydrothermal vent environments, what is
NY: Macmillan. the speaker’s opinion on the possibility of suitable
Yokoyama, S., Koyama, A., Nemoto, A., Honda, H., Imai,
chemical reactions occurring in structures such as
E.-I., Hatori, K. & Matsuno, K. 2003 Amplification of
diverse catalytic properties of evolving molecules in a beehive structures, which are highly porous and have
simulated hydrothermal environment. Orig. Life Evol. strong gradients in temperature and chemistry?
Biosph. 33, 589–595. (doi:10.1023/A:1025741430748) Max Bernstein. I think that it makes sense to look to
such structures since some such solids are known to be
good catalysts, and depending on the temperature of
Discussion precipitation might well sit at a temperature interface
Sydney Leach (Départment Atomes et Molécules en that is advantageous, as I advocated above. From my
Astrophysique, UMR CNRS, Observatoire de Paris- reading of Holm & Andersson (2005), it seems that it’s
Meudon, France). I am much struck by the amazing very important to include minerals in the simulations.
similarity, not only in substance, but also in the very I think that we will probably hear more about this kind
words, between the paragraph you cited from the Kojiki of situation later this week during the talk by Professor
and the cosmogenical statements of Ovid in book I of Wächtershäuser.
his ‘Metamorphoses’. A sample of the Latin text is as J. I. Lunine (Lunar and Planetary Sciences Department,
follows: University of Arizona, USA). You have outlined a large
number of possible states for the early Earth’s
Ante mare et terras et, quod tegit omnia, caelum,
atmosphere and a large number of possible chemical
unus erat toto naturae vultus in orbe,
states in which organic molecules might have been
quem dixere Chaos, rudis indigestaque moles
synthesized and evolved. However, a key issue is
nec quicquam nisi pondus iners congestaque eodem
whether we can distinguish among these various
Non bene iunctarum discordia semina rerum.
physical and chemical states, to better constrain the
The translation of this sample by Mary Innes in the conditions present on the early Earth—and how we
Penguin Classics version of ‘Metamorphoses’ is: might do so. In the absence of this advance, I am
Before there was any Earth or sea, before the canopy concerned that we cannot make much progress on the
of heaven stretched overhead, Nature presented the question of the origin of life. So, how do we decide what
same aspect the world over, that to which men have portion of your kitchen is really relevant to life’s origin?
given the name of Chaos. This was a shapeless Max Bernstein. Yes, I am sorry to have been so vague as
uncoordinated mass, nothing but a weight of lifeless to which one was the most important; I was so, not by
matter, whose ill-assorted elements were indiscrimi- choice, but out of ignorance. It seems that we are in the
nately heaped together in one place. uncomfortable position—to continue with your meta-
The Latin is actually closer to the Kojiki text. It also phor—of having a number of cooks proceed in different
goes on to talk about the separation of Earth and parts of the kitchen and then decide what tastes
heaven (by a god) and the separation out of light and best afterwards, with little say in advance as to which
heavy elements. recipes should be used. Personally, I feel that it is
This has made me wonder whether the Japanese of always safest to be pessimistic. So, lets presume that the
the eighth century had cognisance of Ovid’s first early atmosphere was at most neutral, not reducing;
century poem. Certainly, the Romans were in touch there will still be Miller discharge synthesis and
with China, via the Silk Road and Nestorian Christians photochemistry, but limited in scope. Similarly, lets
were very early in China. The Japanese of course had take the lower estimates of the flux of IDPs, so, we have
much contact with China. Who knows.A good something to work with but will not be seduced by
subject for a Ph.D. student? stories of metres thick layers of organic goo raining
Max Bernstein. You are right, the similarity is indeed down on the surface from these sources.
striking, Ovid does also talk about some material rising M. Wallis (Cardiff Centre for Astrobiology, Cardiff
and other settling down and it’s impressive that Ovid University, UK ). There’s a longstanding mystery with
knew the Earth was a ‘ball.’ I wondered at how familiar IDPs—how their hydrated minerals could form, when
the Kojiki creation story seemed as I read it the first liquid water is not stable on surfaces of small
time and whether the original really had this sense, or if atmosphere-less bodies. Their temperature is generally
the translator had been influenced by western science too low for mobile H2O monolayers on crystalline
or myths in producing the English version. My brother- surfaces. Intermediate size bodies must be the

Phil. Trans. R. Soc. B (2006)

 Sources of prebiotic matter M. Bernstein 1701

processing site for classes of IDPs. Comets are one Max Bernstein. I am incredibly excited about the
obvious candidate—composed of weakly coherent, stardust mission ([Link]/) which, this
weakly gravitating material that readily disintegrates past Jan. 15, returned to Earth samples from comet
under Jupiter perturbations and under solar heating Wild 2. It is still quite early in the sample analysis, the
when in the inner Solar System. Planetary bodies are preliminary teams are still examining the aerogel tiles,
also a source of meteorites and IDPs via major but it’s clear that there are specific compounds. At this
stochastic collisions, as even for the Earth in the point, there is little information on the organic material
Chioxutub impact. Material processing in comets and both because the organic matter does not retain its
planets surely generates complex organic and even integrity on impact into the aerogel as well as the
biological material that are very different and poten- minerals grains and because they are still trying to
tially important components of the interstellar cloud. distinguish between cometary organics and contami-
Max Bernstein. Your points about the composition of nation. The preliminary examination team for organics
IDPs and the parent bodies from which they come as intends to submit a number of manuscripts to science
important sites for chemical synthesis are very good. in the fall of 2006.
IDPs are rather complex, with high temperature C. N. Matthews. Your discussion of the Miller–Urey
components mixed with very fragile organics that experiment and the detection of a-amino acids in space
cannot possibly have formed in the same environment, need amplification. We have shown that such reactions
so I am sure there is a complex history there that give rise to hydrogen cyanide polymers which can then be
involves lots of mixing and collisions in the nebula. hydrolysed/pyrolysed to yield a-amino acids, peptides
Regarding planets as a source of meteorites and and nitrogen heterocycles such as adenine. All detections
IDPs, well, I am sure that you are correct that some of a-amino acids need to be reinterpreted. They are
dust comes from the collision of larger bodies, and in formed from methane, ammonia mixtures, etc., via
the early Solar System there certainly were more of hydrogen cyanide, which polymerizes readily and gives
these kinds of collisions going on. However, I think that rise to polypeptides when treated with water. Further
today most meteorites and IDPs are from asteroids and hydrolysis yields a-amino acids.
comets or bodies smaller than planets anyway. There Essentially this answers a key question in prebiotic
are certainly examples of meteorites known to be from chemistry: how do polymers such as proteins form?
Mars, based on trapped gasses, and Lunar meteorites They form directly from HCN polymers and water,
that are basically basalts, but my understanding is that without the need for the prior synthesis of a-amino
few meteorites or IDPs have compositions and acids by the Strecker mechanism or any other
structures consistent with being fragments of planets. procedure.
Of course, we will know more about comet dust very Max Bernstein. Certainly, one can form amino acids
soon after the stardust samples have been analysed, so and nitrogen heterocycles such as adenine from HCN
it is to be hoped that we will know how to distinguish and it seems reasonable that some of the molecules
comet dust from other sources. observed by Miller could have been derived from
As to evidence of hydration, that is very strong, but I such a pathway given that they did see HCN
am not convinced that this requires a planetary formation in reduced gas discharge experiments.
precursor where liquid water was stable at the surface. See, for example, Stribling & Miller (1987),
A comet or asteroid, if it were large enough, could have pp. 48–52, where they assess the efficiency of HCN
liquid water in the interior, from the heat provided by formation in H2, CH4 and NH3 gas mixtures such as
the decay of radionuclides, or so, I have read. See, for are found in the atmospheres of giant planets and
example, Cohen & Coker (2000). Thus, it has been were originally presumed to have been present on the
suggested that the organic chemistry of carbonaceous early Earth.
meteorites is partly a result of this kind of parent body As for meteoritic amino acids, I cannot be so
aqueous alteration chemistry. Certainly, many of the sanguine. Allow me to first confess that I am a fan of
water-soluble species in meteorites are consistent with alternative mechanisms for formation of amino acids
the hydrolysis of known interstellar molecules (e.g. and have published one of my own involving ice
meteoritic carboxylic acids having derived from inter- photolysis (Bernstein et al. 2002a,b; Munoz-Caro
stellar nitriles) or the combination of simple interstellar et al. 2002). However, a big limitation of your HCN
species into more complex compounds (e.g. for- polymer and my ice photolysis mechanism is that while
maldehyde, ammonia and HCN into glycine). I believe we mostly make glycine, we do not form many of the
that this aqueous alteration happened, and perhaps other amino acids that are seen in meteorites. For
this is the origin of the hydrous minerals in IDPs. example, aminoisobutyric acid in CM chondrites is
I am no expert and I would guess that there are taken as an indicator of a Strecker synthesis, and the
other explanations. The hydrated minerals rimming b-alanine in Orgueil has been suggested to have formed
chondrules in CM chondrites have been attributed to a via a Michael addition (see Botta (2002)).
nebular shock (Ciesla et al. 2003) and perhaps given I see that Professor Ferris has a comment.
enough time hydrated minerals could even form under J. P. Ferris. (Department of Chemistry and Chemical
more gentle conditions. Biology, Rensselaer Polytechnic Institute, New York, USA).
C. N. Matthews (Department of Chemistry, University of It is not reasonable to propose that HCN polymers are
Illinois at Chicago, USA). What do you think of the the source of all prebiotic molecules from comets,
Stardust Mission which has just brought to Earth asteroids and the Miller–Urey process since there are
samples of cometary dust for analysis? Will these results many other compounds for the HCN to react with
tell us about the original organics on Earth? besides HCN.

Phil. Trans. R. Soc. B (2006)

1702 M. Bernstein Sources of prebiotic matter

Max Bernstein. Dr Ferris makes a very good point. might react with one of those other many compounds
The production rate ratio of HCN relative to H2O that Dr Ferris mentioned.
in comets has been reported as ca 10K3–10K4
(e.g. Friedel et al. 2005), implying a low concentration
of HCN relative to H2O in the solid phase. A reaction Additional references
like HCNCHCN/(HCN)2 would depend on the Botta, O. 2002 Relative amino acid concentrations as a
square of the HCN concentration; cutting the signature for parent body processes of carbonaceous
chondrites. Orig. Life Evol. Biosph. 32, 143–163.
concentration of the starting material in half would
Ciesla, F. J., Lauretta, D. S., Cohen, B. A. & Hood, L. L. 2003
diminish the rate of formation of the dimer by a factor A nebular origin for chondritic fine-grained phyllosilicates.
of four. Thus, even though HCN polymerization is Science 299, 549–552. (doi:10.1126/science.1079427)
facile at high concentrations, bringing together many Friedel et al. 2005 BIMA array detections of HCN in
HCN molecules would become unlikely if the comets LINEAR (C/2002 T7) and NEAT (C/2001 Q4).
concentration of HCN is low. Instead, the HCN Astrophys. J. 630, 623–630.

Phil. Trans. R. Soc. B (2006)