Phil. Trans. R. Soc.

B (2006) 361, 1877–1891

doi:10.1098/rstb.2006.1909
Published online 11 September 2006

Conditions for the emergence of life on

the early Earth: summary and reflections
Joshua Jortner*
School of Chemistry, Tel Aviv University, Ramat Aviv, 69978 Tel Aviv, Israel
This review attempts to situate the emergence of life on the early Earth within the scientific issues of
the operational and mechanistic description of life, the conditions and constraints of prebiotic
chemistry, together with bottom-up molecular fabrication and biomolecular nanofabrication and
top-down miniaturization approaches to the origin of terrestrial life.
Keywords: biotic raw materials; building blocks of biomolecules; the chemical universe;
complex biological matter; self-organization; structure–dynamics–function relations

1. PROLOGUE (v) Conditions for the development of primitive life

This discussion meeting has been truly stimulating and forms. These involve information recording and
broad in scope and content. We are particularly retrieval (Eigen 1971, 1996; Lehn 2002a,b,
indebted to Dr Sydney Leach, Professor Ian Smith & 2003; Deamer 2006; Ferris 2006; Taylor
Professor Charles Cockell for arranging this timely, 2006) and energy acquisition and disposal
interdisciplinary and stimulating scientific endeavour. (Canfield 2006; Kasting 2006).
The ‘central dogma’ underlying this discussion (vi) The biological conditions for further develop-
meeting was that life appeared on the early Earth ment of life on Earth. These important,
within 1 billion year (Gyr) of its formation. Several exceedingly difficult and open questions address
facets of the emergence of life (Orgel 1973; Miller & the attainment of biological complexity (Eigen
Orgel 1974; Folsome 1979; Crick 1981; Mason 1992; 1971, 1996; Folsome 1979; Yates 1987; Lehn
Lahav 1999; Deamer & Fleishaker 2005), which were 2002a,b, 2003; Heckl 2004; Deamer 2006;
discussed herein, are as follows. Ferris 2006; Taylor 2006).
(vii) The possible implications of the emergence of
(i) The nature of biotic raw materials (Ferris 2006; life on the early Earth for astrobiology. This
Deamer 2006; Schwartz 2006; Wächtershäuser issue addresses the transferability of the con-
2006). straints and conditions of terrestrial life for the
(ii) The origins of biotic raw materials and why perspectives of extraterrestrial life (Chyba &
and how they were present on Earth. These Hand 2005). The exploration of Mars meteor-
involve terrestrial (Bernstein 2006; Canfield ites (Anand 2006; Grady 2006) touched on this
2006; Deamer 2006; Ferris 2006; Schwartz fascinating issue.
2006) and extraterrestrial sources (Anand 2006;
Grady 2006), including the ‘chemical universe’
of the interstellar medium (Thaddeus 2006).
(iii) The constraints on prebiotic chemistry and the 2. WHAT IS LIFE?
subsequent chemical and biochemical Since Schrödinger (1944) asked the question, ‘What is
evolution. These include the famous presence life?’, the advancement of this provocative, scientific–
of water (Lunine 2006), the possible role of the intellectual challenge has acted as an inspiration to
hot magma (Bernstein 2006), the chemical generations of scientists and scholars (Murphy &
conditions (Canfield 2006; Deamer 2006; O’Neill 1995). In his famous treatise, Schrödinger
Ferris 2006; Kasting 2006), the availability of (1944) inquired whether life is based on the laws of
sources of energy, the prevalence of appropriate physics, because the construction and function of
thermal conditions (Stetter 2006) and the living matter may require a new level of description.
existence of appropriate sites for biosynthesis This hypothesis was transcended by the seminal
(Cockell 2006; Deamer 2006; Ferris 2006). work of Crick & Watson on the structure of DNA,
(iv) The physical and chemical conditions for the which established the structure–function relations in
synthesis of the building blocks of biomolecules biology. Research on the primary processes in bacterial
(Bernstein 2006; Ferris 2006), biomolecules and plant photosynthesis (Deisenhofer et al. 1984;
(Deamer 2006; Ferris 2006) and functional Feher et al. 1989; Michel-Beyerle 1990, 1995;
biostructures (Deamer 2006). Deisenhofer & Norris 1993) extended the traditional
notion of the structure–function relationship.
*[email protected] Dynamic information (in this case, the ultrafast
One contribution of 19 to a Discussion Meeting Issue ‘Conditions for picosecond electron transfer dynamics in the photo-
the emergence of life on the early Earth’. synthetic reaction centre) surpasses and complements

1877 This journal is q 2006 The Royal Society

1878 J. Jortner Conditions for the emergence of life

Scheme 1.

structural information (Jortner & Bixon 1996), provi- only be answered in the twentieth century with the
ding the structure–dynamics–function relations for establishment of the proper molecular composition
central biological processes, which ensure life on Earth. and the structure of the H2O molecule, together with
The description of functional living matter requires a the globally condensed phase properties of the liquid,
holistic conceptual framework, with some of its e.g. H-bonding, local order, radial and angular
cornerstones being: (i) the ideas of Onsager & distribution, solvation, structure breaking, nuclear
Morowitz (Folsome 1979) on complex matter, (ii) the dynamics, phase transitions and response, providing a
implementation of the concepts of molecular infor- conceptual framework of an appropriate scientific
mation at the molecular and supramolecular level theory. Regarding the conceptual framework that will
(Eigen 1971, 1995, 1996; Yates 1987; Lehn 1988, provide answers to the question, ‘What is life?’,
1990, 1995, 1999, 2000, Lehn 2002a,b, 2003; Eigen & Onsager & Morowitz (Folsome 1979), Eigen (1971,
Winkler 1993; Taylor 2006) and (iii) the central role of 1996), Yates (1987) and Lehn (2002a,b, 2003), among
self-organization (self-assembly), which leads to the others, made important contributions, which will
evolution of a ‘complex biological matter’ (Eigen 1971, start to address the significant questions regarding
1995, 1996; Lehn 2002a,b, 2003; Heckl 2004; Deamer the emergence and function of complex biological
2006). A heuristic, highly speculative, partial scheme living matter.
for the emergence of living matter in the ‘parameter A notable attempt to provide a unified description of
space’ of increasing complexity could be as shown in living matter was provided by the Onsager–Morowitz
Scheme 1. definition (Folsome 1979): ‘Life is that property of
The attributes marked by [???] are unknown, being matter that results in the cycling of bioelements in
the most fascinating. aqueous solution, ultimately driven by radiant energy to
The question ‘What is life?’ is not only an extremely attain maximum complexity’. This definition implies
difficult question (Orgel 1973; Miller & Orgel 1974; that coupled cycles involving homogeneous and/or
Folsome 1979; Crick 1981; Lahav 1999; Deamer & heterogeneous chemical reactions of bioelements (i.e.
Fleishaker 2005), but also perhaps not the right prebiotic material, building blocks of biomolecules and
question (Eigen 1995; Chyba & Hand 2005). It is a functional biomolecular structures) in water, which are
popular game in this field to provide robust counter driven by the acquisition and disposal of radiant energy,
examples, which reveal failures in operational result in the organization of complex matter (with
definitions (Folsome 1979; Chyba & Hand 2005). ‘maximum complexity’ presumably referring to infor-
Sagan (1998) catalogues a list of failed attempts, mation content). Of course, there is a ubiquity of
including physiological, metabolic, biochemical, complex matter (with complexity characterized by
genetic and thermodynamic definitions of life, all of spatial, energetic and temporal structure with vari-
which face problems (Chyba & Hand 2005). For ations; Kadanoff 1993) that is not alive. It appears that
example, a metabolic definition finds it hard to exclude the Onsager–Morowitz definition bypasses the
fire (which grows and reproduces via chemical characterization of complex biological matter and how
reactions), a biochemical definition does not exclude it differs from complex chemical matter. Eigen (1971,
enzymes (which are biologically functional but not 1996) addressed the basic differences between
living systems), while a thermodynamic definition does a chemically coupled system and a living system with
not exclude mineral crystals (which create and sustain an abundance of chemical reactions in terms of
local order and may reproduce). To address the information storage, retrieval and processing. Accor-
question ‘What is life?’, one does not require a ding to Eigen (1971, 1996), all reactions in a living
definition, but requires a scientific theory (Cleland & system follow a controlled programme operated from an
Chyba 2002, 2005). A pedagogical example (Chyba & information centre, whose aim is the self-reproduction
Hand 2005) alludes to a much simpler question, ‘What of the programme itself. The three essential
is water?’, which Leonardo da Vinci (1513) faced when characteristics of all living systems yet known (Eigen
he attempted to characterize liquid water in terms of its 1971, 1996) are self-reproduction (without which
phenomenological properties. This question could information would be lost), mutations (which allow

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

 Conditions for the emergence of life J. Jortner 1879

evolution) and metabolism (which allows an optimal approximately 4.0 Gyr ago (Lunine 2006).
choice of a system for a certain function). Eigen (1971, Geological evidence (Watson & Harrison
1996), Yates (1987), Lehn (2002a,b, 2003) and Heckl 2005) indicates that liquid water might have
(2004) advanced and developed the concept of self- been present on Earth 4.3 Gyr ago, in contrast
organization (self-assembly) and proposed that it to the scenario of the magma oceans (Righter &
resulted in the evolution of biological complex matter, Drake 1999).
which rests on the elements, as follows: (i) Molecular (ii) The availability of biotic raw materials (Miller &
structure formation of (living and non-living) matter is Orgel 1974; Folsome 1979; Crick 1981; Lahav
driven by molecular interactions and operates on a 1999; Ferris 2006; Wächtershäuser 2006).
huge diversity of possible structural combinations. (ii) These include the biotic elements (e.g. C, H,
Prior to the biological evolution, the chemical N, O, P, S, Fe, Mg, etc.), the simple biotic
evolution took place, performing a selection on molecules (e.g. H2, H2O, NH3, CO, CO2, H2S,
molecular diversity, leading to the embedment of CH4, S and SO2) and minerals containing Si,
structural information in chemical entities. (iii) The Fe, Ni, P and S (Deamer 2006; Ferris 2006;
implementation of the concepts of molecular infor- Schwartz 2006). Terrestrial sources of biotic raw
mation pertains to information storage at the molecular material can be minerals (Deamer 2006; Ferris
level and the retrieval, transfer and processing of 2006; Schwartz 2006), hydrothermal sources
information at the supramolecular level. (iv) The (Whitaker & Banfield 2006; Bassez 2003;
formation of supramolecular structures is induced by Bernstein 2006; Canfield 2006), marine aero-
molecular recognition (based on non-covalent inter- sols (Donaldson et al. 2004), volcanic exhala-
molecular interactions, e.g. H-bonding, van der Waals tions (Canfield 2006; Wächtershäuser 2006)
interactions, charge transfer in donor–acceptor and the atmosphere of primitive Earth (Miller
sequences and interactions in ion coordination sites). 1953; Miller & Urey 1959; Tian et al. 2005).
This includes self-organization, which allows adap- Considerable attention was devoted to biotic
tation and design at the supramolecular level. (v) Self- raw material from exogeneous sources and, in
organization involves selection in addition to design at particular, to the inventory of organic molecules
the supramolecular level, and may allow the ‘target- of extraterrestrial origin (Chyba et al. 1990;
driven selection of the fittest’ (Lehn 2003), leading to Thomas et al. 1997; Pizzarello 2004; Chyba &
biologically active substances. Hand 2005; Bernstein 2006; Cockell 2006;
The arsenal of self-organization of complex biologi- Thaddeus 2006). These include asteroids,
cal matter driven by information acquisition, storage, meteorites and comets (Chyba et al. 1990;
retrieval and transfer, which allows selection, adap- Thomas et al. 1997), with the Murchison
tation, self-reproduction, evolution and metabolism meteorite (from a comet) containing a variety
(Eigen 1971, 1996; Yates 1987; Lehn 2002a,b, 2003), of organic compounds, including amino acids,
may constitute many of the missing links (marked by purines and pyrimidines, sugar alcohols and
[???]) in scheme 1. Of course, there are many gaps in acids (Pizzarello 2004). The exploration of the
the conceptual framework for the description of chemistry of Mars meteorites pertaining to
complex biological matter reviewed here. In particular, carbon cycles on the early Earth and Mars
the mechanistic aspects of information-driven self- (Grady 2006) and to Fe isotope cycles on Mars
organization and its implications remain to be eluci- (Anand 2006) reflects a perceptive scientific
dated and will be subjected to intensive and extensive approach to the open issues of Martian biologi-
experimental and theoretical scrutiny in the future. cal activity. Interstellar dust particles constitute
Some significant issues involve the inclusion of another potentially important source of pre-
dissipative non-equilibrium processes in living systems biotic raw materials (C, H and N) on Earth
(Haken 1977) and the ‘transition’ from programmed (Chyba & Sagan 1992; Chyba & Hand 2005;
and instructed self-organized systems to ‘learning’ Thaddeus 2006). For some plausible, but
systems, which can be trained (Lehn 2002a,b, 2003). uncertain, early atmospheric models, the come-
tary input of prebiotic building blocks of
biomolecules, such as amino acids, may be
3. EMERGENCE OF LIFE ON EARTH: CONDITIONS important (Pierazzo & Chyba 1999). During the
AND CONSTRAINTS period of 4.6–3.6 Gyr ago, the organic material
Returning to operational and mechanistic descriptions, from comet and asteroid dust amounted to
some of the necessary prerequisites and conditions for 107–109 kg yrK1, i.e. tons per day (Bernstein
the emergence of early life on Earth are as follows. 2006). It is an open question whether this dust
impact has been uniform, which would have
(i) The existence of liquid water as a universal resulted in a monolayer of organic material on
solvent (Darwin 1871; Oparin 1924; Blum the surface of the Earth, or local, which would
1962) owing to its ability for H-bonding, its produce sites for biosynthesis.
function as a medium for reactivity, hetero- (iii) The availability of sources of energy, i.e. solar
geneous catalysis and self-organization (Bernal light, lightening, cosmic rays and heat, which
1949, 1951; Ferris et al. 1996; Ferris 2002, induce the formation of building blocks of
2006; Deamer 2006). Surface liquid water biomolecules (amino acids or nucleobases) from
could become stable within 500 million simple molecules (Miller 1953; Miller & Urey
years (Myr) of the Earth’s formation, i.e. 1959; Folsome 1979; Chyba & Sagan 1992).

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

1880 J. Jortner Conditions for the emergence of life

(iv) The prevalence of appropriate chemical con- transfer (time-scales of 3–200 ps) in universal arrange-
ditions. These are as follows: ment of the prosthetic groups in reaction centres.
(a) The chemical mechanisms for the pro- The primary charge separation in photosynthetic
duction of building blocks of biomolecules reaction centres (figure 1), whose structure is very
(amino acids, nucleobases, phosphates, similar in both bacteria and plants, proceeds via a
sugars and porphyrins) from simple sequence of well-organized, highly efficient, directional
molecules. These may rest on photochemical and specific electron transfer processes between pros-
or radiation chemical radical reactions thetic groups across the membrane protein. Remark-
(Miller 1953; Miller & Urey 1959; Folsome able features of charge separation in both the reaction
1979) or on a heterogeneous catalysis of the centres of bacteria and the photosystem II of plants
Fischer–Tropsch CO/H2 reaction on silicon/ (which allow for a quantum yield Yx1.0 for energy
metal oxides to form amino acids and conversion) on the picosecond time-scales preclude
nucleobases (Folsome 1979). The ubiquity energy waste owing to energy backtransfer to the
of clay minerals was important for the antenna and intramolecular energy damping (Bixon &
following: (i) adsorption of relevant molecu- Jortner 1999). Another fascinating structural feature
lar species from solution (Bernal 1949, 1951) of the reaction centres (figure 1) pertains to the two-
and (ii) the clay-catalysed formation of branched membrane protein (Deisenhofer et al. 1984;
biomolecules (e.g. polypeptides, proteins Feher et al. 1989), with the prosthetic groups
and nucleobase oligomers), DNA and, in symmetrically arranged across the two branches,
particular, RNA (Ferris et al. 1996; Orgel resembling a ‘Gothic window’ (figure 1). A notable
1998a,b; Ferris 2002, 2006; Leman et al. feature of ultrafast picosecond electron transfer in the
2004; Deamer 2006; Taylor 2006). bacterial photosynthetic reaction centre involves
(b) The composition of the atmosphere of the structural redundancy manifested in symmetry break-
early Earth (Miller 1953; Miller & Urey ing, i.e. unidirectionality of charge separation across a
1959; Stribling & Miller 1987; Tian et al. single ‘active’ branch of the (two-branched) mem-
2005; Canfield 2006; Kasting 2006). brane protein (Paddock et al. 2005; Poluektov et al.
(c) Appropriate thermal conditions, with the 2005). Similar features are manifested for the
temperatures being sufficiently high to drive photosystem II of plants. This structural redundancy
activated chemical reactions (Chyba & optimizes different functions of the end quinone
Hand 2005), although nuclear tunnelling groups in the ‘active’ and ‘inactive’ branches. The
can prevail at exceedingly low temperatures structural redundancy of the photosynthetic reaction
(Goldanskii et al. 1986). Concurrently, the centre, with the inactive branch serving as a structural
temperatures should not be too high to element, may lead to the conjecture that the
ensure thermal stability, with extreme con- development of the early forms of photosynthetic
ditions prevailing for the existence of bacteria was based on a single-branched system. The
hyperthermophilic bacteria surviving up to activity and composition of the ancient atmosphere in
1138C (Stetter 2006), with this limit extend- the Early Archaean period were driven by Fe-based
ing to 1218C (Kashefi & Lovely 2003). anoxygenic photosynthesis (Canfield 2006). Geologi-
(d) The existence of proper sites for biosynthesis cal evidence revealed the existence of anoxygenic
(Cockell 2006; Ferris 2006; Deamer 2006). photosynthetic organisms dating back to 3.4 Gyr ago
(v) Energy acquisition and disposal by functional (Westall 2006), while oxygenic photosynthetic organ-
biological systems. This could be achieved by isms emerged approximately 2.7 Gyr ago (Canfield
early photosynthesis, although it is an open 2006; Kasting 2006). The nature of the (single- or
question whether primitive oxygenic photosyn- double-branched) structure of the early photosyn-
thetic organisms, which date back to 2.7 Gyr ago thetic organisms is an open problem.
(Canfield 2006; Kasting 2006), preceded early
forms of life such as prokaryotic cell organisms,
or vice versa. This estimate is important for 4. THE CHEMICAL UNIVERSE
dating the transformation of the early Earth’s Interstellar dust particles (Leach 1996; Thaddeus
atmosphere from a chemically reducing to 2006) might have been a source of prebiotic carbon,
oxidizing medium. hydrogen and nitrogen (Chyba & Sagan 1992; Chyba &
Hand 2005), perhaps pointing towards the intercon-
Energy acquisition, storage and disposal by living nection between the interstellar chemistry and the
systems on Earth proceed in one of the two ways: by terrestrial origin of life (Ehrenfreund et al. 2002).
either the use of chemical energy through respiration or The spectroscopic mapping of the universe by
fermentation (involving donor–acceptor electron radioastronomy (Le Tueff et al. 2000) and optical
transfer processes) or the conversion of light energy spectroscopy (Leach 1996; Thaddeus 2006) focused
into chemical energy. The latter process involves on the chemical composition of both planetary
photosynthesis in both bacteria and plants (Deisenhofer atmospheres (Chyba & Hand 2005) and the interstellar
et al. 1984; Feher et al. 1989; Michel-Beyerle 1990, medium (Leach 1996; Thaddeus 2006). These studies
1995; Deisenhofer & Norris 1993). The two initial steps provided important information on the following: the
of photosynthesis involve ultrafast electronic energy cosmic abundance of the elements (Le Tueff et al. 2000;
transfer (time-scales of 70 fs–100 ps) in different Thaddeus 2006); the molecules in outer space
non-universal antenna structures and ultrafast electron (Thaddeus 2006); and the infrared (Cook et al. 1996;

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

 Conditions for the emergence of life J. Jortner 1881

(a) Leach 1996; Cook & Saykally 1998; Gibb et al. 2000;
P
Peeters et al. 2004) and visible (Herbig 1995; Snow
BB 2001) interstellar bands that give clues to the molecular
BA nature of interstellar dust (grains) and the elucidation
of chemical reactions in outer space with the formation
of cosmic dust (Leach 1996; Thaddeus 2006).
Spectroscopic studies are of considerable signi-
ficance for the unambiguous identification of prebiotic
single molecules and dust containing biotic raw
material in the interstellar medium. These may
provide biotic raw material on Earth and a molecular
HB HA
basis for astrobiology (Chyba & Hand 2005). From
the present spectroscopic information on the inter-
stellar molecules, the following points were inferred.
QA
QB (i) To date, 135 molecules were identified (Thaddeus
2006). (ii) Most of these molecules were carbon-based
organic molecules (with the largest abundance of H, C
(b) and N), while molecules containing Si, P, S, Mg, Na
1P* and K were also observed (Thaddeus 2006). (iii) The
P+BA–
largest molecule observed (Thaddeus 2006),
3.5 ps H–(CbC)5–CN, contains 13 atoms (molecular weight
P+HA–
0.9 ps 147). (iv) No conclusive evidence for amino acids
3P* was obtained. Recently, there has been a report (Kuan
1 ns et al. 2003) on the detection of glycine in the
200 ps interstellar medium, which created quite a stir in the
P+QA–
astronomical community (Hollis et al. 2003).
P+QB–
ns

However, a subsequent analysis (Snyder et al. 2005)

100 µs
00

50 µs indicates that the spectroscopic evidence is incon-

–1

ms
20

100 clusive and the possible detection of glycine is to be

taken very cautiously. (v) Interstellar grains (of
>1 s
approx. 1000 Å in size) constitute clusters of large
P organic molecules (Thaddeus 2006). Self-assembly
may be operative in the ‘transition’ from molecules to
grains. (vi) The diffuse infrared interstellar emission
(c) bands, which were assigned to C–H and C–C
vibrations (Cook et al. 1996; Leach 1996; Cook &
Saykally 1998; Peeters et al. 2004), are the best
present evidence for the identification of dust as large
structures of organic molecules. (vii) The unidentified
200–300 diffuse interstellar bands, which range from
ultraviolet to near-infrared region (Herbig 1995;
Leach 1996; Snow 2001; Thaddeus 2006), present
an outstanding astronomical, physical, chemical and
spectroscopic challenge. The electronic spectra of
polycyclic aromatic hydrocarbons or their cations
were considered as possible candidates (Leger et al.
1987; Leach 1996; Bréchignac & Pino 1999). A recent
intriguing proposal (Zhou et al. 2006) attributed these
bands to short single-wall carbon nanotubes, e.g.
C160H20, with the size distribution giving rise to the
Figure 1. The bacterial photosynthetic reaction centre of large number of bands. This proposal again points
Rhodopseudomonas viridis portraying (a) the structure towards the prevalence of huge organic structures in
(Deisenhofer et al. 1984) and (b) the electron transfer the interstellar medium.
dynamics (Michel-Beyerle 1990, 1995; Deisenhofer & Norris Molecules from other galaxies, which were identified
1993; Bixon & Jortner 1997). (c) The structure of the by Phil Solomon (Le Tueff et al. 2000; table 1), contain
membrane protein that contains the prosthetic groups. a variety of organic molecules, with the largest molecule
The spatial structure of the prosthetic groups in (a) containing seven atoms, and H20, NH3, SO and SiO
(P, bacteriochlorophyll dimer; B, accessory bacteriochloro- were also identified. The ubiquity of carbon-based
phyll; H, bacteriopheophytin; Q, quinone) reveals two
molecules in the interstellar medium and, in particular,
branches (labelled A and B). In (b), the kinetic scheme for
charge separation with the individual rates (marked on the
from other galaxies provides a tentative empirical
arrows) reveals the dominance of sequential charge separ- indication that carbon-based chemistry may dominate
ation to Q A over the recombination processes. The structural over silicon-based chemistry. However, it should be
redundancy is manifested by the exclusive charge separation borne in mind that carbon is a much more abundant
across the single (A) branch. element than silicon. Furthermore, most silicon

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

1882 J. Jortner Conditions for the emergence of life

Table 1. Molecules in other galaxies. (Adopted from Phil can also survive such hypervelocity impacts
Solomon (Le Tueff et al. 2000).) (Pierazzo & Chyba 1999), providing favourable
conditions for the exogeneous delivery of
organic materials on Earth.

The dynamics of impactor–target collision pertains

to the chemical physics of matter under extreme
conditions. A microscopic physical analogue for
macroscopic impact events is provided by high-energy
cluster–wall collisions. Such processes are triggered by
the acceleration of atomic and molecular cluster ions
(containing 10–104 constituents with velocities up to
approximately 100 km sK1 and kinetic energies up to
compounds, which have a much lower condensation 100 eV per particle), which collide with a molecular
temperature than the corresponding carbon or metal solid surface (Schek et al. 1994; Schek &
compounds, will be trapped as condensates in dust Jortner 1996). Thermal femtosecond dynamics of
and will not be easily amenable to identification as free- these high-energy clusters (Schek et al. 1994) provide
flying molecules. The open issue of carbon-based a medium for reactive processes, such as dissociation
chemistry versus silicon-based chemistry in other of diatomics embedded in the colliding cluster
galaxies is of considerable relevance for astrobiology (figure 2). More interestingly, these impact phenomena
(Chyba & Hand 2005). induce novel and isoteric chemical processes, such as
the N2CO2/2NO reaction of the burning of nitrogen
(Raz & Levine 2001), providing a basis for novel
5. IMPACT EVENTS chemical reactions. Under these extreme conditions,
Reactive processes of asteroid and comet impacts on the cluster matter is subjected to a microshock wave
Earth involve planet–planetary body collisions with propagation within itself, which produces temperatures
impact velocities of tens of kilometres per second. For up to 4!104 K and pressures of 600 kbar within (Ar)n
example, the Shoemaker-Levy comet crashed into clusters (nZ141, 321, 555; Schek & Jortner 1996),
Jupiter on 22 July 1994 at a velocity of 60 km sK1 with the pressure–temperature Hugoniot curves for the
(www.jpl.nasa.gov/slg/). Such impact events on Earth clusters being qualitatively similar to those in the
generate high temperatures (104–105 K) and pressures corresponding bulk matter (Ross et al. 1986). These
(hundreds of kilobars), both in the terrestrial impact extreme pressure conditions result in an extreme
region and within the colliding planetary body. Three compression of the impacting cluster. For example,
classes of reactive processes are relevant in this context. I. Schek & J. Jortner (1999, unpublished results)
observed that the density of the (H2)n cluster can be
(i) Formation of impact craters. Asteroid and comet increased by a numerical factor of approximately 1.7
impact events constitute the extraterrestrial under pressures of 250 kbar and temperatures of 104 K
mechanism, which delivers a localized high- (figure 3). This increased density of the hydrogen
temperature and high-pressure pulse of energy cluster is still too low to produce metallic hydrogen.
into the target, resulting in extreme local However, there is a distinct possibility that, in other
structural and ecological changes (Cockell & molecular clusters, an impact-induced extreme com-
Lee 2002). Impact craters could serve as pression will produce a metallic phase. In such
possible sites for prebiotic chemistry (Cockell transient metallic clusters, plasma produced by the
2006). high-temperature impact may be operative in relevant
(ii) Local chemical effects in the impact region. An molecular syntheses (Managadze et al. 2003).
impactor can create a local environment con- High-energy cluster–wall collisions containing pre-
ductive to the synthesis of reduced carbon biotic materials and simple biotic molecules will
compounds by the Fischer–Tropsch type provide an interesting hunting ground for the pro-
reaction (Mukhin et al. 1989; Chyba & Sagan duction of building blocks of biomolecules under
1992). Impact-induced shock heating of redu- extreme conditions.
cing gas mixtures in the early Earth’s atmos-
phere could result in the formation of amino
acids (Bar-Nun et al. 1970). 6. THE ORIGIN OF LIFE: BOTTOM-UP APPROACH
(iii) Hypervelocity impact phenomena within the The bottom-up approach (scheme 2) rests on the
impactor. The high-velocity (10–100 km sK1) sequential steps, which are as follows.
impact of asteroids or comets, which initially
contain prebiotic materials or building blocks (i) Molecular fabrication of the building blocks
of biomolecules, can result in the synthesis of biomolecules from simple prebiotic molecules
of amino acid oligomers (Bernstein 2006). It induced by external energy sources (Miller
was experimentally demonstrated that hyperve- 1953; Miller & Urey 1959; Mason 1992;
locity impacts can oligomerize amino acid Wills & Bada 2000). These building blocks of
monomers (Blank et al. 2001) and other large biomolecules are produced and dissolved in the
organic molecules (Miruma 1995; Managadze ‘primordial soup’ (Darwin 1871; Oparin 1924),
et al. 2003). Furthermore, organic compounds where all subsequent reactions occur.

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

 Conditions for the emergence of life J. Jortner 1883

Scheme 2.

(ii) Nanofabrication of biomolecules by catalysis control of information for production and replication
(Deamer 2006; Ferris 2006; Wächtershäuser and (iv) protection for survival via energy flow and
2006) and self-assembly (Eigen 1971, 1996; metabolism. Self-organization by design with the
Yates 1987; Lehn 2002a,b, 2003; Deamer control of structure (Eigen 1971, 1996; Lehn
2006). Some experimental progress towards 2002a,b, 2003; Heckl 2004; Deamer 2006) is pertinent
the formation of polypeptides and nucleic acid for issues (i) and (ii). Retrieval, transfer and processing
oligomers was made a long time ago (Oró 1961), of information at the supramolecular level (Eigen 1971,
but the synthesis of proteins and nucleic acids 1996; Lehn 2002a,b, 2003; Taylor 2006) pertain to
under these conditions remains a challenge issue (iii). Self-organization by selection (Eigen 1971,
(Chyba & McDonald 1995). 1996; Lehn 2002a,b, 2003) uses the response to
(iii) Formation of complex biological matter (with internal and external factors to achieve adaptation
our limited knowledge about these central (issues (iii) and (iv)).
processes, as discussed in §3). Reactivity and catalysis are crucial for the develop-
ment of chemical systems of structural and dynamic
A major chemical problem associated with the complexities (Eigen 1971, 1996; Lehn 2002a,b, 2003).
bottom-up approach pertains to the atmospheric con- The formation of ordered biomolecules has to transcend
ditions on the early Earth. The early atmosphere came to the picture of reactivity in a homogeneous solution. The
be viewed as rich in CO2 (Kasting & Catling 2003), rather role of catalysis in prebiotic synthesis of biopolymers was
than being hydrogen-rich and reducing, as originally addressed by Bernal (1949, 1951), who proposed that
assumed by Miller & Urey (1953, 1959). A drastic dissolved organic substances were concentrated by
reduction of the yield for the production of organic absorption on the surfaces of clay mineral particles
molecules in the CO2-rich, less reducing atmosphere was suspended in the early oceans, which acted as catalysts
observed (Stribling & Miller 1987; Bernstein 2006). An for the formation of biomolecules. The synthesis of long
alternative approach (Wächtershäuser 1988, 1990) prebiotic oligomers of both nucleotides and amino acids
rests on the relations between inorganic chemistry was accomplished on mineral surfaces, i.e. montmor-
and biochemistry in the reaction of CO2 in aqueous illonite for nucleotides, illite and hydroxylapatite for
solutions, e.g. amino acids (Ferris et al. 1996). Self-organization (self-
assembly) on mineral surfaces involves nanostructure
fabrication by one-step (or few steps) generation of
complex matter (Eigen 1971, 1996; Ferris 2002, 2006;
Lehn 2002a,b, 2003; Heckl 2004; Deamer 2006). Such
‘holistic’ (‘collective’) self-organization for the building
A heterogeneous surface catalysis on the pyrite of complex biological matter cannot be achieved by the
surface was proposed to result in a cellular metabolism sequential placing of individual molecules (or of
(Wächtershäuser 2006). In addition, a careful scrutiny building blocks of biomolecules) according to a fixed
of the inventory of organics from exogeneous sources design. Clay minerals of montmorillonite, which consist
(Chyba et al. 1990; Chyba & Sagan 1992; Thomas et al. of layered structures, act as catalysts for the formation of
1997; Chyba & Hand 2005; Bernstein 2006), which ordered RNA (Ferris 2002; Huang & Ferris 2003;
was discussed in §3, is required. Migakawa & Ferris 2003; Ferris 2006; Deamer 2006),
with a one-step synthesis of 35–40-mer RNA being
accomplished (Huang & Ferris 2003; Ferris 2006). Self-
7. SELF-ORGANIZATION AND CATALYSIS organization of complex biological matter can also
Major difficulties with the homogeneous primordial involve the assembly of boundary structures, i.e. fatty
soup theory pertain to the following issues (Chyba & acids and membranes, and the encapsulation of
Hand 2005): (i) the synthesis of big ordered nano- biologically active ensembles (Deamer 2006).
structures of biomolecules, (ii) cellular organization of A basic concept that has to be addressed in the
lipids, proteins and nucleotides in RNA, (iii) genetic context of clay-catalysed RNA formation pertains to

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

1884 J. Jortner Conditions for the emergence of life

Ar531I2 / Pt surface

v = 10 km s–1
Ek / N = 30 eV

t=0 t=175 f s

t = 247 f s t=578 f s

Figure 2. A microscopic physical analogue for impactor–target collisions is provided by high-energy cluster–wall collisions.
Reactive chemical dynamics in high-energy Ar nI2 cluster–wall collisions are portrayed. Snapshots of the collision of an Ar531I2
cluster at an initial velocity of 10 km sK1 (kinetic energy of 30 eV per particle) with a platinum surface, as obtained from
molecular dynamics simulations, are shown. The dissociation of I2 is manifested. Data were adopted from Schek et al. (1994).
High-energy wall collisions of clusters containing prebiotic material or biotic molecules can provide a unique chemical medium
for the shock-impact synthesis of building blocks of biomolecules or amino acid oligomers.

the selective catalysis, which maintains the required chain containing N amino acids with 20 distinct
sequence and regioselectivity of the oligomers (Ferris possibilities for each biological amino acid
2006). Selective catalysis accomplishes self-organiz- residue, the total number of structural isomers,
ation with the generation of supramolecular diversity, SIZ20N, is huge. Thus, for NZ200, SIZ10260!
giving access to an array of similar structures that Recent studies on the origin of life focused on
potentially exist (Lehn 2002a,b). These similar RNA as the most important polymer in the
structures correspond to quasispecies (Eigen 1988). early form of life (§9). The same difficulty in
On the other hand, specific catalysis is expected to the formation of a huge number of isomers has
give rise to a single species, not allowing for the been addressed in the prebiotic synthesis of
required diversity. RNA (Szostak & Ellington 1993; Joyce & Orgel
1999). An RNA of sufficient length to initiate a
8. THE ROLE OF HUGE NUMBERS high-fidelity catalysis and replication should
The prebiotic synthesis of proteins or nucleic acids contain about 40 monomer units. A minimal
requires the production of an ordered biopolymer. precondition for the origin of life is two such
Combinatory arguments reveal that the probability of RNAs catalysing the synthesis of each other.
the formation of compositionally and conformationally Random polymerization of two RNAs, each
ordered systems is negligibly small, in view of the containing 40 nucleotides, would result in 1048
existence of huge numbers of compositional/conforma- isomers, weighing 1028 g, which is comparable
tional isomers. These huge numbers of alternative, to the mass of the Earth ( Joyce & Orgel 1999).
redundant isomers or conformers constitute a major A possible resolution of this paradox of
problem in the description of the evolution of life on structural redundancy rests on the role of self-
Earth (Levinthal 1969; Joyce & Orgel 1999). Two organization by design and selection (Eigen
paradoxes of huge numbers are as follows. 1971, 1996; Lehn 2002a,b, 2003; Heckl 2004;
Ferris 2006; Deamer 2006), which may be
(i) The paradox of compositional redundancy (Crick driven by selective catalysis (Ferris 2006), as
1981; Joyce & Orgel 1999). For a polypeptide discussed in §7.

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

 Conditions for the emergence of life J. Jortner 1885

0.40 thermodynamics (Berry 1993; Fraunfelder &

Wolynes 1994; Wolynes et al. 1995).
0.36
d (gr/cc)

0.32 density From the foregoing discussion, indications emerge

0.28
regarding the central role of self-organization and
dynamics on energy landscapes in overcoming compo-
0.24 (H2)537 sitional and conformational redundancy in the pre-
0.20 biotic synthesis of proteins and nucleic acids.
240
P (kbar)

180 9. THE ORIGIN OF LIFE: TOP-DOWN APPROACH

120 pressure Self-organization, which plays a central role in the
construction of complex matter, supplements the
60 bottom-up molecular fabrication in terms of top-
0 down miniaturization (Lehn 2003). The top-down
9600 approach to the origin of life rests on two major aspects,
which are as follows.
7200
T (K)

4800 temperature (i) Deconstructuralism of a system to small units that still

exhibit biological functions. A great success of this
2400
approach pertains to the discovery that the RNA
molecule is capable of both catalytic activity and
0 2.0 4.0 6.0 8.0 10.0 information storage (Altman et al. 1989; Cech
initial velocity (km s–1) 1993). This provided a solution to the puzzle
Figure 3. Microscopic modelling of matter under extreme (Dyson 1985) whether proteins preceded DNA
conditions created by high-energy impactor–target collisions, or vice versa. In an ‘RNA world’, the RNA
portraying microshock wave propagation producing high molecule performs the dual function of both
temperatures and pressures in high-energy (H2)537 clusters present-day proteins that act as enzymes to
colliding at velocities of 1–10 km sK1 with a platinum wall catalyse reactions and DNA that acts to store
(I. Schek & J. Jortner 1999, unpublished results). High molecular information (Crick 1968; Orgel 1968,
densities (up to a numerical factor of 1.7 of the normal 1988a,b, 2000; Orgel & Lohrman 1974; Cech
density), high temperatures (up to 104 K) and high pressures et al. 1981; Gilbert 1986; Joyce & Orgel 1999;
(up to 250 kbar) are generated, providing a unique medium Taylor 2006). A major problem in this attractive
for the production of building blocks of biomolecules under
picture is that the prebiotic origin of RNA
extreme conditions.
remains mysterious (Shapiro 1988; Chyba &
(ii) The paradox of conformational redundancy McDonald 1995; James & Ellington 1995).
(Levinthal 1969). Protein folding describes the (ii) Mapping the genetic relationship of life on Earth to
complex process in which polypeptide chains elucidate the properties of the last common ancestor
adopt their three-dimensional native confor- (Hutchison et al. 1999; Marshall 2002). At the
mation required for their biological function. level of the complete cell, efforts are now made to
Levinthal (1969) pointed out that for a protein strip down a genome to reveal the minimal set
made up of 100 amino acids, with three possible of genes required for cellular functionality
conformations for each amino acid residue, there (Hutchison et al. 1999; Marshall 2002).
are 3100 (approx. 1049) conformations for the
entire polypeptide chain. Even if the time required
to change from one configuration to another is 10. SOME OPEN QUESTIONS
only 10 ps, a random search through all the The foregoing discussion already reflected on the
conformation spaces will require 1036 s or 1029 ubiquity of open questions, starting from the current
years. The Levinthal (1969) paradox implies that absence of a scientific theory for the ‘definition of life’.
protein folding would take longer time than the We then alluded to many gaps in our understanding of
age of the universe! The Levinthal argument is the conditions and constraints for prebiotic chemistry.
based on the unphysical assumption that the Several open questions in this fascinating field that are
energy landscape (potential energy surface) of of considerable interest are as follows.
the protein corresponds to a ‘golf course’, being
totally flat with one hole for the native configu- (i) The origin of biomolecular chirality. This con-
ration (figure 4), and with all configurations of stitutes an important, extensively discussed and
equal probability (Zwanzig et al. 1992). In real life, controversial issue (Quack 2002, 2003). It
the energy landscape of a polypeptide or protein concerns a nearly exclusive selection of
(figure 4) is rugged with a very large number of L-amino acids and D-saccharides for terrestrial
minima, basins (‘valleys’) and saddle points biopolymers. Parity violation of molecular and
(‘mountain ridges’). The system slides from the biomolecular chiralities is important; however,
initial configuration on the energy landscape to energy differences between chiral molecules
the global minimum. The energy landscapes of are small, being in the range of picojoules per
proteins govern both folding kinetics and mole (10K11–10K12 J moleK1; Quack 2002).

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

1886 J. Jortner Conditions for the emergence of life

(a) (b)

N N

Ala6 cyc-Ala6
(c) (d)
20
16
energy (kcal mol–1)

energy (kcal mol–1)

16
12 12

8 8
4 4 B
A C
0
–1.6 0
0 1 1
1.6 –2.8 – 0.4 –2.0 0 0
–1.2 –1 –1
q1 q2

Figure 4. Energy landscapes of complex systems. The energy landscapes of cyclic (alanine)6 polypeptides were obtained from
molecular dynamics simulations. These energy landscapes of (c) linear (Ala6) and (d) cyclic (cyc-Ala6) polypeptides portray the
potential energy surfaces in the two reduced coordinates obtained from the principal coordinate analysis (adopted from Levy
et al. 2002). The two potential energy surface models show the grossly oversimplified energy landscapes for (a) a golf course,
corresponding to the Levinthal picture, and (b) a funnel. Motion on the real energy landscape of a complex system overcomes
conformational redundancy, which is only inherent in the oversimplified model (a) for a golf course.

Fundamental hypotheses for the prebiotic antibiotics produced by bacteria (Lenler et al.
enantiomer enrichment involve the following: 1999). D-Glutamic acid is the prominent
(i) mechanisms driven by parity violation enantiomer incorporated into poly-g-glutamic
(Quack 2002), (ii) homochiral selection by acid in the capsules of Bacillus subtilis and some
photolysis with circularly polarized light other bacteria (Foster & Popham 2002). The
(Meierhenrich & Thiemann 2004) and (iii) ratio of D- and L-glutamic acid residues in poly-
stochastic and accidental mechanisms. The g-glutamic acid can vary, depending on the rate
latter rest on the suggestions for low-tempera- of the production of D-glutamic acid in the cell
ture phase transitions under the influence of (Ashiuchi et al. 1999). D-Alanine residues in the
parity violation (Salam 1991) or on a nonlinear bacterial cell wall of Staphyloccus aureus, a
kinetic scheme with a very small selective Gram-positive organism, are involved in anti-
advantage arising from parity violation (Chela- biotic resistance (Sieradzki & Torriasz 2006).
Flores 1991). Some interesting compound One of the best-studied peptide antibiotics,
mechanisms for the emergence of homochir- from the biosynthetic point of view, is gramici-
ality were proposed (Koch et al. 2002; Pizzar- din S, which contains D-phenylalanine (Lenler
ello & Weber 2004; Nanita & Cooks 2006). et al. 1999). Accordingly, D-glutamic acid,
These involve a sequential–parallel scheme of D-alanine, and D-phenylalanine exist in biologi-
chiral imbalance (presumably arising from cally active peptide chains of bacteria, making
parity violations (Quack 2002, 2003) or them resistant to proteolytic enzymes (Sieratzki
photolytic selection (Meierhenrich & Thie- & Torriasz 2006, Cui et al. 2006). At present,
mann 2004)), followed by chiral enrichment the experimental and theoretical basis for a
(presumably driven by chiral synthesis; Pizzar- proper mechanism of homochirality requires
ello & Weber 2004) and, subsequently, chirality further scrutiny and the problem is open.
transfer. One possible process for chirality (ii) The build-up hierarchy. The understanding of
transfer involves homochirality preference by bottom-up self-organization requires an experi-
an enantiometric substitution of individual mental control of molecular fabrication and
amino acids or sugars on (serine)8 HC ‘magic biomolecular non-fabrication in model systems.
number’ clusters (Julian et al. 2002; Nanita & In particular, the mechanistic facets of the
Cooks 2006). Not only is the homochirality ‘holistic’ (‘collective’) one-step (or few steps)
problem unsolved, but also it is intriguing to self-organization of the building blocks of
inquire whether primitive life was homochiral. biomolecules to form complex biomolecules
Notable, but rare, cases of the violation of have to be elucidated. Concurrently, the
homochirality in living matter involves the advancement of theoretical concepts, which
presence of D-amino acids in some bacteria can be subjected to experimental tests, is
(Foster & Popham 2002) and in some imperative.

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

 Conditions for the emergence of life J. Jortner 1887

(iii) The top-down approach to the origin of life. Some of estimates of tOL were inferred from geological
the important open questions are related to the and planetological evidences, which gave tOLZ
understanding of the prebiotic origin of RNA 3.5 Gyr, while stable isotope chemistry yielded
and the elucidation of the properties of the last tOLx3.8–3.9 Gyr. Thus, life appeared on the
common genetic ancestor. The latter issue can early Earth at the time-scale of tO–tOL
give rise to the first artificial genome (Hutchison x0.7–1.1 Gyr of its formation, according to the
et al. 1999; Marshall 2002), opening up avenues ‘central dogma’ underlying this discussion meet-
towards ‘artificial life’. ing. The time window DtZtEKtOL marks the
(iv) The organization and function of complex biological time-scale for the evolution of primitive life on the
matter. This constitutes one of the central ‘grand early Earth, which falls in the range
questions’ of modern science. For the sake of Dtx0.1–0.5 Gyr. This timing is important for
methodology, we follow Lehn (2003) adopting the qualitative assessment of the nature of the
a constructionalist approach, noting that the chemical processes that led to the formation of
organization of complex biological matter is complex biological material on the early Earth.
induced by electromagnetic forces. Molecular For Dtx0.1 Gyr, the formation of life was ‘easy’,
recognition, which is based on such interactions, while for Dtx0.5 Gyr, the formation of life was
provides a central cause for self-organization at ‘hard’ (Chyba & Hand 2005). The distinction
the molecular, supramolecular and nanostruc- between the ‘hard’ and the ‘easy’ formation of
tural level. The second, related but distinct, early life can be highlighted by the adaptation of
‘grand question’ addresses the cosmological the Carter formula (Carter 1983; Barrow &
organization of matter by gravitational forces Tiepler 1988) and its slight extension ( Jortner
(Lehn 2003). Some of the many fascinating 2006, unpublished results). Provided that the
open questions in the realm of complex biological onset of early life involved n improbable and
matter are as follows. (i) What are the mechanistic independent steps, then Dt/tEZ bn/(bn+1), and
aspects of information-driven self-organization? tOL/tEZ1/(bn+1), where b (b/1) is a dynamic
(ii) What is the nature of the ‘transition’ from time-stretching parameter ( Jortner 2006, unpub-
programmed and instructed systems to learning
lished results). ‘Short’ time windows, e.g.,
(and thinking) systems? (iii) What are the
Dtx0.1 Gyr with tOL/tEx0.98 imply that nb
complementary roles of bottom-up construction
and n are negligibly small (manifesting the
and top-down miniaturization? (iv) At what level
‘easy way’), while ‘long’ time windows, e.g.,
of molecular–supramolecular–nanostructural
Dtx0.5 Gyr with tOL/tEZ0.88 imply that
complexities does biological function set in?
nbx0.12, so that nx1–2 (manifesting the
Perhaps, the most important issue is the complete,
‘hard way’).
unambiguous functional characterization of
complex biological matter. The fascinating scientific work reported at this
(v) Time-scales for the origin of life. The characteristic
discussion meeting reflects on the quest for front-line
time, tOL , for the onset of the origin of life on
solid experimental evidence and theoretical under-
Earth (an incompletely defined, but useful
standing, which will provide the conceptual basis for
concept) must be shorter than two times: the
the understanding of the emergence of life on the
time tOx4.6 Gyr for the formation of Earth by
early Earth.
terrestrial accretion (Chyba & Hand 2005;
Lunine 2006) and the time tEx4.0 Gyr for the I am most grateful to Dr Sydney Leach for his perceptive
onset of the appropriate geological, environ- comments and sage advice. I am indebted to Professors Max
mental and chemical conditions that enable the Bernstein, Charles Cockell and James Ferris for their
emergence of life. tE is determined by (at least) enlightening correspondence, and to Professor Alex Keynan
for enlightening information. The support of my research by
three times (that are given relative to the time
the Zelman Weinberg Foundation at Tel-Aviv University is
for the formation of the earth): (i) t1x0.1Gyr for gratefully acknowledged.
the solidification of the magma ocean to form the
crust (Solomatov 2000); (ii) t2x0.5 Gyr for the
termination of the heavy impact bombardment
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