Full text of DOI:10.1089/153110702762027826

ASTROBIOLOGY
Volume 2, Number 3, 2002
© Mary Ann Liebert, Inc.
Life Before RNA
STEPHEN J. SOWERBY1 and GEORGE B. PETERSEN2
ABSTRACT
The hypothesis that life originated and evolved from linear informational molecules capable
of facilitating their own catalytic replication is deeply entrenched. However, widespread ac-
ceptance of this paradigm seems oblivious to a lack of direct experimental support. Here, we
outline the fundamental objections to the de novo appearance of linear, self-replicating poly-
mers and examine an alternative hypothesis of template-directed coding of peptide catalysts
by adsorbed purine bases. The bases (which encode biological information in modern nu-
cleic acids) spontaneously self-organize into two-dimensional molecular solids adsorbed to
the uncharged surfaces of crystalline minerals; their molecular arrangement is specified by
hydrogen bonding rules between adjacentmolecules and can possess the aperiodic complexity
to encode putative protobiological information. The persistence of such information through
self-reproduction, together with the capacity of adsorbed bases to exhibit enantiomorphism
and effect amino acid discrimination, would seem to provide the necessary machinery for a
primitive genetic coding mechanism. Key Words: RNA—Life—Information—Self-replica-
Astrobiology 2, 231–239.
tion—Self-organization.
resulting polypeptide chains fold into complex
three-dimensional solids with the capacity to cat-
alyze specific chemical reactions.
INTRODUCTION
LUCIDATION OF ITS DOUBLE-HELICAL STRUCTURE
supported the identification of DNA as the
E
In modern cells, the transfer of information
postulated “aperiodic solid” of information-bear- from DNA to protein is mediated by RNA mole-
ing chromosomes (Schrödinger, 1944) and pro-
vided a mechanism for the molecular basis of
heredity (Watson and Crick, 1953a,b). Informa-
tion in nucleic acids is conveyed by a linear, ir-
regular sequence of nucleotides that encodes the
construction of protein catalysts essential for life.
The nucleotides specify the linear sequences
cules. However, in addition to encoding protein
sequences, RNA also plays a catalytic role in the
formation of the peptide bond (Khaitovich
et al.,
1999). Other naked RNA sequences exhibit lim-
ited catalytic activity on a variety of cellular sub-
strates (Yarus, 1999), and, in the laboratory, RNA
catalysis has been engineered by rounds of
in vitro
of L- -amino acids (Crick, 1958), whose linear
arrangement is the primary determinant of pro-
a
mutation, amplification, and selection—a process
of forced Darwinian evolution (Beaudry and
tein structure and function (Anfinson, 1973). The Joyce, 1992). Such techniques could ultimately
peptide bond, the chemical linkage between yield artificial self-replicating polymers (Johnston
amino acid residues, is formed in a dehydration
reaction between the ammonium and carboxylate
moieties of adjacent amino acid molecules. The
2001). The capacity for RNA sequences to
convey information (genotype), catalyze chemi-
cal reactions (phenotype), and undergo Darwin-
et al.,
1Global Technologies (NZ) Ltd., Dunedin, New Zealand.
2Department of Biochemistry, University of Otago, Dunedin, New Zealand.
231

232
SOWERBY AND PETERSEN
eral species (Winter and Zubay, 1995; Cohn
et al.,
2001a,c). Such adsorption
ian evolution lends support to the idea that the
very first forms of chemical “life” were naked
RNA molecules capable of facilitating their own
replication and evolution (Gilbert, 1986).
The prebiotic appearance of the purine coding
bases of RNA, adenine and guanine, seems
straightforward. Simulation experiments of the
chemistry of the primitive Earth (Miller, 1987) and
the atmosphere of the Jovian moon Europa (Levy
2001; Sowerby
et al.,
could have protected them from hydrolytic attack
within the prebiotic environment, but would also
have removed them from the aqueous phase and
prevented them from participating in chemical
processes leading to polymers or their mono-
meric building blocks.
Quite apart from their fundamental chemical
difficulties, the origin of informational, self-
replicating polymers also suffers from an in-
formational paradox—the origin of the first such
molecules (Cairns-Smith, 1982; Yockey, 1992;
Shapiro, 2000). The odds are stacked against the
2000) and analyses of organic material re-
et al.,
covered from carbonaceous chondrites (Cronin,
1998) yield various mixtures of amino acids and
some of the purine bases of RNA. These products
are strongly indicative of hydrogen cyanide–based
random, appearance of exceptionally rare
chemistry as the
source of primordial organic
de novo
first
species (Ferris and Hagan, 1984; Ferris, 1992; Mi-
nard 1998).
polymer sequences, and that begs for a deter-
ministic rather than stochastic origin. Such con-
siderations inevitably force us to consider the
possibility that life arose from simpler processes
that did not rely on the primary involvement of
linear, self-replicating molecules.
et al.,
The chemical problems with the
pre-
de novo
biotic appearance of RNA center predominantly
on difficulties with the prebiotic origin of the
sugar–phosphate scaffold (Schwartz and de Graaf,
1993) that forms the pseudocrystalline backbone
of the linear polymer. A prebiotic route to the
sugar is not trivial because carbohydrates are
born of chemistry incompatible with the cyanide
GENETIC TAKEOVER
Chemical and cellular life can be regarded as
distinct because the properties of living systems
are not necessarily limited to those systems en-
capsulated by a cellular membrane (Langton,
1989) and a certain level of chemical evolution
may have occurred before the development of a
cellular apparatus (Oparin, 1957). The “double-
origin” hypothesis of Dyson (1985) envisages the
spontaneous origin of a protein-catalyzed metab-
olism capable of self-reproduction. By-products
route to the bases (Arrhenius
1994). At the
et al.,
same time, the laboratory synthesis of linear RNA
polymers on the surfaces of clay catalysts from
artificially activated mononucleotide precursors
(Ferris and Ertem, 1992) obscures the real-world
problems of premature chain termination
(Shapiro, 2000) and enantiomeric cross-inhibition
(Joyce
1987). This has led to the suggestion
et al.,
that RNA was preceded by informational poly-
mers with simpler chemical backbones that did
not contain the ribose sugar moieties but still pos-
sessed the functional coding elements, the purine
of the metabolism enabled a
origin, giving
second
rise to replicating RNA that parasitized the
metabolism. This scenario is chemically less de-
and pyrimidine bases (Joyce
1987; Nelson
et al.,
2000). This scenario is appealing because of
manding than a
RNA world because the
de novo
et al.,
problems with RNA synthesis and replication can
be overcome by utilizing the machinery of the
metabolism. Dyson likened this to a bacterio-
phage utilizing the host biochemistry of a bac-
terium to complete the replication part of its life
the way that nucleic acids transmit their genetic
information from one generation to the next. The
hydrogen bond pairing of complementary bases
provides a mechanism for a linear, connected,
evolutionary hierarchy of polymer sequences.
For the polymer hypotheses, the chemical dif-
ficulties of polymerization are further compli-
cated by the susceptibility of the RNA bases to
aqueous-phase hydrolysis (Shapiro, 1995, 1999;
Levy and Miller, 1998), a process accelerated at
elevated temperatures (Levy and Miller, 1998).
Prevailing conditions could have alleviated this
problem, since the bases are known to adsorb
spontaneously to the surfaces of uncharged min-
cycle. The difference between
self-reproduction
is made distinct. Self-replica-
and
self-replication
tion implies direct copying from a parent struc-
ture. Self-reproduction, on the other hand, does
not require heredity in the first instance, but such
a system can nevertheless seed subsequent gen-
erations.
Cairns-Smith (1982) argued for a prevital, naked
genetic element, G1, that somehow influenced its

233
LIFE BEFORE RNA
environment to ensure its perpetuation. The mag- modern nucleic acids were established within the
nitude of such an influence would not be impor- framework of a G1-encoded “metabolism” and
tant, but any manifestation of environmental gradually developed the ability for coding and
change would, in essence, be the phenotype of translation until they dominated the nature of the
G1, which, in addition to tipping the scales in fa- metabolism: G1 was usurped and eventually re-
vor of perpetuating G1, would provide an envi- placed by the nucleic acid genetic elements (G2).
ronment conducive to organic chemistry. Cairns- This was the essence of “genetic takeover.”
Smith (1982) suggested that the adsorptive and
Genetic takeover is a process that might have
catalytic properties of clays could have been the involved a number of different genetic materials.
instruments of chemical change and that the ape- No linear connected hierarchy of genetic archi-
riodic arrangement of defect structure in their tectures needs to have existed, and subsequent
crystalline solid phase could have provided the genetic architectures would not necessarily bear
architecture for replicative information process- any resemblance to their predecessors. In this sit-
ing.
uation, it would be impossible to deal with the
Although their scenarios are superficially dif- technicalities of the origin of RNA in the absence
ferent, Dyson (1985) and Cairns-Smith (1982) con- of the chemical platform from which it
cur: A prenucleic acid organic chemistry on the originated.
directly
primitive Earth provided the metabolic architec-
If such a scenario is to be contemplated, the
ture of catalysts for the subsequent synthesis of first problem, it seems, would be to demonstrate
informational nucleic acids, which may have the feasibility of some persistent, non-nucleic
originally played a role in catalysis and, also, acid, G1, that has the ability to store information,
have been used for purposes other than the stor- evolve, confer phenotypic advantage on itself,
age of genetic information. The distinction be- and, at the same time, specify complex organic
tween these two scenarios is that, in Dyson’s chemistry. Only then would the chemical archi-
proposition, the formation of such a catalytic me- tecture become sufficiently complex to lead to
tabolism was spontaneous—it was
preceded secondary genetic system(s) (G2) from which nu-
not
by an informational architecture, as required by cleic acids could ultimately be derived.
Cairns-Smith’s proposal.
It is technically challenging to see how Dyson’s
“metabolism” dependent upon protein catalysts
could arise spontaneously and then evolve inde-
pendently of an informational architecture. Non-
biological amino acid polymerization can be
achieved by dehydration on the surfaces of inor-
ganic solids (Brack, 1993; Lahav, 1994; Rode,
1999), and the selective adsorption of chiral
amino acid enantiomers has been demonstrated
NONPOLYMER INFORMATIONAL
CHEMISTRY
Living systems exist in the solid regime in the
vicinity of an order–chaos phase boundary
(Kauffman, 1993). Nonlinear dynamic systems
demonstrate complex behavior, adaptability, and
computation in this transition region. Biochemi-
cally, such a boundary exists between the chaotic
chemical milieu of the cell and the ordered solid
of cellular structures. Molecules held rigid by co-
valent and noncovalent interactions form a solid
phase. Free-moving particles distributed within
the aqueous matrix are in the liquid phase. These
definitions are, however, blurred at the cellular
level. Cytoplasmic molecules are clearly dis-
solved, but the positions of their atomic building
blocks are fixed relative to one another, and so
they represent the germ of a solid phase (Schrö-
dinger, 1944). By this reasoning, one might regard
a complex protein molecule as a solid, whereas
its molecular building block precursors, the
amino acids, are able to move freely with respect
to one another and are fluid. This subtle differ-
on chiral inorganic crystal faces (Hazen
et al.,
2001). However, abiotic peptides have not gener-
ally been favored as prebiotic catalysts because
noncoded polymerizations have to overcome as-
tronomical odds to generate the specific amino
acid sequences of biological proteins (Yockey,
1992). Furthermore, the formation of homochiral
catalysts would require a symmetry break (Aveti-
sov and Goldanskii, 1993), and the presence of in-
terfering organic compounds (such as carboxylic
acids and amines) would cause premature chain
termination (Shapiro, 2000).
According to Cairns-Smith (1982), prevital ge-
netic information
have been a prerequisite
must
for evolution because
information can per-
only
information can evolve. In his view,
sist and
only

234
SOWERBY AND PETERSEN
ence means that individual molecular species damental interactions of bases with mineral
such as amino acids can serve as diffusible inter- solids are an inescapable consequence of their
mediates in chemical metabolism but become prebiotic appearance in the geochemistry of the
chemically redefined within the context of macro- early Earth. Furthermore, we have developed a
molecules.
During nucleic acid replication and protein teractions had a critical role in the origin of life
synthesis, a phase transition occurs as chaotic- (Sowerby 1996, 2000, 2001b). In our elabo-
plausible hypothesis that such fluid–mineral in-
et al.,
phase monomers are selectively solidified into ration of genetic takeover, the prevital genetic el-
new polymeric solids. Such processes all but ement, G1, is composed of the bases of nucleic
eliminate the stochastic nature of chemical reac- acids, which form aperiodic, tessellated patterns
tions because, at nucleic acid and protein sur- on the surfaces of crystals. The “genotype” re-
faces, liquid-phase molecules cross a fluid–solid sides in their information-bearing arrangements,
phase boundary and lose rotational and transla- which obey strict interaction rules and so are of
tional degrees of freedom. Upon adsorption, ki- deterministic origin; “phenotype” is manifested
netic pathways are made available to otherwise in the form of prebiotic proteins synthesized on
unfavorable chemical reactions by facilitating ap- this primitive coding template of adsorbed bases.
propriate collisions between surface-adsorbed It is our hypothesis that these
encoded protein sys-
had the capacity to evolve and so ultimately
species. If life is poised at the edge of chaos, it
tems
seems reasonable to suggest that life also origi- provide the chemical platform from which mod-
nated there (Kauffman, 1993). If life is maintained ern nucleic acids and protein translation origi-
and perpetuated at a solid–liquid interface, it is nated.
logical to focus investigation of the origins of life
at such a phase boundary.
The idea that a complex, encoded pre-RNA
chemistry existed on the prebiotic Earth is radi-
In the geochemical environment of the early cal, but rests on solid experimental evidence:
Earth, the mineral–water interface would have
been the dominant order–chaos phase boundary.
Minerals have long been invoked in models for
the origin of life (Bernal, 1951) and can provide
1. Simulation of the chemistry of the early Earth
and extraterrestrial environments reveals that
purine and pyrimidine bases and amino acids
are contemporary products of nonbiological
surfaces for physical adsorption (Sowerby
et al.,
1998; Smith, 1998), discrimi-
1996; Parsons
et al.,
nation of chiral enantiomers (Hazen
cyanochemistry (Miller, 1987; Minard
et al.,
2000) and indicates a non-
2001),
et al.,
1998; Levy
et al.,
and catalytic polymerization of amino acids
(Brack, 1993; Lahav, 1994; Rode, 1999) and nu-
cleotides (Ferris and Ertem, 1992). Minerals can
set the redox state of geochemical environments
(Shock, 1990) and provide the reducing energy
for the construction of biological precursors such
contrived, putative availability of the relevant
compounds.
2. The affinity of the bases for the surfaces of un-
charged inorganic solids (Winter and Zubay,
1995; Cohn
2001; Sowerby
2001a)
et al.,
et al.,
withdraws the bases from solution so that they
are protected from hydrolysis. While such
adsorption means that the free bases could
not have participated in any aqueous-phase
process leading to RNA, we postulate that this
phenomenon could have been a primary pre-
requisite for the construction of G1. The bases
are planar molecules that can tessellate a sur-
face in two dimensions to give arrays that are
stabilized by van der Waals interactions with
the underlying surface and by hydrogen
bonds formed between adjacent molecules, a
configuration originally postulated on the ba-
sis of thermodynamic measurements made at
as amino acids (Hennet
1992) and the es-
et al.,
tablishment of pH gradients (Russell and Hall,
1997). Precipitated mineral particles can also pro-
vide vesicles for encapsulation (Russell and Hall,
1997).
A THEORY BASED ON EXPERIMENT
Scanning tunneling microscopy (Binnig
et
1982) is a powerful tool that we have used to
al.,
investigate putative protobiological structures
formed from the bases of nucleic acids adsorbed
the mercury–water interface (Saffarian
et al.,
to inorganic surfaces (Sowerby
1996, 1998b,
et al.,
1987). The hydrogen bond interactions be-
tween the bases are drawn from a large reper-
2000, 2001b; Sowerby and Petersen, 1997). Our re-
sults have led us to the conclusion that the fun-

235
LIFE BEFORE RNA
toire of possibilities, including those of Wat-
son–Crick pairing found in nucleic acids, and
1993; Lahav, 1994; Rode, 1999) under plausi-
ble prebiotic conditions.
the monolayers are constructed using physico- 5. Prebiotic chemistry, it seems, will have pro-
chemical and geometric rules governing local
interactions (Sowerby 2000). Electro-
duced mixtures of both left- and right-handed
versions of the amino acids; a symmetry break
is required to separate one structural isomer
from the other (Avetisov and Goldanskii,
1993). On certain minerals, the monolayers are
enantiomorphic even though they are com-
et al.,
chemical measurements show that maximal
adsorption of the bases occurs at the potential
of zero charge (Vetterl, 1966). The proposed
mechanism of monolayer formation relies on
the spatial restriction of solvent at the un-
charged interface, where hydrogen bonding
interactions between the bases are favored.
This is in contrast to the aqueous phase, where
the bases are surrounded by water molecules
posed of achiral molecules (Sowerby
et al.,
1996). The resulting symmetry break could be
related to the peculiar property of biological
systems to use only the L-enantiomer amino
acids.
and remain dissolved (de Levie and Wand- 6. While monolayers formed from pure solutions
lowski, 1994). The interaction of nucleic acid
bases with clays (Winter and Zubay, 1995) and
of bases are crystalline, those formed from
of adenine and uracil are
mixtures
(Sowerby
aperiodic
2000). Such co-adsorption has
et al.,
graphite (Sowerby
2001a) shows that
et al.,
purine bases are, quantitatively, significantly
more readily adsorbed than the pyrimidines
and that this adsorption shows a strong tem-
been confirmed electrochemically (Kirste and
Donner, 2001), but interpretation of the co-ad-
sorbates is not trivial. Aperiodicity is an es-
sential prerequisite to convey information
(Schrödinger, 1944; Cairns-Smith, 1982). In
an abstract way, the aperiodic monolayers re-
semble nucleic acids except that the pseu-
docrystalline, sugar–phosphate scaffold is
provided by a mineral crystal and the arrange-
ment of bases is in a two-dimensional matrix,
rather than a one-dimensional string. The
spontaneous self-assembly of such solids from
aqueous mixtures of nucleic acid bases evap-
orated on the surface of crystalline minerals
suggests the existence of an organic, nonpoly-
meric, informational architecture.
perature dependence (Sowerby
2001c).
et al.,
Although not all of the surfaces studied in
model experiments can be considered domi-
nant prebiotic materials, uncharged mineral
surfaces were present in prebiotic times and
would have facilitated the accretion of organic
matter. Relevant examples come from the min-
eral families, zeolites, feldspars, and silicas
(Smith, 1998). Bulk adsorption studies show
that the purine base, adenine, adsorbs to clays
(Winter and Zubay, 1995), pyrite (FeS2), quartz
(SiO2), pyrrhotite (FeS), magnetite (Fe3O4),
and forsterite (Mg2SiO4) (Cohn
2001).
et al.,
The geochemical prevalence of these minerals 7. Significantly, the bases can modulate, in a
in the Hadean ocean would have allowed
them to act as a sink for prebiotic purines. Re-
moval of the bases from the aqueous phase
would confer protection from hydrolysis, as
well as establishing a nonequilibrium thermo-
dynamic framework for increased base syn-
thesis.
base-specific way, the adsorption equilibria of
selected amino acids (Sowerby 2002). The
mapping between bases and amino acids is the
signature of a coding mechanism (Yockey,
1992) and suggests that the monolayers could
specify the arrangement of chiral amino acids
before evaporative peptide bond formation.
et al.,
3. The spacing of the proton acceptors in the base
arrays is consistent with peptide bond di-
In our hypothesis (Sowerby
2000), the
et al.,
mensions. Molecular modeling indicates that spatial arrangement of bases in an aperiodic ar-
amino acids can form hydrogen bonds with ray could function as a template. The amino acids
the proton acceptors in the monolayers and are are expected to be bound to the surface by hy-
in the correct spatial arrangement for subse- drogen bonds formed between a single H atom
quent peptide formation (Sowerby and Heckl, of the amino acid ammonium group and the H-
1998).
acceptors of the underlying bases. Molecular
4. Spontaneous formation of peptide bonds be- modeling indicates that the amino acid arrays
tween amino acids is facilitated by evapora- will probably be further stabilized by lateral hy-
tion on the surfaces of inorganic solids (Brack, drogen bonds between the carboxylate groups of

236
SOWERBY AND PETERSEN
the adsorbed amino acids and the ammonium nario, coding of amino acids and peptide bond
groups of their nearest neighbors (Sowerby and formation would occur as a one-step process.
Heckl, 1998). If
can occur through specific Polymerization would thus effect the “transla-
coding
interactions of the amino acids with the variable tion” of the two-dimensional information source
electronic surface formed by the adsorbed bases, represented by the underlying base matrix to a
the spatial arrangement of bases in the aperiodic series of one-dimensional products, and, since
structure would function as a template for dif- many peptide-forming events would occur si-
ferent patterns of amino acid adsorption.
multaneously, each two-dimensional template
The roles of the isostructural components of could conceivably encode a number of one-di-
the amino acids in promoting specificity of bind- mensional peptide strings. At the same time, such
ing to the base template is a key feature of this a geometric template would discriminate be-
proposal. Logically, these components (rather tween -amino acids and other interfering com-
a
than the R-groups)
participate in the prim- pounds such as carboxylic acids, because only -
must
a
itive “coding” mechanism, since only these in- amino acids would have the correct geometry for
teractions can lead to a favorable geometry for peptide bond formation.
peptide bond formation. There is clearly suffi-
The dominant base synthesized in putative
cient variation in the electronic configuration prebiotic chemistries is adenine, formed through
surrounding the ammonium and carboxylate the simple condensation of hydrogen cyanide
isostructural moieties to allow discrimination (Ferris and Hagan, 1984). The concentration of
among different amino acid species (Sowerby
adenine in the prebiotic ocean was low (estimated
et
2002). The geometry of the H-acceptors of the to have been of the order of 30 ), and a means
al.,
mM
base layers would mean that the carboxylate and to concentrate it may have been needed (Miller,
ammonium residues of the amino acids will be 1987). Adenine adsorbs strongly to inorganic
bound in-plane to the base surface in the correct solids such that the fluid–solid phase equilibrium
orientation for peptide synthesis (Sowerby and is far displaced to the solid phase (Cohn
et al.,
2001a,c). Oxidative deami-
Heckl, 1998), thus increasing the chances of fa- 2001; Sowerby
et al.,
vorable collisions. Dehydration is, of course, re- nation of the fluid-phase adenine would also give
quired to effect polymerization. Peptide bond rise to hypoxanthine (Shapiro, 1995), a purine
formation is not kinetically favored in liquid wa- base with similar adsorption characteristics to
ter and would be facilitated by evaporation on adenine (Sowerby
2001a) and with the ca-
et al.,
the base monolayer. In this context, the mono- pacity to form similar self-assembled monolayer
layer base “template” would effectively fill a structures (Sowerby 2002). Adsorbed
et al.,
role equivalent to that of the substrate binding adenine monolayer structures exclude water
site of an enzyme. (Sowerby 1998a) and, once adsorbed, would
et al.,
Rehydrated peptides would, however, be only be kinetically protected from hydrolytic decom-
weakly adsorbed to the surface because the for- position. Mineral surfaces would have been a sink
mation of water during peptide bond formation for prebiotically available purines and would
would remove the surface-bound H-atom of each have sequestered much of the aqueous-phase
amino acid that provided the primary mechanism yield. A corollary is that adsorption would have
for adsorption. The thermodynamic context of cy- pulled the chemical equilibrium in favor of
cles of dehydration and rehydration would thus purine synthesis, with a consequent higher yield
act as a mechanism for peptide/protein synthe- than might otherwise be expected. The purine
sis.
The linearity of peptides is a consequence of yield adenine, but to a much lesser extent (Levy
the polarized structure of amino acids, which can 2000). Like its deamination product, xan-
be linked only in a “head-to-tail” fashion. The thine, guanine can also form monolayers (Heckl
amino acids will form a two-dimensional layer 1991; Sowerby and Petersen, 1999). Chem-
base, guanine, is also synthesized in reactions that
et al.,
et al.,
whose composition is dictated by the base com- istry, it would seem, deems that prebiotically syn-
position of the two-dimensional base layer to thesized purine bases would be predominantly
which they are adsorbed, and peptide bond for- displaced to the surface of mineral solids, and one
mation would be able to take place in any direc- might picture that primordial monolayer compo-
tion on this planar surface. In the simplest sce- sition would be dominated by a mixture of ade-

237
LIFE BEFORE RNA
nine and hypoxanthine, punctuated by occasional interactions are important, because self-assembly
guanine and xanthine molecules. is a way of recruiting information that exists
Adenine and hypoxanthine have been, in fact, within the rules of the interactions. Such self-pro-
proposed as the coding elements of a primitive grammability (Rasmussen 1991) is evident
et al.,
two-base, purine-only coding system (Crick, in the self-assembly of crystals from atoms, ions,
1968). Both bases, when adsorbed to a graphite or molecules and the formation of micelles from
surface, modulate the adsorption equilibria of lipids, the latter being clearly relevant to the ori-
different amino acids—a process of coding gins of life (Deamer, 1997).
(Sowerby
2002)—and such a modulation
Phenotypic advantage conferred by the cat-
et al.,
phenomenon would be expected to take place alytic capacity of encoded peptide products that
on any inorganic solid. It has been proposed leads to a change in the composition of the mono-
that aperiodicity in crystalline inorganic mate- layer itself would effect an evolution of the in-
rials had an informational role in the origin of formation content. In the fluid phase, for exam-
life (Cairns-Smith, 1982). Aperiodicity is not, ple, such a peptide might catalyze the conversion
however, an inherent property of compounds of adenine to hypoxanthine, or
thus
vice versa,
formed by strong long-range electrostatic inter- changing the surface composition of newly as-
actions, because the possible atomic configura- sembled monolayer and, thus, the capacity of the
tions of ionic solids are energetically well structure to encode new compositions of pep-
separated. Molecular solids, however, are con- tides. The catalyzed synthesis of the other bases
structed from components that interact pre- would lead to a greater information-carrying ca-
dominantly by weak, short-range van der Waals pacity and the codes for new peptide catalysts.
and hydrogen bond interactions, and crystalline
In this way, the self-assembly of a G1-encoded
polymorphs are possible because different con- system capable of evolution could lead to a me-
figurations can exist with similar energies tabolism of encoded catalysts capable of complex
(Pertsin and Kitaigorodsky, 1987).
organic chemistry, which could ultimately lead to
But how could such a system allow for the per- a nucleic acid-based architecture.
sistence and evolution of information? A truly
This hypothesis is not unlike the crystal gene
aperiodic structure would never repeat; the abil- hypothesis of Cairns-Smith (1982), where aperi-
ity of the information to persist would reside in odicity in inorganic solids acts as the primordial
the substructure of the monolayers and the re- information source. A distinct difference, how-
currence of discrete motifs or patterns. Proteins ever, is the role of heredity in the propagation of
are not continuous but have discrete sizes. A pro- the crystal genes. In our model, heredity is not in-
tein-coding portion of monolayer template can be volved; information is held within the bases
considered as a motif within a larger aperiodic themselves. Self-reproduction is an inherent pro-
structure, in the same way as coding sequences perty of the monolayers and does not preclude,
of nucleic acids are only portions of the genome on the basis of probability, the likelihood of a sim-
of an organism. The fact that the tessellation of ilar system generating elsewhere in the cosmos
the mineral surface by the bases will reflect the where similar conditions prevail. Two attractive
specific structural rules that dictate interbase hy- features of this hypothesis are its strong experi-
drogen bond formation would limit the number mental basis and the fact that it is amenable to
of “permitted” base patterns that can be formed further testing by experiment.
from a mixture of bases. As a result, the primary
structures of the encoded peptides would not be
random, but would be expected to comprise a
limited number of motifs repeated in different
contexts, even though the entire aperiodicity may
ACKNOWLEDGMENTS
We gratefully acknowledge the theoretical and
never be duplicated or replicated. Spontaneous experimental contributions of our collaborators,
processes such as these circumvent the “chicken Wolfgang M. Heckl (Munich) and Nils G. Holm
and egg” problem of self-replication because no (Stockholm), in the development of the hypothe-
parent template is required.
rather ses presented in this paper. We are grateful to Sir
Reproduction
of monolayer structure would al- Roy McKenzie for his generous gift to support
than
replication
low persistence of information. The interparticle our research.

238
SOWERBY AND PETERSEN
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