The PAH World
Discotic polynuclear aromatic compounds
as a mesophase scaffolding at the origin of life
S. N. Platts
s.platts{*at*}gl.ciw.edu
"... le hasard ne favorise que les esprits préparés "
(chance only favors prepared minds) Louis Pasteur (1822-1895)
The 'PAH World' is a novel chemical structural model for the plausible
formation of oligomeric proto-informational templating materials on
the early Earth; presumably progenitors of the widely expected
RNA World in chemical evolution theory. The model is based on the
self-assembling discotic mesogenic behaviors of polynuclear aromatic
compounds, their photochemical edge-derivatizations, and the
selectivity of such stacked supramolecular 'aromatic core' scaffolds
for the edge-on binding and ~ 0.34 nm plane-parallel spacing of
essentially random collections of small prebiotic heterocycles, taken
up and concentrated directly from the presumed and surrounding 'dilute
primordial soup.' The constrained inter-base separation distance would
select for oligomerizing 'linkers' of fairly specific size, such as
small methanal oligomers, which would also be taken up from the
prebiotic chemical environment, condensing with the small heterocycles
and also with each other to form the flexible structural backbone of a
first generation of proto-informational oligomeric material,
stabilized against both hydrolytic and photolytic degradations by its
association with the parent discotic mesophase. A transient local pH
decrease (e.g.,volcanic SO2(aq.)) would disrupt the hydrogen bond
interactions anchoring the oligomer to the discotic scaffold, thereby
releasing segments or portions of oligomeric material to explore
intramolecular degrees of motional freedom out in solution, perhaps
folding back on themselves to match up fortuitous base residue
pairings via familiar Watson-Crick-like complementarities. Segments
rich in such chance complementarities would likely persist by virtue
of the combined cooperative strength deriving from (i.) the multiple
intramolecular hydrogen bond interactions between paired bases, and
(ii.) the attractive pi-pi stacking van der Waals interactions occurring
between neighboring and stacked basepairs. This combination of
interactions establishing the domains of essentially hydrophobic
quasi-discotic mesophases in the secondary and tertiary structures of
these oligomeric proto-informational materials; base mismatchings
within such domains naturally leading to point replacements selecting
to minimize conformational potential energies. The new 'PAH World'
model is pleasing to chemical intuition, and provides the first
satisfying structural answer to the problem of a likely origin for the
phenomenon of life.
The figures below provide the details for this model.
Figure 1
Diagram illustrating a stacked and self-assembled
mesophase-type arrangement of discotic polynuclear aromatic
molecules, in which the aromatic cores of these molecules have become
associated and the system has self-organized by virtue of the weak
inter-molecular van der Waals forces of attraction operating between
the ! molecular orbitals of nearest-neighbor PAHs; these weak nett
attractive forces often simply being termed !-! stacking interactions
. The stacked PAHs are disposed plane-parallel and are necessarily
separated by ca. 0.34 nm (cf. the 0.34 nm interplanar spacing seen in
the ideal crystal structure for mineral graphite, and the 0.34 nm
inter-basepair helical rise in the classic 1953 Watson-Crick
structural model for the B crystallographic form of DNA); this
inter-PAH distance essentially reflecting the characteristic size of
the 2pz atomic orbitals of the Period 2 atoms (i.e., mostly carbon,
and occasionally nitrogen) comprising the aromatic core skeleta of
these exogenous polynuclear aromatic compounds. Illustrated at right
are three stacked molecules of an exemplar discotic polynuclear
aromatic compound: hexa-peri-benzocoronene (C42H18 ,
hexabenzo[bc,ef,hi,kl,no,qr]coronene, HBC ). This particular PAH core
has been of some considerable interest in the recent optoelectronics
materials literature, where the field of discotics is advancing
rapidly at the present time.
Figure 2
Various exemplar edge structures for partially
derivatized PAH-type and/or graphene-type polynuclear aromatic
molecules. The edges are shown vertically down the righthand side of
each of the six PAH/graphene fragments illustrated, and hydroxy
functionalities have been added into the edge structures at random,
simply to be illustrative of photochemical and/or geohydrothermal
derivatizations at the edges of polynuclear aromatic species. Other
types of organic functionalization/derivatization (e.g., -COOH, =O)
are certainly possible, especially given the known productive richness
of organic photochemistry. The PAH/graphene edges shown are partially
hydroxylated and are thus also partially oxidized relative to the
parent aromatic hydrocarbons. There are clearly many more possible
polynuclear edge structures than those being shown here, and the
variety of conceivable edge structures is further increased by the
various chemical functionalities that are possible. All common edge
functions (e.g., hydroxyl, keto, carboxylic acid, etc.) can engage in
hydrogen bonding, and the planar dispositions of such functions around
the edges of individual PAHs arranged in stacked discotic arrays
offers immediate potential for the edge-on binding and ca. 0.34 nm
plane-parallel spacing of small sp2- hybridized heterocyclic
molecules, moving firmly towards the first physicochemically plausible
mechanism for the selection and concentration of prebiotic nucleobases
and other similar small molecules out of the long presumed dilute
prebiotic soup . The new PAH World structural model directly addresses
the long recognized dilution and selection problems inherent in all
dilute prebiotic soup models of the past, these problems having
hitherto constituted two of the major chemical stumbling-blocks in the
origins-of-life field during the now fifty-two years since Stanley
L. Miller s breakthrough discoveries in prebiotic chemistry.
Figure 3
This figure is purely diagrammatic and is simply meant to help convey
the essential features of the new PAH World model system. Three
prebiotic nucleobases are shown hydrogen bonded to hydroxy functions
in the edge structures of some derivatized and neighboring PAHtype
molecules, which are themselves disposed in a stacked and discotic
array. The exemplar polynuclear aromatic compound being envisaged here
is 1,3-dihydroxy hexa-peri-benzocoronene (C42H18O2 , 1,3-dihydroxy
hexabenzo[bc,ef,hi,kl,no,qr]coronene, HBC-1,3-diol ). The hydroxy
functionalities, and their 1,3 dispositions, are merely meant to be
illustrative of the general chemical principle of photochemical and/or
hydrothermal derivatization at the edges of PAH-type and graphene-type
molecules. The three nucleobases are being shown in their keto
tautomeric forms, so as to be consistent with the seemingly reasonable
assumption that prebiotic Hadean (i.e., > ca. 3.85 Ga) surface and
rain waters were probably acidulous. The keto tautomers bear the
pro-glycosidic purine and pyrimidine secondary amine nitrogens (i.e.,
the NH functions at N(9) and N(1), respectively) disposed outwards,
and thus chemically accessible to the surrounding solution. Two
unspecified prebiotic oligomers of formaldehyde, (HCHO)n , are shown
between neighboring heterocyclics, and it seems likely that the fairly
constrained interbase spacing would lead to the system selecting for
oligomerizing linkers which are themselves of similar size. The
derivatized PAH/graphene edge structures can now effectively be seen
to represent something of an electronic phase boundary between the
discotically arrayed aromatic cores of the PAHs and the presumed
surrounding aqueous media of Darwin s warm little pond . The
phenomenon of life might now be seen as deriving from what is
effectively a phase separation between the discotic aromatic cores of
the PAHs versus the surrounding aqueousbased phase. It seems probable
that the essentially regular (2pz) inter-basepair plane-parallel
spacing distance of ca. 0.34 nm was inherited by molecular biology as
a chemical memory of this unique mode of origin, and that this
structural molecular fossil has been conserved to us in the
essentially quasi-discotic mesophase regions of heterocyclic
nucleobase pairings in the secondary and higher order structures of
extant nucleic acids.
Figure 4
The pyrimidyl and imidazole NH functions of the three nucleobases are
now shown condensed via N-glycosidic-type covalent linkages to the
presumed (HCHO)n oligomers, and the formaldehyde oligomers are
themselves now shown having condensed together to produce an extended
oligomeric backbone for the primitive proto-informational molecular
material; albeit that this earliest backbone material is probably
likely to have been branched in structure, rather than
straightforwardly linear as depicted in the figure. At this stage, the
nucleobase residues remain hydrogen bonded to the stacked and
scaffolding array of functionalized PAH-type molecules, and the
co-operative effects of these multiple hydrogen bonds together with
the multiple !-! stacking interactions serves to stabilize and
maintain the proto-informational oligomeric material against both
hydrolytic and photolytic degradations during further growth. The
N-glycosidic-type covalent bonds are not drawn to scale in the figure,
and the methanalderived oligomeric backbone is simply indicated here
by a zigzag line.
Figure 5
Diagram showing the expected effect of a sudden decrease in ambient pH
causing disruption of the inter-molecular hydrogen bonding
interactions hitherto existing between sections of proto-informational
oligomeric material and the stack of discotic and derivatized PAHs. A
sudden decrease in local pH, such as would be caused by a volcanic
release of acidic gases (e.g., SO2(g) and CO2(g)), would lead to
significant degrees of protonation of the hydroxy, keto, and amino
functions both in the PAH/graphene edge structures and in the
heterocyclic bases, thus setting up strong Coulombic forces of
inter-molecular repulsion between the positive electric charges which
would be almost instantaneously resident on the oxygen and nitrogen
functionalities in the PAH/graphene edges and also in the
proto-informational oligomer s heterocyclic base residues. Sections of
primitive proto-informational oligomeric template material would thus
be released to explore conformational degrees of freedom out in
solution. The sections of oligomer might be either totally freed of
the PAH/graphene stack altogether, or might perhaps remain tethered to
the discotic stack at one or both ends via some sort of structural
branching/cross-linking. Once the pH catastrophe had passed, the
levels of protonation of the heterocyclic base functions would
decrease as the ambient pH returned to normal, and the sections of
newly released oligomer would then be free to fold back on themselves
to bring electrically neutral heterocyclic base residues into hydrogen
bonding proximities, perhaps to match up adventitious
Watson-Crick-like complementarities.
Figure 6
Two representations of a single section of newly released
proto-informational oligomeric material which, having become
dissociated from a stacked and scaffolding array of derivatized
polynuclear aromatic species, has been free to explore conformational
degrees of freedom out in solution. The ca. 0.34 nm inter-heterocyclic
base-residue plane-parallel separation constraint, structurally
inherited from the discotic derivatized PAH/graphene scaffold, would
be expected to readily favor the intra-molecular matching up (i.e.,
hydrogen bonded basepairing) of complementary small heterocyclic base
residues, as segments of protoinformational material came upon one
another in the essentially blind process of exploring their individual
available conformational parameter spaces. In the idealized and
simplified example being shown here, involving a single molecule of an
oligomer having an entirely linear (i.e, unbranched backbone) primary
structure, a single strand of nascent proto-informational oligomer is
shown having folded back upon itself, when it at once becomes
intuitively conceivable that fortuitous Watson-Crick-like basepaired
complementarities would be matched up. Further, that in the case of a
single oligomeric molecule folding back on itself to form a stem-loop
type secondary structural motif like that shown here, the backbone
chains of the presumed intramolecular proto-duplex-like structure
would thus be set to run anti-parallel, this being immediately
reminiscent of a crucial and recurring secondary structural feature of
extant nucleic acids, originating with the famous anti-parallel chain
backbones described by Watson & Crick in their classic 1953 double
helical structural solution for the B-form of DNA, and being very
evident in the higher-order structures of ribosomal RNA and transfer
RNA molecules. Having formed fortuitous Watson-Crick-like basepairs,
it is entirely physicochemically conceivable that the co-operative
reinforcing strengths of the multiple intra-molecular
inter-heterocyclic hydrogen bonds and inter-basepair !-! stacking
interactions would lead to the persistence of complementarity-rich
segments of proto-informational material. Such complementarity-rich
regions might themselves now usefully be considered as constituting
quasi-discotics and to be exhibiting a mesophase-like behavior, with
the nascent mesophase being stabilized against dissociation by virtue
of the presence of the localizing and reinforcing oligomeric
backbone. Given the seeming prebiotic implausibility of an
oligomerized sugar-phosphate backbone at such an early stage in
chemical evolution, it would seem that practically any prebiotically
plausible and flexible backbone material could have initially sufficed
towards fulfilling the primary requirement of stabilizing these
complementarity-rich regions of proto-informational quasidiscotic
mesophase material against dissociation and/or hydrolytic/photolytic
environmental degradation. The maintenance of the characteristic
ca. 0.34 nm inter-basepair spacing distance through geologic and
evolutionary time to the present day, together with the structural and
mechanistic chemistries of known ribozymic activity supporting an RNA
World scenario, would suggest that the sugar-phosphate backbones of
extant nucleic acids were selected for early in the history of life on
Earth, both towards stabilizing and securing these quasi-discotic
mesophase regions, and for the presumed chemical evolutionary
advantages accruing at the essentially blindly-stumbled-upon origin of
ribozyme-like chemical activities, extant examples of which crucially
involve both the ribose-residue and the phosphate-residue moieties of
the oligomeric backbone material itself in their ribozymic
activities. In further regard to the etiology (borrowing Albert
Eschenmoser s use of this term) of the oligomeric backbone, it would
seem reasonable that the configurational locking-in of stereochemical
chiral informational specificities at asymmetric carbon centers in the
earliest backbone materials could certainly have moved these early
systems towards minimizing the conformational potential energies of
these first segments of proto-informational oligomeric material; this
chiral lock in configurational parameter space presumably representing
the long-expected and contingent frozen accident of causation of
biological homochirality, and thus an early chance chemical
evolutionary step in the downstream direction of something more nearly
resembling a recognizable progenitor of the widely expected RNA World
milestone in origins-of-life science. The
conformational-potentialenergy- lowering selection for the
conservation of complementarity-rich regions of protoinformational
oligomeric materials may well be the single most important
physicochemical and etiological factor towards a narrowing down of the
informational possibilities in terms of the subset of small prebiotic
nitrogenous heterocycles from which was eventually to be derived the
biological genetic code of nucleobase residues for all life on Earth.
Figure 7
Two-dimensional representation of some possible secondary structures
for portions of nascent proto-informational oligomeric material newly
released from attachment to discotic polynuclear aromatic
functionalized PAH/graphene scaffolding, perhaps owing to a transient
decrease in the local pH resulting from a sudden volcanic release of
an acidic oxide (e.g., SO2(aq.)). The zigzag lines represent
oligomeric backbone material (e.g., (HCHO)n ); the short straight
lines represent individual prebiotic heterocyclic residues oriented
with their z-axes in the plane of the paper (i.e., individual base
residues are oriented edge-on to the viewer); and the longer straight
lines represent hydrogen bonded pairs of complementary base
residues. Note that the edge-on perspective has been maintained
throughout for simplicity and ease of illustration. Whereas the
previous figure (Fig. 6) showed the idealized case of a single
molecule of a linear proto-informational oligomer, here are shown
probably more likely examples of branched backbone primary oligomeric
structures, showing regions of both intra- and inter-molecular
interbase hydrogen bonding and !-! base stacking associations, in
which fortuitous Watson-Crick-like basepairs have matched-up owing to
chance complementarities of sequence. The essential planarity of the
various base pairings, combined with degrees of rotational freedom in
the backbone material itself, has led to the basepairs being able to
behave as quasi-discotic mesogens, with the consequent formation of
mesophase-like regions in which stabilizing !-! stacking van der Waals
interactions are able to operate at the ca. 3.4 Ĺngström
plane-parallel separation distances between neighboring and stacked
basepairs. At the present stage of the model s development,
formaldehyde (i.e., methanal, HCHO) oligomers appear to offer the
simplest prebiotically acceptable solution to the problem of the
likely original backbone materials, and the small variabilities in the
inter-residue spacings shown in the figure reflects variability in the
admissible sizes of the small linker molecules originally selected
from the prebiotic chemical environment during the formation of the
proto-informational oligomeric materials at the discotic scaffolds
(i.e., reflecting degrees of inter-discotic lateral and rotational
freedom in the supramolecular scaffolding structures). Branching and
cross-linking in the backbones seems likely in terms of the primary
structures of the oligomeric products being envisaged here, versus the
linear primary structures of ribozymic oligonucleotides called for in
the context of the widely regarded RNA World hypothesis. Further
development of the new PAH World model in the downstream direction of
something more strongly resembling the widely expected RNA World seems
to await a full etiological explanation of the structural, chemical,
and stereochemical reasons behind the chemical evolutionary selection
for the sugar-phosphate oligomeric backbones observed in extant
nucleic acids. The formation of quasi-discotic mesophase regions in
such secondary structures as are being shown in the figure would be
essentially independent of the precise chemical identities of the
basepaired small heterocycles, and this feature of the model
immediately suggests collections of essentially random sequence
starting points at the origin of an incipient and blind informational
potential and capacity.
Webpage Design: Chris McCarthy exoplanet{+}gmail{o}com