The PAH World

Discotic polynuclear aromatic compounds as a mesophase scaffolding at the origin of life

S. N. Platts

"... 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.
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