Clay Minerals and the Origin of Life

Chapter 10.4

Clay Minerals and the Origin of Life A. Brack Centre de biophysique mole´culaire, CNRS, Orle´ans cedex 2, France

Chapter Outline 10.4.1. Introduction 10.4.2. Clay Minerals as a Possible Genetic Material 10.4.3. Clay Minerals and the Origin of Biological One-Handedness 10.4.4. Clays as Prebiotic Catalysts

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10.4.5. Clay Minerals and the RNA World 10.4.6. Polypeptide Formation on Clay Minerals 10.4.7. Clay Minerals and the Formation of Vesicles 10.4.8. Conclusion References

512 515 517 518 518

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10.4.1 INTRODUCTION It is difficult to define the word ‘life’. One generally considers as living an open chemical system able, a minima, to transfer its molecular information via self-reproduction and also able to evolve. The concept of evolution implies that the system normally transfers its information fairly faithfully but makes a few random errors, leading potentially to a higher efficiency and a better adaptation to environmental stresses. Schematically, the premises of primitive life can be compared to parts of chemical assemblages. By chance, some parts self-assembled to generate assemblages capable of bringing other parts together to form identical assemblages. Sometimes, a minor error in the building generated more efficient assemblages, which became the dominant species. By analogy with contemporary life, it is generally believed that the parts were made of organic matter, that is, carbon skeletons flanked by H, O, N and S atoms. As parts of an open system, the constituents must have been able to diffuse at a reasonable rate. A solid-state life is generally discarded, the constituents Developments in Clay Science, Vol. 5A. http://dx.doi.org/10.1016/B978-0-08-098258-8.00016-X © 2013 Elsevier Ltd. All rights reserved.

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being unable to migrate and to be easily exchanged. A gaseous phase would allow fast diffusion of the parts, but the limited inventory of stable volatile organic molecules would constitute a severe handicap. Ocean (liquid) water offered the best environment for the diffusion and exchange of organic molecules. However, the diffusion within the oceans must have somehow been limited to allow the self-organization of the first living assemblages. The key role of clay minerals in the origin of life was first suggested by Bernal (1949). The advantageous features of clays according to Bernal were (i) their ordered arrangement, (ii) their large adsorption capacity, (iii) their shielding against sunlight UV, (iv) their ability to concentrate organic chemicals and (v) their ability to serve as polymerization templates. Clay minerals are formed by aqueous alteration of silicate minerals (see Chapter 3). As soon as liquid water became permanently present on the surface of the Earth, clay minerals accumulated and became dispersed in the water reservoir. Since the seminal hypothesis of Bernal, many prebiotic scenarios involving clays have been written and many prebiotic experiments have used clay minerals (Negron-Mendoza et al., 2010).

10.4.2 CLAY MINERALS AS A POSSIBLE GENETIC MATERIAL Scientists who had observed the crystallization of minerals initiated by the addition of seeds to a sursaturated solution were tempted to associate life with mineral crystals. Schneider (1977), for example, suggested that complex dislocation networks encountered in crystals can, in some cases, follow the criteria of living units and lead to a crystalline physiology. He also discussed the places of possible occurrence in nature of this kind of physiology, such as terrestrial and extraterrestrial rocks, interplanetary dust, white dwarfs and neutron stars. According to Cairns-Smith (1982), there is no compelling reason to necessarily relate the last common ancestor made of organic molecules with first life. Although the easy accessibility of numerous organic building blocks of life was demonstrated experimentally, the dominant use of these molecules in living organisms can be seen as a result of evolution rather than a prerequisite for its initiation. Cairns-Smith proposed that the first living systems, and the chemical evolution preceding it, could have been based on a chemistry different from that which we know. The structurally and functionally complex genetic system of modern life arose secondarily in a living organism using a less efficient primary system with a much higher probability of spontaneous assembly. As genetic candidates, Cairns-Smith advocated crystalline inorganic material presenting suitable properties such as the ability to store and replicate information in the form of defaults, dislocations and substitutions. Clay minerals such as kaolinite are particularly attractive because they crystallize at ambient temperatures from aqueous solutions of silicate rock weathering products. The following ‘genetic takeover’ scenario was proposed by Cairns-Smith for the mineral origin of life. Certain clay

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minerals having properties that favour their synthesis proliferated and their replication defects, likewise, became more common. In certain lines, the development of crude photochemical machinery favoured the synthesis of some non-clay species such as polyphosphates and small organic compounds. Natural selection favoured these lines of clay minerals since the organic compounds they produced catalyzed the clay mineral formation. Multiple-step pathways of high specificity including chiral stereoselection arose through specific adsorption, followed by the appearance of polymers of specified sequence, at first serving only structural roles. Base-paired polynucleotides replicated giving rise to a secondary and minor genetic material. This secondary material proved to be useful in the alignment of amino acids for polymerization. The ability to produce sequence-specified polypeptides and proteins was accompanied by the ability to produce specific enzymes. More efficient pathways of organic synthesis ensued, and, finally, the clay machinery was dispensed in favour of a polynucleotide-based replication–translation system. Although each step of the hypothetical sequence of events was developed in detail, the scenario was not supported by experimental facts. About the same period, Weiss (1981) at the Institute of Inorganic Chemistry in Munich published a paper that appeared, at the time, to provide experimental support to Cairns-Smith’s scenario. He selected and purified a ‘matrix’ montmorillonite (Mt) having an excess charge of 0.28 charges/(Si,Al)4O10. An aliquot of the clay mineral matrix was added to a breeding solution containing Naþ, Kþ, Mg2þ, Al3þ and Si(OH)4. The concentration of the breeding solution was such that homogeneous nucleation in the absence of matrix layers yielded Mt with isomorphous substitution of 0.42 charges/(Si,Al)4O10-unit (formula unit). The D1-daughter first generation Mt exhibited a charge density of 0.28 charges/formula unit. This D1-generation was then used as a matrix for the analogous synthesis of the D2-generation. Up to the 10th generation, the spread was low, the main products being clay minerals with a charge density of 0.28 charges/formula unit. From the 16th to the 18th generation, the number of errors increased rapidly. In the generation D20, almost no material with the original value of 0.28 charges per formula unit remained. Although a rapid decay in replication quality was observed at the 20th generation, the experiments demonstrated that clay minerals were capable of replicating. Unfortunately, this publication itself did not undergo replication. Several requests for experimental details were submitted to the author in order to duplicate these experiments. Since no satisfactory answers could be obtained, the claymediated replication cannot be considered as established. One aspect of the proposal by Cairns-Smith that imperfect crystals can transfer their imperfections from one crystal to another was investigated. Platy particles of potassium hydrogen phthalate riddled with dislocations were studied to ascertain whether parallel screw dislocations could serve as an information store. Evidence of screw dislocations was obtained from growth hillocks through differential interference contrast microscopy, atomic force

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microscopy and luminescence labelling of hillocks in conjunction with confocal laser scanning microscopy (Ballard et al., 2007). Other mineral surfaces were tested to understand how the exceedingly complicated molecules and connections, such as the protein biosynthesis via DNA and RNA required for living systems, could have evolved from chemical systems that lacked these molecules. The most promising avenue was opened up by Wa¨chtersha¨user (1988, 1998). According to this author, the starting material was simple inorganic molecules such as CO2, H2S and N2 in contact with the sulphur-containing surfaces of Fe, Ni and Co. The energy source required to reduce CO2 was provided by the oxidative formation of pyrite (FeS2) from troilite (FeS) and hydrogen sulphide. Pyrite has positive surface charges and bonds the products of CO2 reduction, giving rise to a two-dimensional reaction system, a ‘surface metabolism’ that, later on, included autocatalytic cycles. Experimental laboratory work has already demonstrated the first steps of this new hypothesis (Heinen and Lauwers, 1996; Huber and Wa¨chtersha¨user, 1997, 1998).

10.4.3 CLAY MINERALS AND THE ORIGIN OF BIOLOGICAL ONE-HANDEDNESS Common clay minerals such as kaolinite and Mt had no intrinsic chirality associated with their crystal structures and, thus, were not expected to develop stereoselective interactions with chiral prebiotic molecules. Nevertheless, both clays were claimed to exhibit asymmetric effects by several authors. Degens et al. (1970) reported that kaolinite catalyzed the stereoselective polymerization of L-aspartic acid eight times faster than the corresponding D-enantiomer. These claims were repeated by Jackson (1971) who reported further that kaolinite preferentially adsorbed L- rather than D-phenylalanine, the edge faces of kaolinite crystals being responsible for the stereoselective effects. Using a variety of analytical techniques, Bonner and Flores (1973) found no differences in the adsorption of L- versus D-phenylalanine on kaolinite. In Bonner’s experiments, kaolinite also failed to promote the asymmetric polymerization of aspartic acid (Flores and Bonner, 1974; Bonner and Flores, 1975). Bondy and Harrington (1979) used radio-labelled biological compounds to highlight a possible stereoselective adsorption capacity of Mt. They incubated very dilute 108 M solutions of D- and L-enantiomers of 3H-leucine, aspartic acid and glucose with small quantities of Mt. They claimed that the natural L-enantiomers were bound about 10 times more effectively than the mirror images and suggested that primordial clay minerals might have been responsible for the prebiotic selection of L-amino acids and D-sugars. In experiments carefully designed to eliminate artefacts, Youatt and Brown (1981) showed that there was no stereoselective binding of L-amino acids by the clay mineral, the results published by Bondy and Harrington being attributed to the adsorption of the decomposition products of the radioactive substrates. Friebele et al. (1981) similarly failed to observe

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stereoselective adsorption when they exposed several racemic amino acids in sodium Mt dispersions at pH 3, 7 and 10. Siffert and Naidja (1992) observed a stereoselectivity of Mt in the adsorption and deamination of aspartic and glutamic acids. L-Glutamic acid and D-aspartic acid were found to be more adsorbed than the enantiomeric or the racemic forms. As for deamination, the amounts of ammonia released from the L-enantiomers of glutamic and aspartic acids were clearly higher than those obtained from the D- or racemic forms. These results were somehow contradictory. To confirm the data, it would be helpful to repeat the experiments with synthetic clay minerals devoid of any biological organic contaminants or imprints. It was recently reported that an allophane sample from New Zealand showed a clear preference for L-alanyl-L-alanine over the D-enantiomer. The size, intra-molecular charge separation and surface orientation of L-alanyl-Lalanine were suggested to confer a ‘structural chirality’ to the complex. The allophane sample was extracted from a 150,000-year-old weathered volcanic ash bed. Although the clay was carefully purified before use, some original organic contamination and/or imprinting could not be ruled out. Here again, synthetic allophane devoid of any organic contaminant or imprint still needs to be prepared with varied Al/Si ratios in order to check further and quantify the enantiomeric preference (Hashizume et al., 2002). By means of a self-consistent field method, Julg (1988) calculated that two identified enantiomeric forms of kaolinite exhibit different energies owing to the weak nuclear interactions. The kaolinite form whose trihedron (vectors a, b, c) is direct is more stable and should, consequently, be more abundant in nature. He then calculated that the adsorption energy of L-amino acids on the preferred kaolinite structure was larger than that of the D-forms by 0.14 and 0.04 kJ mol1 for the positively charged amino acid and the zwitterion, respectively (Julg et al., 1989). Julg also calculated that the addition of cyanide ions to ethyliminium cations adsorbed on the preferred enantiomeric form of a kaolinite crystal could lead to an excess of L-alanine at the expense of the D-form by 0.36 kcal/mol (Julg, 1987). Consequently, Julg advocated that kaolinite could have been one of the causes of the L-homochirality of the protein amino acids. Nevertheless, quoting Bonner (1991): ‘it should be emphasized that none of Julg’s speculations and conjectures is supported by a single shred of experimental evidence’. It must be noted that the stimulating hypotheses of Cairns-Smith (1982) emphasizing the role of clays in the origin of life did not account for the crucial one-handedness of biopolymers required, ensuring the survival of selfreplicating organic systems (Avetisov et al., 1991). Obviously, the possibility that clays can discriminate between optical isomers of amino acids attracted a great deal of interest and hope, but it generated, at the same time, a lot of controversies. The results in the case of clay minerals coated with chiral adducts such as phenanthroline tris-chelated

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nickel (Yamagishi, 1985) are not questionable. For non-coated clay minerals, there is always a serious risk of biological contamination or imprinting by bacteria or biofilms. Even if the purification is carried out to the extreme, biological imprinting of the clay mineral during its geochemical formation is still possible. Repeating the experiments with synthetic clay minerals appears to be the best way to legitimize the data.

10.4.4 CLAYS AS PREBIOTIC CATALYSTS By analogy with contemporary living systems, it is often considered that primitive life emerged as a cellular species requiring boundary molecules able to isolate the system from the aqueous environment (membrane). Also needed would have been catalytic molecules to provide the basic chemical work of the cell (enzymes) and information-retaining molecules that allowed the storage and transfer of the information needed for replication (nucleic acids). Formally, the synthesis of polymers of nucleotides and amino acids appears simple. The condensation reaction consists in eliminating water molecules between monomer units, thus linking them together. However, the formation of either proteins or nucleic acids from their monomers in water is not energetically favoured. For example, the peptide bond of proteins is thermodynamically unstable in water. Thus, energy is required to link two amino acids together in an aqueous milieu. For example, the free energy needed for two amino acids to form the dipeptide in water is about 4 kcal/mol at 37  C and pH 7. The equilibrium constant of the reaction is only about 103, and the equilibrium concentration of the dipeptide in 1 M solutions of the free amino acids is only slightly above 103 M. The thermodynamic barrier is very large for the formation of a long-chain polypeptide. Dixon and Webb (1958) pointed out that 1 M solutions in each of the 20 proteinaceous amino acids would yield at equilibrium a 1099 M concentration for a protein of 12,000 molar mass. The volume of this solution would have to be 1050 times the volume of the earth to yield one molecule of protein at equilibrium. Thus, an energy input such as heat or chemical activation was necessary to yield nucleic acids and polypeptides on the primitive earth. Polymers can be prepared in the presence of water if condensing agents are added or if activating groups are bound to the reacting monomers to provide the requisite free energy for bond formation. In both cases, it is important to limit the competing hydrolysis of the activating groups. Polymer formation on clay minerals is a solution to this problem.

10.4.5 CLAY MINERALS AND THE RNA WORLD There is a general consensus that RNA was the most important biopolymer in early life on earth (the RNA world) since even modern peptide bond formation (protein biosynthesis) in the ribosome was found to be catalyzed by RNA and not by protein enzymes (Ban et al., 2000). DNA is believed to have

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appeared after RNA and to have derived later from RNA for the following reasons: i. The ribose structural unit present in RNA monomers was probably formed from formaldehyde or an oligomer of formaldehyde. The prebiotic synthesis of the deoxyribose of DNA requires the reaction of a mixture of starting materials. ii. The modern biosynthesis of DNA triphosphates proceeds from RNA triphosphates using an unusual enzyme that apparently evolved after RNA formed. iii. RNA, in contrast to DNA, exhibits catalytic activity as well as information storage. Thus, it could have served as a catalyst as well as a storehouse of genetic information in the first life (Zaug and Cech, 1986). The adsorption of RNA components by clay minerals was extensively studied. For example, the adsorption of adenine, cytosine, uracil, ribose and phosphate by Mg2þ–Mt was investigated (Hashizume et al., 2010). The isotherms for adenine, cytosine and uracil were of the C-type and the amount adsorbed increased linearly with the equilibrium solute concentration. All three nucleic acid bases were apparently adsorbed by coordination to Mg2þ ions through a water bridge. Very little ribose was adsorbed by Mg2þ–Mt. The isotherm of phosphate adsorption was of the L-type. The plateau value indicated that phosphate adsorbed on the edge surface of Mt. At comparable solute concentrations, adsorption decreased in the order adenine > cytosine > uracil. This observation reflects differences in basicity, size and aqueous solubility among the three compounds. In another study, the interactions of nucleic acid bases with sulphidemodified Mt were studied at pH 2 and 7. The analysis by Mo¨ssbauer and EPR spectroscopies and X-ray diffractometry showed that nucleic acid bases penetrate into the interlayer space of the clay minerals and oxidize Fe2þ to Fe3þ. At the two pH values, the order of the adsorption of nucleic acid bases on the clay minerals was adenine  cytosine > thymine > uracil. The adsorption of adenine and cytosine on the clay minerals increased with decreasing pH. For unaltered Mt, this result could be explained by electrostatic forces between the positively charged adenine/cytosine and the negative charges of the clay mineral. FT-IR spectra showed that the interaction between the nucleic acid bases and the clay minerals was through NHþ or NH2 þ groups. X-ray diffractograms showed that the nucleic acid bases adsorbed on the clay minerals were distributed on the interlayer surfaces and on external surface aluminol and silanol groups (Carneiro et al., 2011). The interactions of adenine and thymine with zeolites were also studied using different techniques. As shown by XRD, thymine increased the decomposition of the zeolites (Y, ZSM-5) while adenine prevented it. Zeolite Y adsorbed almost the same amount of adenine and thymine. Thus both nucleic acid bases could be protected from hydrolysis and UV radiation and could be available for chemical evolution (Bau´ et al., 2011).

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Initial attempts to form RNA by heating monomers or by using condensing agents did not yield long oligomers. Polymerization studies that used activated monomers were the most successful and these are reviewed here, keeping in mind that, in most instances, potential prebiotic sources of the activated monomers remain to be discovered. One of the successful applications of Bernal’s proposal concerns the observation that oligomers containing 6–14 monomer units are formed when RNA monomers ImpA (Fig. 10.4.1) activated on the phosphate with an imidazole group condense in the presence of Mt (Ferris and Ertem, 1993). The formation of oligomers was generalized to the other nucleotide bases cytosine, guanine, inosine and uracil. Catalysis has the potential for limiting the number of isomers formed. For example, the natural 30 ,50 -linked phosphodiester bond is favoured in the reaction of purine nucleotides on Mt. The 20 , 50 -linkage is favoured in the absence of catalysis and in the clay mineralcatalyzed reactions of pyrimidine nucleotides. Analysis of the dimers formed in the reaction of mixtures of two or more activated nucleotides demonstrated strong sequence selectivity of the dimers formed (Ertem and Ferris, 2000). The 50 -purine-pyrimidine sequence is favoured over the 50 -pyrimidine-purine sequence at the end of the polymer chain by a factor of about 20. In addition, five 50 -sequences (A-C, A-U, G-C, A-A and GA) are formed in significantly larger amounts (73% total yield) than the 11 others in the reaction of mixtures of the four activated monomers of the nucleotides A, C, G and U. The formation of short RNA oligomers with Mt as catalyst was the first step in the preparation of the RNA needed for the initiation of the RNA world. In the second step, it was shown that it is possible to generate longer RNA by elongation of short oligomers (Fig. 10.4.2) using the ‘feeding’ protocol (Ferris et al., 1996; Ferris, 2002). The decanucleotide (pdA)9pA bound to Naþ–Mt was fed with ImpA, and the reaction mixture was allowed to stand for 1 day at 25  C. The dispersion was then centrifuged to separate the aqueous phase from the Mt. Fresh ImpA solution was added to the Mt–oligomer complex, and the reaction was allowed to proceed for another day. Polyadenylates containing more than 20 mers were formed after feeding twice with ImpA, with the main products being 11–14 mers. Polynucleotides containing more than 50 mers were formed after 14 feedings, with the principal oligomeric products containing 20–40 monomer units. Twenty-five to thirty O N

N

P

O

Adenine

5⬘ O

O– 3⬘ 2⬘ HO

OH

FIGURE 10.4.1 RNA activated monomer ImpA with the 20 , 30 and 50 positions for the phosphodiester linkages.

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O N

(pdA)9pA

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+

N

P

O

Adenine

5⬘ O

ImpA

O–

(pdA)9pApA

3⬘ 2⬘ HO

+ ImH

etc. OH

FIGURE 10.4.2 Elongation of a decanucleotide by reaction with ImpA.

mers were obtained with the corresponding uridine-activated monomer (Ferris, 2002). The reaction of D,L-ImpA showed partial inhibition by the monomer unit of the opposite handedness. The longest oligomer formed was a 8 mer while the longest oligomer formed from one enantiomer was a 10 mer (Joshi et al., 2000; Urata et al., 2001). The linear dimers formed from racemic mixtures of ImpA and ImpU exhibited a 60:40 ratio of the D-D and L-L dimers to D-L and L-D dimers formed (Joshi et al., 2000). A study was undertaken to establish whether there exists a correlation between the extent of catalytic property and the charge density of Mt. The catalytic activity of Mt with lower charge density was superior to that of higher charge density Mt. Lower charged Mt formed longer oligomers that contained 9–10 monomer units, while Mt with high charge density catalyzed the formation of oligomers that contained only 4 monomer units (Ertem et al., 2010). During the Hadean to early Archean period (4.5–3.5 Ga), the surface of the Earth’s crust was predominantly composed of basalt and komatiite lavas, so Meunier et al. (2010) considered that the composition of these rocks favoured the crystallization of Fe–Mg clay minerals rather than that of Al-rich ones such as Mt. It was assumed that every square metre of basalt or komatiite rocks was punctuated by myriads of clay mineral-rich patches, each of them potentially behaving as a single chemical reactor that could concentrate the organic compounds in the ocean water. Considering the high catalytic potential of clay minerals, and particularly of the Fe-rich ones (electron exchangers), it is probable that large parts of the surface of the young Earth participated in the synthesis of prebiotic molecules during the Hadean to early Archean period through innumerable clay mineral-rich micro-settings in the massive parts and the altered surfaces of komatiite and basaltic lavas. This led the authors to suggest that Fe,Mg-clay minerals should be preferred to Al-rich ones such as Mt to conduct experiments for the synthesis and the polymerization of prebiotic molecules.

10.4.6 POLYPEPTIDE FORMATION ON CLAY MINERALS Clay minerals can also be used to condense amino acids in water by chemical activation, temperature/moisture cycles or both. A model for the prebiotic formation of polypeptides is based on the contemporary biosynthesis of proteins, which proceeds via the chemically activated monomer aminoacyladenylate (Fig. 10.4.3).

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The amino acylphosphate derivatives of 50 -AMP condensed to polypeptides on Mt (Paecht-Horowitz et al., 1970; Paecht-Horowitz and Eirich, 1988). The products were polypeptides as long as 56 mers in which the C-terminal group of the peptide was attached to the 20 - and/or 30 -hydroxyl group of 50 -AMP. In an homogeneous aqueous solution, alanyl adenylate condensed partially to heptaalanine but deactivation via hydrolysis remained the main pathway. Initially, it was reported that amino acyladenylates were formed by the reaction of amino acids with ATP in the presence of a zeolite. However, it was not possible to reproduce this synthesis (Warden et al., 1974). Glutamic acid was subjected to the feeding protocol using the condensing agent carbonyl diimidazole. The activation proceeded via the intermediary formation of an N-carboxyanhydride (Ehler and Orgel, 1976; Brack, 1987) (Fig. 10.4.4). Illite was incubated with the amino acid and carbonyl diimidazole until short oligomers were formed. The solid was separated by centrifugation, and fresh monomer and activating agent were added. The process was repeated as often as necessary for the production of oligomers of lengths of 40 or more. In the absence of illite, oligomers up to the 10 mer were detected but the majority of the products were shorter than the 5 mer. In the presence of illite, the shorter oligomers remained in the supernatant while the longer oligomers adsorbed to the illite. After 50 feedings, oligomers up to at least the 55 mer were detected, the bulk of the adsorbed product being in the 30–50 size range (Ferris et al., 1996; Hill et al., 1998). Illite failed to produce substantial amounts of aspartic acid, the other acidic amino acid (Hill et al., 1998). The feeding protocol was not restricted to negatively charged amino acids. Oligoarginines were accumulated on the surface of illite by carbonyl diimidazole. In the absence of a mineral, the longest detectable oligomer was the 6 mer. In the presence of illite, oligomers up to the 12 mer could be detected after 10 cycles (Liu and Orgel, 1998). The O H2N

CHR

C

O O

P

Adenine O

O

–

O

OH

HO

FIGURE 10.4.3 Amino acyladenylate.

O HN

NH2JCH(CH2JCH2JCOOH)JCOOH

+

N

N

CO

N

N

O O

+

2 ImH

HOOC

FIGURE 10.4.4 Formation of the N-carboxyanhydride of glutamic acid with carbonyl diimidazole.

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formation of long polypeptide chains from neutral amino acids has not yet been accomplished. Fluctuating moisture and temperature cycles were used to polymerize amino acids in the presence of clay minerals. Lahav et al. (1978) subjected mixtures of glycine and Naþ-kaolinite or Naþ-bentonite to wet-dry and temperature fluctuations (25–94  C) and observed the formation of oligopeptides up to five glycine residues in length. Only trace amounts of diglycine formed without the clay minerals. White and Erickson (1980) studied the influence of the dipeptide histidyl-histidine on the polymerization of glycine during fluctuating moisture and temperature cycles on kaolinite. A turnover of 52 was observed, that is, each dipeptide molecule promoted the polymerization of 52 molecules of glycine. The drying/wetting cycles at 80  C were extended to alanine in the presence of Mt and hectorite (Bujdak and Rode, 1997). Only 0.1% of alanine dimerized on hectorite and no reaction proceeded on Mt. Clay minerals more efficiently catalyzed peptide chain elongation than amino acid dimerization. The reaction yields of tripeptides from diglycine and cyclic diglycine reached about 0.3% on Mt and 1% on hectorite. Different amino acids thioesters were polymerized in the presence of Mt (Bertrand et al., 2001): Thioesters represent a moderate, prebiotically plausible amino acid activator (Weber and Orgel, 1979; Weber, 1998) and were shown to adsorb onto Mt. They easily formed in warm, acid and sulphur-rich environments. They play a key role in modern metabolisms, for example, of the acetyl-coenzyme A and could be the origin of a prebiotic energy transfer (DeDuve, 1998). In the presence of Mt, the formation of the cyclic dipeptide, the main product formed in the control reaction, was totally inhibited. However, no oligomer longer than the tetrapeptide could be obtained. It is likely that the thioesters remained intercalated in Mt since they could not be detected in the supernatant. LeuSEt exposed to wetting-drying and temperature (25–80  C) cycles, polymerised up to the heptapeptide in the presence of montmorillonite.

10.4.7 CLAY MINERALS AND THE FORMATION OF VESICLES Mt was shown to accelerate the spontaneous conversion of fatty acid micelles into vesicles. The group of Jack Szostak assumed that a layer of cations associated with or adjacent to the Mt surface attracts negatively charged micelles or free fatty acid molecules, thereby increasing their concentration locally and thus facilitating their aggregation into a bilayer membrane. Clay mineral particles often become encapsulated in these vesicles, thus providing a pathway for the prebiotic encapsulation of catalytically active surfaces within vesicles. In addition, RNA adsorbed to clay minerals can be encapsulated within vesicles. Once formed, such vesicles can grow by incorporating fatty acid supplied as micelles and can divide without dilution of their contents by

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extrusion through small pores. These processes mediate vesicle replication through cycles of growth and division (Hanczyc et al., 2003). The analysis of mineral-mediated vesicle catalysis was extended to include other natural minerals and synthetic surfaces of varying shape, size and charge density. While RNA polymerization on minerals may be restricted to the surface environment provided by Mt, vesicle formation is enhanced in the presence of disparate types of surfaces. A model is presented in which new sheets of amphiphiles form just proximal to a surface. Similar interactions between amphiphiles and minerals on early earth may have resulted in the encapsulation of diverse mineral particles with catalytic properties (Hanczyc et al., 2007).

10.4.8 CONCLUSION Since Bernal’s suggestion that clay minerals could have participated in the processes leading to primordial life, the mineral surfaces were endowed with exceptional virtues such as the possibility to host a primitive mineral life or to the potential to have generated the biological one-handedness. So far, these exceptional virtues have not been legitimized by experimental data. But clay minerals could have been excellent catalysts for the formation of biopolymers of the first life in aqueous environment as demonstrated by the remarkable experiments of Orgel at the Salk Institute in San Diego and by the group of Ferris at the Rensselaer Polytechnic Institute in Troy. The elongation of RNA to chains longer than 40 mers could have provided the RNA that initiated the RNA world. It was proposed that such RNA with chain lengths above 40 mers would have been able to replicate by template-directed synthesis with sufficient fidelity to maintain the core information content of their sequences (Joyce and Orgel, 1999). In addition, it was postulated that a 40 mer is the minimum chain length required for RNA to catalyze the reactions of other RNA molecules (Szostak and Ellington, 1993; Joyce and Orgel, 1999). The longest chains of both polynucleotides and polypeptides were obtained by using the feeding protocol, which represents a plausible model for prebiotic polymerization. All these data suggest that clay minerals played an active role in the abiotic origin of life.

REFERENCES Avetisov, V.A., Goldanskii, V.I., Kuz’min, V.V., 1991. Handedness, origin of life and evolution. Phys. Today 44, 33–42. Ballard, T., Freudenthal, J., Avagyan, S., Kahr, B., 2007. Test of Cairns-Smith’s “crystalsas-genes” hypothesis. Faraday Discuss. 136, 231–245. Ban, N., Nissen, P., Hansen, J., Moore, P.B., Steitz, T.A., 2000. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 289, 905–920. Bau´, J.P.T., Carneiro, C.E.A., de Souza Jr., I.G., de Souza, C.M.D., da Costa, A.C.S., di Mauro, E., Zaia, C.T.B.V., Coronas, J., Casado, C., de Santana, H., Zaia, D.A.M., 2011.

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Chapter

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