Mineral Surfaces: A Mixed Blessing for the RNA World?

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faces was a productive and even necessary step toward the. RNA world. This conclusion may be premature. For decades, scientists have postulated that mineral ...
ASTROBIOLOGY Volume 9, Number 2, 2009 © Mary Ann Liebert, Inc. DOI: 10.1089/ast.2008.0928

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Mineral Surfaces: A Mixed Blessing for the RNA World? Nicholas V. Hud

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ASTROBIOLOGY, Arora and Kamaluddin report that ribonucleotide monophosphates bind to the surface of aluminum oxide (Arora and Kamaluddin, 2009). These results are presented in support of their hypothesis that metal oxides facilitated the prebiotic formation of RNA polymers, either by protecting mononucleotides from degradation or by promoting nucleotide polymerization. In their own words, “The present work shows aluminum oxide to be a good adsorbent for ribonucleotides and therefore supports the possible role of metal oxides in chemical evolution.” Such statements reflect the opinion of many prebiotic chemists that mononucleotide adhesion to mineral surfaces was a productive and even necessary step toward the RNA world. This conclusion may be premature. For decades, scientists have postulated that mineral surfaces facilitated the origin of life by concentrating molecules from solution and by catalyzing chemical reactions (Bernal, 1949; Hazen, 2005). The prebiotic role of mineral surfaces as general catalysts looks very attractive, particularly for the formation of biological building blocks from smaller, plausibly prebiotic molecules (Saladino et al., 2004). However, more specific proposals for the roles of minerals in life’s origin necessarily remain more speculative. These proposed roles include, but are not limited to, nucleotide and amino acid polymerization (Ferris et al., 1996; Liu and Orgel, 1998), the chiral selection of molecules (Hazen et al., 2001), the first cell-like compartments (Hanczyc et al., 2003; Martin and Russell, 2003), the creation of metabolic cycles (Wächtershäuser, 2007), and Cairns-Smith’s highly influential proposal that the first replicating living systems were themselves clay surfaces (Cairns-Smith, 1982). Surfaces can exhibit remarkable catalytic properties, but the current enthusiasm displayed by many prebiotic chemists for mineral surfaces may be greater than is warranted. Surely, not every example of a biomolecule interacting with a mineral surface should be considered a clue to the origin of life. The article by Arora and Kamaluddin regarding nucleotide adhesion to metal oxides presents an opportunity for an open dialogue on this point. Adhesion of nucleotides to a mineral surface is, at best, a double-edged sword. In support of their proposal for the participation of metal oxides in chemical evolution, Arora and Kamaluddin cite the extensive work from the Ferris N THIS ISSUE OF

laboratory that has demonstrated the polymerization of chemically activated mononucleotides on clay surfaces (Ferris et al., 1996; Huang and Ferris, 2006). Ferris and coworkers have clearly shown that polymer growth can be promoted by a surface that binds both the polymer and its activated monomeric units. Nevertheless, the enhanced affinity of polymers relative to monomers also presents potential problems. With the coupling of each additional residue, a polymer grown on a surface increases its free energy of surface attachment (de Duve and Miller, 1991; Orgel, 1998). Such a polymer can become effectively irreversibly bound to the surface until a considerable change in the local environment (e.g., pH, salinity, or temperature) promotes release from the surface. Therefore, short-term gains provided by surface attachment can lead to an additional obstacle. Nucleotide coupling with chemically activated mononucleotides has proven inefficient in aqueous solution (Joyce and Orgel, 2006), but monomer attachment to a mineral surface represents only one way to solve the polymerization problem. Some alternative scenarios for the origin of the first RNA-like polymers include the possibility that prebiotic nucleoside coupling occurred in a different solvent than water or that the original linkage group between nucleosides was not phosphate. For example, experiments with nucleosides and oligonucleotides dissolved in formamide indicate that phosphorylation and polymerization can be thermodynamically favored in this plausibly prebiotic solvent (Schoffstall, 1976; Schoffstall et al., 1982; Benner et al., 2004; Ciciriello et al., 2008). Deamer and coworkers have also reported that phosphodiester linkages are formed between mononucleotides when they are dried from water in the presence of lipids (Rajamani et al., 2008). Finally, structurally analogous acetal linkages have been achieved by simply drying mononucleosides from aqueous solution in the presence of the aldehyde glyoxylate (Bean et al., 2006). Thus, mineral-catalyzed polymerization of activated mononucleotides is only one of several current proposals for how the first informational polymers were formed. With regard to the particular results presented by Arora and Kamaluddin, adsorption of unactivated mononucleotides to a surface does not necessarily imply that RNA polymer formation will be promoted by the surface. In fact,

School of Chemistry and Biochemistry, Georgia Institute of Technology, Atlanta, Georgia.

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254 surface attachment could hinder polymerization. If nucleotides are not appropriately organized on a surface, their attachment represents a further barrier to polymerization, as the nucleotides must dissociate then re-associate at favorable sites before polymerization can occur. Furthermore, if molecules other than nucleotides compete for adsorption, then adsorbed nucleotides could find themselves next to non-nucleotide molecules. The prebiotic reactions that produced the first nucleotides or their predecessors undoubtedly produced a substantial number of other molecules that also adhered to mineral surfaces. Coupling of nucleotides to nonnucleotide molecules (reactions which could be surface catalyzed) would reduce the amount of nucleotides available for the production of RNA—a step in the wrong direction. Some of the problems likely to arise if mononucleotide surface attachment precedes polymerization could be avoided by the self-assembly of nucleotides (or their bases) in solution prior to polymerization. Moreover, we have argued that the self-assembly of molecules that form Watson-Crick base pairs, prior to polymerization, could have been a critical step toward the emergence of the first RNA-like polymers (Hud and Anet, 2000; Hud et al., 2007). In the solution state, reversible interactions (noncovalent and covalent) under thermodynamic control can be highly selective (Li et al., 2002)— sufficiently, perhaps, to have assembled and segregated the first nucleoside bases from a complex prebiotic “soup.” Such a selection could have prevented co-polymerization of the nucleotides with molecules that have similar reactive groups but do not form Watson-Crick base pairs (e.g., sugars, sugar phosphates). Without the selective partitioning of nucleotides prior to polymerization, whether on a surface or in solution, the incorporation of nucleotides into mixed polymers (i.e., polymers also containing nonpairing residues) would have been an inevitable and potentially devastating mechanism for the loss of information-carrying molecules. Arora and Kamaluddin do not comment on the possibility that alumina might selectively bind mononucleotides in an orientation that promotes or allows Watson-Crick base pairing. However, the data presented in their article suggest that Watson-Crick base pairing would not be favored for mononucleotides bound to alumina. Infrared spectra indicate that the N1 positions of the purine and the N3 positions of the pyrimidine nucleotides are involved in surface binding. In the absence of evidence that base-paired mononucleotides bind with greater affinity than unpaired mononucleotides, it is not clear how alumina might selectively partition mononucleotides from non-base-pairing nucleotide-like molecules prior to polymerization. Mineral surfaces may have played an important role in the origin of life. However, alternative scenarios for promoting the formation of RNA-like polymers—including self-assembled complexes in solution and polymerization in non-aqueous solvents—also merit consideration. In any case, it is prudent and constructive to keep in mind the pros and cons of surface attachment. References Arora, A.K. and Kamaluddin. (2009) Role of metal oxides in chemical evolution: interaction of ribose nucleotides with alumina. Astrobiology 9:165–171.

HUD Bean, H.D., Anet, F.A.L., Gould, I.R., and Hud, N.V. (2006) Glyoxylate as a backbone linkage for a prebiotic ancestor of RNA. Orig. Life Evol. Biosph. 36:39–63. Benner, S.A., Ricardo, A., and Carrigan, M.A. (2004) Is there a common chemical model for life in the universe? Curr. Opin. Chem. Biol. 8:672–689. Bernal, J.D. (1949) The physical basis of life. Proceedings of the Physical Society. Section B 62:597–618. Cairns-Smith, A.G. (1982) Genetic Takeover and the Mineral Origins of Life, Cambridge University Press, Cambridge. Ciciriello, F., Costanzo, G., Pino, S., Crestini, C., Saladino, R., and Di Mauro, E. (2008) Molecular complexity favors the evolution of ribopolymers. Biochemistry 47:2732–2742. de Duve, C. and Miller, S.L. (1991) 2-Dimensional life. Proc. Natl. Acad. Sci. U.S.A. 88:10014–10017. Ferris, J.P., Hill, A.R., Liu, R.H., and Orgel, L.E. (1996) Synthesis of long prebiotic oligomers on mineral surfaces. Nature 381:59–61. Hanczyc, M.M., Fujikawa, S.M., and Szostak, J.W. (2003) Experimental models of primitive cellular compartments: encapsulation, growth, and division. Science 302:618–622. Hazen, R.M. (2005) Genesis, The Scientific Quest for Life’s Origin, Joseph Henry Press, Washington, DC. Hazen, R.M., Filley, T.R., and Goodfriend, G.A. (2001) Selective adsorption of L- and D-amino acids on calcite: implications for biochemical homochirality. Proc. Natl. Acad. Sci. U.S.A. 98:5487–5490. Huang, W. and Ferris, J.P. (2006) One-step, regioselective synthesis of up to 50-mers of RNA oligomers by montmorillonite catalysis. J. Am. Chem. Soc. 128:8914–8919. Hud, N.V. and Anet, F.A.L. (2000) Intercalation-mediated synthesis and replication: a new approach to the origin of life. J. Theor. Biol. 205:543–562. Hud, N.V., Jain, S.S., Li, X.H., and Lynn, D.G. (2007) Addressing the problems of base pairing and strand cyclization in template-directed synthesis—a case for the utility and necessity of “molecular midwives” and reversible backbone linkages for the origin of proto-RNA. Chem. Biodivers. 4:768–783. Joyce, G.F. and Orgel, L.E. (2006) Progress towards understanding the origin of the RNA world. In The RNA World, Third Edition: The Nature of Modern RNA Suggests a Prebiotic RNA World, edited by R.F. Gesteland and J.F. Atkins, Cold Spring Harbor Laboratory Press, Woodbury, NY, pp 23–56. Li, X., Zhan, Z.-Y.J., Knipe, R., and Lynn, D.G. (2002) DNA-catalyzed polymerization. J. Am. Chem. Soc. 124:746–747. Liu, R. and Orgel, L.E. (1998) Polymerization on the rocks: -amino acids and arginine. Orig. Life Evol. Biosph. 28:245–257. Martin, W. and Russell, M.J. (2003) On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 358:59–85. Orgel, L.E. (1998) Polymerization on the rocks: theoretical introduction. Orig. Life Evol. Biosph. 28:227–234. Rajamani, S., Vlassov, A., Benner, S., Coombs, A., Olasagasti, F., and Deamer, D. (2008) Lipid-assisted synthesis of RNA-like polymers from mononucleotides. Orig. Life Evol. Biosph. 38:57–74. Saladino, R., Crestini, C., Costanzo, G., and DiMauro, E. (2004) Advances in the prebiotic synthesis of nucleic acids bases: implications for the origin of life. Curr. Org. Chem. 8:1425– 1443.

MINERAL SURFACES: A MIXED BLESSING? Schoffstall, A.M. (1976) Prebiotic phosphorylation of nucleosides in formamide. Orig. Life Evol. Biosph. 7:399–412. Schoffstall, A.M., Barto, R.J., and Ramos, D.L. (1982) Nucleoside and deoxynucleoside phosphorylation in formamide solutions. Orig. Life Evol. Biosph. 12:143–151. Wächtershäuser, G. (2007) On the chemistry and evolution of the pioneer organism. Chem. Biodivers. 4:584–602.

255 Address reprint requests to: Nicholas V. Hud School of Chemistry and Biochemistry Georgia Institute of Technology Atlanta, GA 30332 E-mail: [email protected]