918Accesses
109Citations
4Altmetric
Abstract
Adenine plays an essential role in replication in all known living systems today, and is prominent in many other aspects of biochemistry. It occurs among the products of oligomerization of HCN. These circumstances have stimulated the idea that adenine was a component in a replication system that was present at the start of life. Such replicators have included not only RNA, but also a number of simpler RNA-like alternatives which utilize a simpler backbone.
Despite these encouraging indicators, a consideration of the chemical properties of adenine reveals reasons that disfavor its participation in such a role. These properties include the following: (1) Adenine synthesis requires HCN concentrations of at least 0.01 M. Such concentrations would be expected only in unique circumstances on the early Earth. Adenine yields are low in prebiotic simulations, and if a subsequent high-temperature hydrolysis step is omitted, the reported yield does not represent adenine itself, but 8-substituted adenines and other derivatives. (2) Adenine is susceptibile to hydrolysis (the half life for deamination at 37 °C, pH 7, is about 80 years), and to reaction with a variety of simple electrophiles, forming a multiplicity of products. Its accumulation would not be expected over a geological time scale, and its regioselective incorporation into a replicator appears implausible. (3) The adenine-uracil interaction, which involves two hydrogen bonds (rather than three, as in guanine-cytosine pairing) is weak and nonspecific. Pairing of adenine with many other partners has been observed with monomers, synthetic oligonucleotides and in RNA. The hydrogen-bonding properties of adenine appear inadequate for it to function in any specific recognition scheme under the chaotic conditions of a prebiotic soup.
New and fundamental discoveries in the chemistry of adenine would be needed to reverse this perception. An alternative and attractive possibility is that some other replicator preceeded RNA (or RNA-like substances) in the origin of life.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Benner, S.A., Allemann, R.K., Ellington, A.D., Ge, L., Leanz, G.F., Krauch, T., MacPherson, L.J., Monroney, S., Piccirilli, J.A. and Weinhold, E.: 1987,Cold Spring Harbor Symp. Quant. Biol.LII, 53.
Benner, S.A., Ellington, A.D. and Tauer, A.: 1989,Proc. Natl. Acad. Sci. USA86, 7054.
Bonicel, A., Marriage, N., Hughes, E. and Teoule, R.: 1980,Radiation Res.80, 19.
Boren, T., Elias, P., Claesson, C, Barciszewska, M., Gehrke, C.W., Kuo, K.C., and Lustig, F.: 1993,J. Mol. Biol.230, 799.
Breimer, L.: 1984,Nucleic Acid Res.12, 6359.
Brown, T., Leonard, G.A., Booth, E.D. and Kneale, G., 1990:J. Mol. Biol.212, 437.
Budowsky, E.I., Sverdlov, E.D. and Monastyrskaya, G.S.: 1971,Biochim. Biophys. Acta246, 320.
Cairns-Smith, A.G.: 1982,Genetic Takeover and the Mineral Origins of Life, Cambridge Univ. Press, Cambridge, U.K.
Chaw, Y.F.M., Crane, L.E., Lange, P. and Shapiro, R.: 1980,Biochemistry19, 5525.
Cherny, D.Y., Belotserkovskii, B.P., Frank-Kamenetskii, M.D., Egholm, ML, Buchardt, O., Berg, R.H. and Nielsen, P.E.: 1993,Proc. Natl. Acad. Sci. USA90, 1667.
Chetsanga, C.J. and Grigorian, C: 1985,Proc. Natl. Acad. Sci. USA82, 633.
Chou, S.-H., Cheng, J.-W. and Reid, B.R.: 1992,J. Mol. Biol.228, 138.
Cronin, J.S., Pizzarello, S. and Cruikshank, D.P.: 1988, inMeteorites and the Early Solar System, Kerridge, J.F. and Matthews, M.S., eds., Univ. of Arizona Press, Tucson, 819–857.
Dunn, D.B. and Hall, R. H.: 1975, InHandbook of Biochemistry and Molecular Biology, 3rd Edition, Fasman, G.D., ed., CRC Press, Cleveland, 76.
Dyllick-Brenzinger, C, Sullivan, G.R., Pang, P. and Roberts, J.D.: 1980,Proc. Natl. Acad. Sci. USA77, 5580.
Eschenmoser, A. and Loewenthal, E.: 1992:Chem. Soc. Rev.21, 1.
Ferris, J.P.: 1984, Chemical and Engineering News, August 1984, p 22.
Ferris, J.P. and Hagan, W.J., Jr.: 1984,Tetrahedron40, 1083.
Ferris, J.P.: 1992,Origins of Life Evol. Biosphere22, 109.
Ferris, J.P., Joshi, PC, Edelson, E.H. and Lawless, J.G.: 1978,J. Mol. Evol.11, 293.
Ferris, J.P. and Kuder, J.E.: 1970,J. Amer. Chem. Soc.91, 2527.
Frick, L., MacNeela, J.P. and Wolfenden, R.: 1987,Bioorganic Chem.15, 100.
Fuller, W.D., Sanchez, R.A., and Orgel, L.E.: 1972 a,J. Mol. Biol.67, 25.
Fuller, W.D., Sanchez, R.A. and Orgel, L.E.: 1972b,J. Mol. Evol.1, 249.
Garrett, E.R. and Mehta, P.J.: 1972,J. Amer. Chem. Soc.94, 8542.
Gennis, R.B. and Cantor, C.R.: 1970,Biochemistry9, 4714.
Gilbert, W.: 1986,Nature319, 618.
Giner-Sorolla, A. and Oró, J.: 1993, Abstracts 7th ISSOL Meeting, 10th International Conference on the Origin of Life, Barcelona, 45.
Gonnella, N.C., Nakanishi, H., Holtwick, B., Horowitz, D.S., Kanamori, K., Leonard, N.J. and Roberts, J.D.: 1983,J. Amer. Chem. Soc.105, 2050.
Gordon, M.P., Weliky, V.S. and Brown, G.B.: 1957,J. Amer. Chem. Soc.79, 3245.
Hayatsu, R., Studier, M.H., Matsuoka, S. and Anders, E.: 1972,Geochim. Cosmochim. Acta36, 555.
Hayatsu, R. and Anders, E.: 1981,Topics Curr. Chem.99, 37.
Hunziker, J., Roth, H.-J., Bohringer, M., Giger, A., Diederichsen, U., Gobel, M., Krishnan, R., Juan, B., Leumann, C. and Eschenmoser, A.: 1993,Helv. Chim. Acta76, 259.
Jeong, K., Tjivikua, T., Muehldorf, A., Deslongchamps, G., Famulok, M. and Rebek, J. Jr.: 1991,J. Amer. Chem. Soc.113, 201.
Jones, A.S., Mian, A.M. and Walker, R.T.: 1966, J. Chem. Soc. C, 692.
Joyce, G.F.: 1989,Nature338, 217.
Joyce, G.F. and Orgel, L.E.: 1993, InThe RNA World, Gesteland, R.F. and Atkins, J.F., eds., Cold Spring Harbor Laboratory Press, Plainview, N.Y., 1.
Joyce, G.F., Schwartz, A.W., Miller, S.L. and Orgel, L.E.: 1987,Proc. Natl. Acad. Sci. USA84, 4398.
Kochetkov, N.K. and Budovskii, E.I.: 1971,Organic Chemistry of Nucleic Acids, Parts A and B, Plenum, New York.
Leonard, N.J., McDonald, J.J., Henderson, R.E.L. and Reichmann, M.E.: 1971,Biochemistry10, 3335.
Lindahl, T.: 1993,Nature362, 709.
Lister, J.H.: 1971,Fused Pyrimidines, Part II, Purines, Wiley Interscience, New York.
Maskos, K., Gunn, B.M., LeBlanc, D.A. and Morden, K.M.: 1993,Biochemistry32, 3583.
Maurel, M.-C. and Convert, O.: 1990,Origins of Life Evol. Biosphere20, 43.
Mian, A.M. and Walker, R.T.: 1968, J. Chem. Soc. C, 2577
Miller, S.L. and Orgel, L.E.: 1973,The Origins of Life on the Earth, Prentice Hall, Englewood Cliffs, N.J.
Miller, S.L.: 1987,Cold Spring Harbor Symp. Quant. Biol.LII, 17.
Muller, D., Pitsch, S., Kittaka, A., Wagner, E., Wintner, C.E. and Eschenmoser, E.: 1990,Helv. Chim. Acta73, 1410.
Orgel, L.E.: 1986a,Origins of Life17, 27.
Orgel, L.E.: 1986b,J. Theor. Biol.123, 127
Orgel, L.E. and Crick, F.H.C.: 1993,FASEB J.7, 238.
Oró, J.: 1960,Biochem. Biophys. Res. Commun.2, 407.
Oró, J. and Kimball, A.P.: 1961,Arch. Biochem. Biophys.94, 221.
Pitha, J., Jones, N. and Pithova, N.: 1966,Canad. J. Chem.44, 1045
Pitsch, S., Wendeborn, S., Juan, B. and Eschenmoser, A.: 1993,Helv. Chim. Acta76, 2161.
Ponnamperuma, C, Lemmon, R.M., Mariner, R. and Calvin, M.: 1963,Proc. Nat. Acad. Sci. USA49, 737.
Rebek, J., Jr.: 1990,Acc. Chem. Res.23, 399.
Roques, P., Le Gall, J. Y., Lacombe, L. and Olomucki, M.: 1992,J. Org. Chem.57, 1579.
Saenger, W.: 1984,Principles of Nucleic Acid Structure, Springer-Verlag, New York, 76–78.
Sanchez, R., Ferris, J. and Orgel, L.E.: 1966,Science153, 72.
Sanchez, R., Ferris, J.P. and Orgel, L.E.: 1967,J. Mol. Biol30, 223.
Schlesinger, G. and Miller, S.L.: 1973,J. Amer. Chem. Soc.95, 3729.
Schneider, K.C. and Benner, S.A.: 1990,J. Amer. Chem. Soc.112, 453.
Schwartz, A.W. and Bakker, C.G.: 1989,Science245, 1102.
Schwartz, A.W. and De Graaf, R.M.: 1993,J. Mol. Evol.36, 101.
Schwartz, A.W., Joosten, H. and Voet, A.B.: 1982,Biosystems15, 191.
Schwartz, A.W. and Orgel L.E.: 1985,Science228, 185.
Schwartz, A.W., Visscher, J., Bakker, C.G. and Niessen, J.: 1987a,Origins of Life17, 351.
Schwartz, A.W., Visscher, J., Van der Woerd, R. and Bakker, C.G.: 1987b,Cold Spring Harbor Symp. Quant. Biol.LII, 37.
Segal, A., Fedyk, J., Melchionne, S. and Seidman, I.: 1987,Chem.-Biol. Interactions61, 189.
Shapiro, R.: 1981, InChromosome Damage and Repair, Seeberg, E. and Kleppe, K., eds., Plenum Press, New York, 565–570.
Shapiro, R.: 1984,Origins of Life14, 565.
Shapiro, R.: 1986,Origins: A Skeptic's Guide to the Creation of Life on Earth, Summit, New York.
Shapiro, R.: 1988,Origins of Life Evol. Biosphere18, 71.
Shapiro, R. and Pohl, S.H.: 1968,Biochemistry7, 448.
Sharp, P.A. and Eisenberg, D.: 1987,Science238, 729.
Shea, K.J., Spivak, D.A. and Sellergren, B.: 1993,J. Am. Chem. Soc.115, 3368.
Sodum, R.S. and Shapiro, R.: 1988,Bioorganic Chem.16, 272.
Solomon, J.J., Cote, I.L., Wortman, M., Decker, K. and Segal, A.: 1984,Chem.-Biol. Interactions51, 167.
Solomon, J.J., Singh, U.S. and Segal, A.: 1993,Chem.-Biol. Interactions88, 115.
Sowers, L.C., Shaw, B.R., Veigl, M.L. and Sedwick, W.D.: 1987,Mutation Res.177, 218.
Spach, G.: 1984,Origins of Life14, 433.
Stevens, M.A. and Brown, G.B.: 1958,J. Amer. Chem. Soc.80, 2759.
Stevens, M.A., Magrath, D.I., Smith, H.W. and Brown, G.B: 1958,J. Amer. Chem. Soc.80, 2755.
Stoks, P.G. and Schwartz, A.W.: 1981:Geochim. Cosmochim. Acta45, 563.
Stribling, R. and Miller, S.L.: 1987,J. Mol. Evol.32, 282.
Strasak, M.: 1991,Naturwissenschaften78, 121.
Stryer, L.: 1988,Biochemistry, Third Edition, W.H. Freeman, New York, 82.
Subbaraman, L.R., Subbaraman, J. and Behrman, E.J.: 1969,Biochemistry8, 3059.
Summers, D. P. and Chang, S.: 1993,Nature365, 631.
Voet, A.B. and Schwartz, A.W: 1983,Bioorganic. Chem.12, 8.
Voet, D. and Rich, A.: 1970,Prog. Nucleic Acid Res. Mol. Biol.10, 183.
Wakamatsu, H., Yamada, Y., Saito, T., Kumashiro, I. and Takenishi, T.: 1966,J. Org. Chem.31, 2035.
Waldrop, M.M.: 1989,Science246, 1248.
Watson, J.D., Hopkins, N.H., Roberts, J.W., Steitz, J.A. and Weiner, A.M.: 1987,Molecular Biology of the Gene, Fourth Ed., Vol. II, Benjamin/Cummings, Menlo Park, CA., 1104.
Yuasa, S., Flory, D., Basile, B. and Oró, J.: 1984,J. Mol. Evol.21, 76.
Zimmerman, S.C., Wu, W. and Zeng, Z.: 1991,J. Amer. Chem. Soc.113, 196.
Author information
Authors and Affiliations
Department of Chemistry, New York University, 10003, New York, N.Y., USA
Robert Shapiro
- Robert Shapiro
You can also search for this author inPubMed Google Scholar
Rights and permissions
About this article
Cite this article
Shapiro, R. The prebiotic role of adenine: A critical analysis.Origins Life Evol Biosphere25, 83–98 (1995). https://doi.org/10.1007/BF01581575
Received:
Published:
Issue Date:
Share this article
Anyone you share the following link with will be able to read this content:
Sorry, a shareable link is not currently available for this article.
Provided by the Springer Nature SharedIt content-sharing initiative