Montmorillonite-catalysed formation of RNA oligomers: The possible role of catalysis in the origins of life

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 361, Issue 1474, 2006, Pages 1777-1786

  Ferris, James P ^a  

^a Research Rensselaer Polytechnic Institute   (United States)

Author keywords

Montmorillonite catalysis; Origin of life; Prebiotic; Ribonucleic acid; Sequence

Indexed keywords

MONTMORILLONITE; ORIGIN OF LIFE; RNA; EARLY EARTH;

EID: 33750054721     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2006.1903     Document Type: Conference Paper

References (75)

1. Amelin, Y. 2005 A tale of early Earth told in zircons. Science 310, 1914-1915.
2. Ban, N., Nissen, P., Hansen, J., Moore, P. B. & Seitz, T. A. 2000 The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289, 905-920. (doi:10.1126/science.289.5481.905)
3. Banin, A., Lawless, J. G., Mazzurco, J., Church, F. M., Margulies, L. & Orenberg, J. B. 1985 pH profile of the adsorption of nucleotides onto montmorillonite. Orig. Life Evol. Biosph. 15, 89-101. (doi:10.1007/BF01809491)
4. 2+. J. Mol. Biol. 144, 567-577. (doi:10.1016/0022-2836(80)90337-X)
5. Brandes, J. A., Boctor, N. Z., Cody, G. D. & Cooper, B. A. 1998 Abiotic nitrogen reduction on the early Earth. Nature 395, 365-367. (doi:10.1038/26450)
6. Cody, G. D., Boctor, N. Z., Filley, T. R., Hazen, R. M., Scott, J. H., Sharma, A. & Yoder Jr, H. S. 2000 Primordial carbonylated iron-sulfur compounds and the synthesis of pyruvate. Science 289, 1337-1340. (doi:10.1126/science.289.5483.1337)
7. Delano, J. 2001 Redox History of the Earth's interior since ∼ 3900 Ma: implications for prebiotic molecules. Orig. Life Evol. Biosph. 31, 311-341. (doi:10.1023/A:1011895600380)
8. Ding, Z. P., Kawamura, K. & Ferris, J. P. 1996 Oligomerization of uridine phosphorimidazolides on montmorillonite: a model for the prebiotic synthesis of RNA on minerals. Orig. Life Evol. Biosph. 26, 151-171. (doi:10.1007/BF01809853)
9. Eigen, M., McCaskill, J. & Schuster, P. 1988 Molecular quasi-species. J. Phys. Chem. 92, 6881-6891. (doi:10.1021/j100335a010)
10. Ertem, G. & Ferris, J. P. 1997 Template-directed synthesis using the heterogeneous templates produced by montmorillonite catalysis. A possible bridge between the prebiotic and RNA worlds. J. Am. Chem. Soc. 119, 7197-7201. (doi:10.1021/ja970422h)
11. Ertem, G. & Ferris, J. P. 2000 Sequence- and regio-selectivity in the montmorillonite-catalyzed synthesis of RNA. Orig. Life Evol. Biosph. 30, 411-422. (doi:10.1023/A:1006767019897)
12. Ferris, J. P. 1992 Marine hydrothermal systems and the origin of life: chemical markers of prebiotic chemistry in hydrothermal systems. Orig. Life Evol. Biosph. 22, 109-134. (doi:10.1007/BF01808020)
13. Ferris, J. P. 2002 Montmorillonite catalysis of 30-50 mer oligonucleotides: laboratory demonstration of potential steps in the origin of the RNA world. Orig. Life Evol. Biosph. 32, 311-332. (doi:10.1023/A: 1020543312109)
14. Ferris, J. P. 2005 Catalysis and prebiotic synthesis. In Molecular geomicrobiology, vol. 59 (ed. J. F. Banfield, J. Cervini & K. Nealson), pp. 187-210. Chantilly, VA: Mineralogical Society of America.
15. Ferris, J. P. & Ertem, G. 1993a Montmorillonite catalysis of RNA oligomer formation in aqueous solution. A model for the prebiotic formation of RNA. J. Am. Chem. Soc. 115, 12 270-12 275. (doi:10.1021/ja00079a006)
16. Ferris, J. P. & Ertem, G. 1993b Oligomerization reactions of ribonucleotides: the reaction of the 5′-phosphorimidazolide of adenosine with diadenosine pyrophosphate on montmorillonite and other minerals. Orig. Life Evol. Biosph. 23, 229-241. (doi:10.1007/BF01581901)
17. Ferris, J. P. & Hagan Jr, W. J. 1984 HCN and chemical evolution: the possible role of cyano compounds in prebiotic synthesis. Tetrahedron 40, 1093-1120. (doi:10.1016/S0040-4020(01)99315-9)
18. Ferris, J. P., Joshi, P. C., Edelson, E. H. & Lawless, J. G. 1978 HCN: a plausible source of purines, pyrimidines, and amino acids on the primitive Earth. J. Mol. Evol. 11, 293-311. (doi:10.1007/BF01733839)
19. Ferris, J. P., Huang, C.-H. & Hagan Jr, W. J. 1986 Clays as prototypical enzymes for the prebiological formation of phosphate esters. Orig. Life Evol. Biosph. 17, 173-174.
20. Ferris, J. P., Ertem, G. & Agarwal, V. K. 1989 Mineral catalysis of the formation of dimers of 5′-AMP in aqueous solution: the possible role of montmorillonite clays in the prebiotic synthesis of RNA. Orig. Life Evol. Biosph. 19, 165-178. (doi:10.1007/BF01808150)
21. Ferris, J. P., Hill Jr, A. R., Liu, R. & Orgel, L. E. 1996 Synthesis of long prebiotic oligomers on mineral surfaces. Nature 381, 59-61. (doi:10.1038/381059a0)
22. Fuller, W. D., Sanchez, R. A. & Orgel, L. E. 1972 Studies in prebiotic synthesis IV. Synthesis of purine nucleosides. J. Mol. Biol. 67, 25-33. (doi:10.1016/0022-2836(72)90383-X)
23. Gestland, T. R., Cech, T. R. & Atkins, J. F. 1999 The RNA world. New York, NY: Cold Spring Harbor Press.
24. Gladman, B., Dones, D., Levinson, H. F. & Burns, J. A. 2005 Impact seeding and reseeding in the inner solar system. Astrobiology 5, 483-496. (doi:10.1089/ast.2005.5.483)
25. Gomes, R., Levison, H. F., Tsiganis, K. & Morbidelli, A. 2005 Origin of the cataclysmic late heavy bombardment period of the terrestrial planets. Nature 435, 466-469. (doi:10.1038/nature03676)
26. Hanczyc, M. M., Fujikawa, S. M. & Szostak, J. W. 2003 Experimental models of primitive cellular compartments: encapsulation, growth and division. Science 302, 618-622. (doi:10.1126/science.1089904)
27. Harrison, T. M., Blichert-Toft, J., Muller, W., Albarede, F., Holden, P. & Mojzsis, S. J. 2005 Heterogeneous Hadean hafnium: evidence of continental crust at 4.4 to 4.5. Science 310, 1947-1950. (doi:10.1126/science.1117926)
28. Huang, W. & Ferris, J. P. 2003 Synthesis of 35-40 mers of RNA oligomers from unblocked monomers. A simple approach to the RNA world. Chem. Commun. 12, 1458-1459. (doi:10.1039/b303134a)
29. Huber, C. & Wächtershäuser, G. 1997 Activated acetic acid by carbon fixation on (Fe,Ni)S under primordial conditions. Science 2776, 245-247. (doi:10.1126/science.276.5310.245)
30. Inoue, T. & Orgel, L. E. 1981 Substituent control of the poly(C)-directed oligomerization of guanosine 5′-phosphoroimidazolide. J. Am. Chem. Soc. 103, 7666-7667. (doi:10.1021/ja00415a051)
31. Joshi, P. C., Pitsch, S. & Ferris, J. P. 2000 Homochiral selection in the montmorillonite-catalyzed and uncatalyzed prebiotic synthesis of RNA. Chem. Commun. 2497-2498. (doi:10.1039/b007444f)
32. Joyce, G. F. & Orgel, L. E. 1999 Prospects for understanding the origin of the RNA world. In The RNA world: the nature of modern RNA suggests a prebiotic RNA (ed. R. F. Gesteland, T. R. Cech & J. F. Atkins), pp. 49-77. New York, NY: Cold Spring Harbor Laboratory Press.
33. Kanavarioti, A. 1997 Dimerization in highly concentrated solutions of phosphorimidazolide activated mononucleotides. Orig. Life Evol. Biosph. 27, 357-376. (doi:10.1023/A:1006526002896)
34. Kanavarioti, A., Monnard, R-A. & Deamer, D. W. 2001 Eutectic phases in ice facilitate nonenzymatic nucleic acid synthesis. Astrobiology 1, 271-281. (doi:10.1089/15311070152757465)
35. Kaplan, R. W. 1971 The problem of chance in formation of protobionts by random aggregation of macromolecules. In Molecular evolution I. Chemical evolution and the origin of life (ed. R. Buvet & C. Ponnamperuma), pp. 319-329. Amsterdam, The Netherlands; London, UK: NorthHolland Publishing Company.
36. +-montmorillonite. J. Am. Chem. Soc. 116, 7564-7572. (doi:10.1021/ja00096a013)
37. Kawamura, K. & Ferris, J. P. 1999 Clay catalysis of oligonucleotide formation: kinetics of the reaction of the 5′-phosphorimidazolides of nucleotides with the non-basic heterocycles uracil and hypoxanthine. Orig. Life Evol. Biosph. 29, 563-591. (doi:10.1023/A:1006648524187)
38. Kebbekus, P. 1988 Formation of RNA oligomers on montmorillonite clay under possible prebiotic conditions. Chemistry, p. 23. Troy, NY: Rensselaer Polytechnic Institute.
39. Lailach, G. E., Thompson, T. D. & Brindley, G. W. 1968 Absorption of pyrimidines, purines, and nucleosides by Li-, Na-, Mg-, and Ca-montmorillonite (clay-organic studies XII). Clay. Clay Min. 16, 285-293.
40. Lohrmann, R., Bridson, P. K. & Orgel, L. E. 1980 Efficient metal-ion catalyzed template-directed oligonucleotide synthesis. Science 208, 1464-1465.
41. 2 to hydrocarbons during serpentinization of olivine. Geochim. Comochim. Acta 65, 3769-3778. (doi:10.1016/S0016-7037(01)00655-X)
42. Miller, S. L. 1955 Production of some amino acids under possible primitive Earth conditions. J. Am. Chem. Soc. 77, 2351-2361. (doi:10.1021/ja01614a001)
43. Miller, S. L. 1997 Peptide nucleic acids and prebiotic chemistry. Nat. Struct. Biol. 4, 167-169. (doi:10.1038/nsb0397-167)
44. Miyakawa, S. & Ferris, J. P. 2003 Sequence- and regioselectivity in the montmorillonite-catalyzed synthesis of RNA. J. Am. Chem. Soc. 125, 8202-8208. (doi:10.1021/ja034328e)
45. Miyakawa, S., Cleaves, H. J. & Miller, S. L. 2002 The cold origins of life: B. Implications based on pyrimidines and purines produced from frozen ammonium cyanide solutions. Orig. Life Evol. Biosph. 32, 209-218. (doi:10.1023/A:1019514022822)
46. Mojzsis, S. J., Harrison, T. M. & Pidgeon, R. T. 2001 Oxygen-isotope evidence from ancient zircons for liquid water at the Earth's surface 4,300 Myr ago. Nature 409, 178-181. (doi:10.1038/35051557)
47. Monnard, P.-A., Apel, C. L., Kanavarioti, A. & Deamer, D. W. 2002 Influence of ionic inorganic solutes on self-assembly and polymerization processes related to early forms of life: implications for a prebiotic aqueous medium. Astrobiology 2, 139-152. (doi:10.1089/15311070260192237)
48. Monnard, P.-A., Kanavarioti, A. & Deamer, D. W. 2003 Eutectic phase polymerization of activated ribonucleotide mixtures yields quasi-equimolar incorporation of purine and pyrimidine nucleobases. J. Am. Chem. Soc. 125, 13 734-13 740. (doi:10.1021/ja036465h)
49. Müller, D., Pitsch, S., Kittaka, A., Wagner, E., Wintner, C. E. & Eschenmoser, A. 1990 Chemie von a-Aminonitrilen. Aldomerisierung von Glycolaldehyd-phosphat zu racemischen Hexose-2,4,6-triphosphaten und (in Gegenwart von Formaldehyd) racemischen Pentose-2,4-diphosphaten: rac-Allose-2,4,6-triphosphat und rac-Ribose-2,4-diphosphat sind die Reaktionshauptprodukte. Helv. Chim. Acta 73, 1410-1468.
50. Nielsen, P. E., Egholm, M., Berg, R. H. & Buchardt, O. 1991 Sequence-selective recognition of DNA by strand displacement with a thymine-substituted polyamide. Science 254, 1497-1500.
51. Nikalje, M. D., Puhukan, P. & Sudalai, A. 2000 Recent advances in clay-catalyzed transformatiions. Org. Prep. Proced. 32, 1-40.
52. Oro, J. 1960 Synthersis of adenine from ammonium cyanide. Biochem. Biophys. Res. Commun. 2, 407-412. (doi:10.1016/0006-291X(60)90138-8)
53. Osterberg, R. & Orgel, L. E. 1972 Polyphosphate and trimetaphosphate formation under potentially prebiotic conditions. J. Mol. Evol. 1, 241-248. (doi:10.1007/BF01660243)
54. Osterberg, R., Orgel, L. E. & Lohrmann, R. 1973 Further studies of urea-catalyzed phosphorylation reactions. J. Mol. Evol. 2, 231-234. (doi:10.1007/BF01654004)
55. Pizzarello, S. 2004 Chemical evolution and meteorites, an update. Orig. Life Evol. Biosph. 34, 25-34. (doi:10.1023/B:ORIG.0000009826.76353.de)
56. Poulet, F., Bibring, J.-P., Mustard, J. F., Gendrin, A., Mangold, N., Langevin, Y., Arvidson, R. E., Gondet, B. & Gomez, C. 2005 Philosilicates on Mars and implications for early martian climate. Nature 438, 623-627. (doi:10.1038/nature04274)
57. Ricardo, A., Carrigan, M. A., Olcott, A. N. & Benner, S. 2004 Borate minerals stabilize ribose. Science 303, 196. (doi:10.1126/science.1092464)
58. Righter, K. & Drake, M. J. 1999 Effect of water on metal-silicate partitioning of siderophile elements: a high pressure and temperature terrestrial magma ocean and core formation. Earth Planet. Sci. Lett. 171, 383-399. (doi:10.1016/S0012-821X(99)00156-9)
59. Sanchez, R. A., Ferris, J. P. & Orgel, L. E. 1967 Synthesis of purine precursors and amino acids from aqueous hydrogen cyanide. J. Mol. Biol. 30, 223.
60. Sawai, H. 1976 Catalysis of internucleotide bond formation by divalent ions. J. Am. Chem. Soc. 98, 7037-7039. (doi:10.1021/ja00438a050)
61. 2+ ion. J. Am. Chem. Soc. 97, 3532-3533. (doi:10.1021/ ja00845a050)
62. Sawai, H. & Yamamto, K. 1996 Lanthanide ion as a catalyst for internucleotide bond formation. Bull. Chem. Soc. Jpn. 69, 1701-1704. (doi:10.1246/bcsj.69.1701)
63. Sawai, H., Kuroda, K. & Hojo, T. 1989 Uranyl ion as a highly effective catalyst for internucleotide bond formation. Bull. Chem. Soc. Jpn. 62, 2018-2023. (doi:10.1246/bcsj.62.2018)
64. Sawai, H., Higa, K. & Kuroda, K. 1992 Synthesis of cyclic and acyclic oligocytidylates by uranyl ion catalyst in aqueous solution. J. Chem. Soc. Perkin I, 505-508. (doi:10.1039/p19920000505)
65. 2. J. Mol. Evol. 19, 376-382. (doi:10.1007/BF02101642)
66. 2+ ions. J. Mol. Evol. 13, 203-214. (doi:10.1007/BF01739480)
67. Springsteen, G. & Joyce, G. F. 2004 Selective derivatization and sequestration of ribose from a prebiotic mix. J. Am. Chem. Soc. 126, 9578-9583. (doi:10.1021/ja0483692)
68. Symonds, R. B., Rose, W. I., Bluth, G. & Gerlach, T. M. 1994 Volcanic gas studies: methods, results, and applications. In Volatiles in magmas (ed. M. R. Carroll & J. R. Holloway) Reviews in Mineralogy, vol. 30, pp. 1-66. Washington, DC: Mineralogical Society of America.
69. Tian, F., Toon, O. B., Pavlov, A. A. & De Sterck, H. 2005 A hydrogen-rich early Earth atmosphere. Science 308, 1014-1017. (doi:10.1126/science.1106983)
70. Voet, A. B. & Schwartz, A. W. 1982 Uracil synthesis via HCN oligomerization. Orig. Life 12, 45-49. (doi:10.1007/BF00926910)
71. Watson, E. B. & Harrison, T. M. 2005 Zircon thermometer reveals minimum melting conditions on earliest Earth. Science 308, 841-844.
72. Wells, L. E., Armstrong, J. C. & Gonzalez, G. 2003 Reseeding of the early Earth by impacts of returning ejecta during the late heavy bombardment. Icarus 162, 38-46. (doi:10.1016/S0019-1035(02)00077-5)
73. Wilde, S. A., Valley, J. W., Peck, W. H. & Graham, C. M. 2001 Evidence from detrital zircons for the existence of continental crust and oceans on the Earth 4.4 Gyr ago. Nature 409, 175-178. (doi:10.1038/35051550)
74. Williams, L. B., Canfield, B., Voglesonger, K. M. & Holloway, J. R. 2005 Organic molecules formed in a "primordial womb". Geology 33, 913-916. (doi:10.1130/G21751.1)
75. Zubay, G. 1998 Studies on the lead-catalyzed synthesis of aldopentoses. Orig. Life Evol. Biosph. 28, 13-26. (doi:10. 1023/A:1006551410542)