Cations as Mediators of the Adsorption of Nucleic Acids on Clay Surfaces in Prebiotic Environments

Abstract

Monovalent ([Na+] > 10 mM) and divalent ([Ca2+], [Mg2+] > 1.0 mM) cations induced the precipitationof nucleic acid molecules. In the presence of clay minerals (montmorillonite and kaolinite), there was adsorption instead of precipitation. The cation concentration needed for adsorption depended on both the valence of the cations and the chemical nature of the nucleic acid molecules. Double-stranded nucleic acids needed higher cation concentrations than single-stranded ones to be adsorbed to the same extent on clay. Divalent cations were more efficient than monovalent ones in mediating adsorption. Adsorption to the clay occurred only when both nucleic acids and cations were present. However, once the complexes were formed, the cations could not be removed from the system by washing, indicating that they are directly involved in the association between nucleic acids and mineral surfaces.These observations indicate that cations take part directly in the formation of nucleic acid-clay complexes, acting as a `bridge' between the negative charges on the mineral surface and those of the phosphate groups of the genetic polymer. The relatively low cation concentrations needed for adsorption and the ubiquitous presence of clay minerals in the environment suggest that the adsorption of nucleic acids on mineral surfaces could have taken place in prebiotic habitats. This may have played an important role in the formation and preservation of nucleic acids and/or their precursor polymers.

cation-bridge adsorption cation-mediated nucleic acids formation clay minerals clay-nucleic acid complexes single/double stranded nucleic acids surface-mediated origin of genetic material 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Banin, A., Lawless, J. G., Mazzucco, J., Church, F. M., Margulis, L. and Orenberg, J. B.: 1985, 'pH profile of the adsorption of nucleotides on montmorillonite', Orig. Life Evol. Biosphere 15, 89-101.Google Scholar
  2. Bernal, J. D.: 1951, The Physical Basis of Life, Routledge & Kegan Paul, London, U.K.Google Scholar
  3. Cairns Smith, G.: 1986, Clay Minerals and the Origin of Life, Cambridge University Press, Cambridge, U.K.Google Scholar
  4. Cech, T. R.: 1987, 'A Model for the RNA-catalyzed Replication of RNA', Proc. Natl. Acad. Sci., Vol. 83, 4360-4363.Google Scholar
  5. Ferris, J. P., Ertem, G. and Agarwal, V. K.: 1989, 'The adsorption of nucleotides and polynucleotides on montmorillonite clay, Orig. Life Evol. Biosphere 19, 153-164.Google Scholar
  6. Ferris, J. P. and Ertem, G.: 1992, 'Oligomerization reactions of ribonucleotides: The reaction of the 5′-phosphorimidazolides of nucleosides on montmorillonite and other minerals, Orig. Life Evol. Biosphere 22, 369-381.Google Scholar
  7. Ferris, J. P.: 1993, Catalysis and prebiotic RNA synthesis, Orig. Life Evol. Biosphere 23, 307-315.Google Scholar
  8. Ferris, J. P., Hill Jr., A. R., Liu, R. and Orgel, L. E.: 1996, 'Synthesis of long prebiotic oligomers on mineral surfaces', Nature 381, 59-61.Google Scholar
  9. Franchi, M., Bramanti, E., Morassi Bonzi, L., Orioli, P. L., Vettori, C. and Gallori, E.: 1999, 'Claynucleic acid complexes: Characteristics and implications for the preservation of genetic material in primeval habitats', Orig. Life Evol. Biosphere 29, 297-315.Google Scholar
  10. Gallori, E., Bazzicalupo, M., Dal Canto, L., Fani, R., Nannipieri, P., Vettori, C. and Stotzky, G.: 1994, 'Tranformation of Bacillus subtilis by DNA bound on clay in non-sterile soil', FEMS Microbiol. Ecol. 15, 119-126.Google Scholar
  11. Gilbert, W.: 1986, 'The RNA world', Nature 319, 618.Google Scholar
  12. Greaves, M. P. and Wilson, M. J.: 1969, 'The adsorption of nucleic acids by montmorillonite', Soil Biol. Biochem. 1, 317-323.Google Scholar
  13. Hesselink, F. T.: 1983, 'Adsorption of Polyelectrolytes from Dilute Solution', in G. D. Parfitt and C. H. Rochester (eds), Adsorption Form Solution at the Solid/Liquid Interface, Academic Press Ltd., London, U.K., pp. 377-412.Google Scholar
  14. Joyce, G. F.: 1989, 'RNA evolution and the origins of life', Nature 338, 217-224.Google Scholar
  15. Khanna, M. and Stotzky, G.: 1992, 'Transformation of Bacillus subtilis by DNA bound on montmorillonite and effect of DNase on the transforming ability of bound DNA', Appl. Environ. Microbiol. 58, 1930-1939.Google Scholar
  16. Krishnamurthy, R., Pitsch, S. and Arrhenius, G.: 1999, 'Mineral induced formation of pentose-2,4-bisphosphates', Orig. Life Evol. Biosphere 29, 139-152.Google Scholar
  17. Lahav, N. and Chang, S.: 1976, 'The possible role of solid surface area in condensation reactions during chemical evolution: Reevaluation', J. Mol. Evol. 8, 357-380.Google Scholar
  18. Lazcano, A. and Miller, S. L.: 1996, 'The origin and early evolution of life: Prebiotic chemistry, the pre-RNA world, and time', Cell 85, 793-798.Google Scholar
  19. Lorenz, M. G. and Wackernagel, W.: 1994, 'Bacterial gene transfer by natural genetic transformation in the environment', Microbiol. Rev. 58, 563-602.Google Scholar
  20. Luther, A., Brandsch, R. and von Kiedrowsky, G.: 1998, 'Surface-promoted replication and exponential amplification of DNA analogues', Nature 396, 245-248.Google Scholar
  21. McBride, M. B.: 1989, 'Surface Chemistry of Soil Minerals', in J. B. Dixon and S. B. Weed (eds), Minerals in Soil Environments, Soil Science Society of America, Madison, WI, U.S.A., pp. 35-87.Google Scholar
  22. Miller, S. L. and Orgel, L. E.: 1974, The Origins of Life on the Earth, Prentice-Hall, Englewood Cliffs, NJ, U.S.A.Google Scholar
  23. Pace, N. R.: 1991, 'Origin of life – Facing up to the physical setting', Cell 65, 531-533.Google Scholar
  24. Paget, E., Jocteur Monrozier, L. and Simonet, P.: 1992, 'Adsorption of DNA on clay minerals: Protection against DNase I and influence on gene transfer', FEMS Microb. Lett. 15, 31-40.Google Scholar
  25. Pietramellara, G., Franchi, M., Gallori, E. and Nannipieri, P.: 2001, 'Effect of molecular characteristics of DNA on its adsorption and binding on homoionic montmorillonite and kaolinite', Biol. Fertil. Soils 33, 402-409.Google Scholar
  26. Pitsch, S., Eschenmoser, A., Gedulin, B., Hui, S. and Arrhenius, G.: 1995, 'Mineral induced formation of sugar phosphates', Orig. Life Evol. Biosphere 25, 297-334.Google Scholar
  27. Rao, M., Odom, D.G. and Orò, J.: 1980, 'Clays in prebiological chemistry', J. Mol. Evol. 15, 317-331.Google Scholar
  28. Risphon, J., O'Hara, P. J., Lahav, N. and Lawless, J. G.: 1982, 'Interaction between ATP, metal ions glycine, and several minerals', J. Mol. Evol. 18, 179-184.Google Scholar
  29. Saenger, W.: 1983, Principles of Nucleic Acids Structure, Springer-Verlag, New York.Google Scholar
  30. Sambrook, J., Fritsch, E. F. and Maniatis, T.: 1989, Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Press, New York.Google Scholar
  31. Smith, J. V.: 1998, 'Biochemical evolution. I. Polymerization on internal, organophilic silica surfaces of dealuminated zeolites and feldspars', Proc. Natl. Acad. Sci. USA 95, 3370-3375.Google Scholar
  32. Smith, J. V., Frederick Jr., P. A., Parsons, I. and Lee, M. R.: 1999, 'Biochemical evolution. III. Polymerization on organophilic silica-rich surfaces, crystal-chemical modeling, formation of first cells, and geological clues', Proc. Natl. Acad. Sci. USA 96, 3479-3485.Google Scholar
  33. Theng, B. K. G.: 1982, 'Clay-polymer interactions: Summary and perspectives', Clays Clay Miner. 30, 1-10.Google Scholar
  34. Theng, B. K. G. and Orchard, V. A.: 1995, 'Interactions of Clays with Microorganisms and Bacterial Survival in Soil: A Physicochemical Perspective', in P. M. Huang, J. Berthelin, J. M. Bollag, W. B. McGill and A. L. Page (eds), Environmental Impact of Soil Components Interactions, CRC Press Inc., London, U.K., pp. 123-143.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  1. 1.Department of Animal Biology and GeneticsUniversity of FlorenceItaly
  2. 2.NY Center for Studies on the Origins of Life and Department of ChemistryRensselaer Polytechnic InstituteTroyU.S.A

Personalised recommendations