Journal of Molecular Evolution

, Volume 57, Supplement 1, pp S182–S189 | Cite as

An Overlooked Riddle of Life’s Origins: Energy-Dependent Nucleic Acid Unzipping

  • Ladislav Kováč
  • Jozef Nosek
  • L’ubomír Tomáška


The imposing progress in understanding contemporary life forms on Earth and in manipulating them has not been matched by a comparable progress in understanding the origins of life. This paper argues that a crucial problem of unzipping of the double helix molecule of nucleic acid during its replication has been underrated, if not plainly overlooked, in the theories of life’s origin and evolution. A model is presented of how evolution may have solved the problem in its early phase. Similar to several previous models, the model envisages the existence of a protocell, in which osmotic disbalance is being created by accumulation of synthetic products resulting in expansion and division of the protocell. Novel in the model is the presence in the protocell of a double-stranded nucleic acid, with each of its two strands being affixed by its 3′-terminus to the opposite sides of the membrane of a protocell. In the course of the protocell expansion, osmotic force is utilized to pull the two strands longitudinally in opposite directions, unzipping the helix and partitioning the strands between the two daughter protocells. The model is also being used as a background for arguments of why life need operate in cycles. Many formal models of life’s origin and evolution have not taken into account the fact that logical possibility does not equal thermodynamic feasibility. A system of self-replication has to consist of both replicators and replicants.


Double-helix unwinding Helicase Life’s origin Osmotic force Protocell Replicant Replicator 


  1. 1.
    Allen, G 1970Natural selection and the origin of life.Persp Biol Med14109126Google Scholar
  2. 2.
    Anderson, PW 1983Suggested model for prebiotic evolution: The use of chaos.Proc Natl Acad Sci USA8033863390PubMedGoogle Scholar
  3. 3.
    Atlan, H 1999La fin de “tout génetique”? Vers de nouveaux paradigmes en biologie.INRAParis54Google Scholar
  4. 4.
    Bachmann, PA, Luisi, PL, Lang, J 1992Autocatalytic self-replicating micelles as models for prebiotic structures.Nature3575759Google Scholar
  5. 5.
    Bockelmann, U, Thomen, Ph, Essavaz-Roulet, B, Vlasnoff, V, Heslot, F 2002Unzipping DNA with optical tweezers: High sequence sensitivity and force flips.Biophys J8215371553PubMedGoogle Scholar
  6. 6.
    Boland, T, Ratner, BD 1995Direct measurement of hydrogen bonding in DNA nucleotide bases by atomic force microscopy.Proc Natl Acad Sci USA9252975301PubMedGoogle Scholar
  7. 7.
    Borowiec, JA 1996

    DNA helicases.

    DNA replication in eukaryotic cells.Cold Spring Harbor Laboratory PressCold Spring Harbor, NY
    Google Scholar
  8. 8.
    Cavalier-Smith, T 1987The origin of cells: A symbiosis between genes, catalysts, and membranes.Cold Spring Harb Symp Quant Biol52805823PubMedGoogle Scholar
  9. 9.
    Chadwick AV (2001) Abiogenic origin of life: A theory in crisis.
  10. 10.
    Deamer, DW 1997The first living systems: A bioenergetic perspective.Microbiol Mol Biol Rev61239261PubMedGoogle Scholar
  11. 11.
    De Duve, C 1991Blueprint for a cell: The nature and origin of life.PattersonBurlingtonGoogle Scholar
  12. 12.
    Delbrück, M 1978

    Mind from matter.

    Heidcamp, WH eds. Nature of life.University Park PressBaltimore147
    Google Scholar
  13. 13.
    Dover, G 1999Looping the evolutionary loop.Nature399217218CrossRefGoogle Scholar
  14. 14.
    Dworkin, JP, Deamer, DW, Sandford, SA, Allamandola, LJ 2001Self-assembling amphiphilic molecules: Synthesis in simulated interstellar/precomentary ices.Proc Natl Acad Sci USA98815819CrossRefPubMedGoogle Scholar
  15. 15.
    Dyson, F 1999Origins of life, 2nd ed.Cambridge University PressCambridgeGoogle Scholar
  16. 16.
    Egelman, EH 2001Pumping DNA.Nature409573574CrossRefPubMedGoogle Scholar
  17. 17.
    Essevaz-Roulet, B, Bockelmann, U, Heslot, F 1997Mechanical separation of the complementary strands of DNA.Proc Natl Acad Sci USA941193511940CrossRefPubMedGoogle Scholar
  18. 18.
    Fenn, JB 1982Engines, energy and entropy.FreemanNew YorkGoogle Scholar
  19. 19.
    Fontana, W, Schuster, P 1998Continuity in evolution: On the nature of transitions.Science28014511455CrossRefPubMedGoogle Scholar
  20. 20.
    Forst, CV 1998Molecular evolution: A theory approaches experiments.J Biotechnol64101118CrossRefGoogle Scholar
  21. 21.
    Ghiselin, MT 1987Replicators and replicanda. Bioeconomics and the metaphysics of selection.J Soc Biol Struct10361369Google Scholar
  22. 22.
    Guatelli, JC, Whitfield, KM, Kwon, DY, Barringer, KJ, Richman, DD, Gingeras, TR 1990Isothermal, in vitro amplification of nucleic acids by a multienzyme reaction modeled after retroviral replication.Proc Natl Acad Sci USA8718741878PubMedGoogle Scholar
  23. 23.
    Johnston, WK, Unrau, PJ, Lawrence, MS, Glasner, ME, Bartel, DP 2001RNA-catalyzed RNA polymerization: Accurate and general RNA-templated primer extension.Science29213191325PubMedGoogle Scholar
  24. 24.
    Joyce, GF 1989RNA evolution and the origin of life.Nature338217224CrossRefPubMedGoogle Scholar
  25. 25.
    Kauffman, SA 1993The origin of order. Self-organization and selection in evolution.Oxford University PressNew YorkGoogle Scholar
  26. 26.
    Koch, AL 1985Primeval cells: Possible energy-generating and cell-division mechanisms.J Mol Evol21270277Google Scholar
  27. 27.
    Kornberg, A, Baker, TA 1992DNA replication.FreemanNew YorkGoogle Scholar
  28. 28.
    Kuhn, H 1972Selbstorganisation molekularer Systeme und die Evolution des genetischen Apparats.Angew Chem84838862PubMedGoogle Scholar
  29. 29.
    Kuhn, H 1988Origin of life and physics: Diversified macrostructure—Inducement to form information-carrying and knowledge-accumulating systems.J Res Dev323746Google Scholar
  30. 30.
    Lahav, N 1999Biogenesis: Theories of life’s origin.Oxford University PressOxfordGoogle Scholar
  31. 31.
    Langton, CG, Taylor, C, Farmer, JD, Rasmussen, S 1992Artificial life II.Addison–WesleyRedwood City, CAGoogle Scholar
  32. 32.
    Lee, DH, Granja, JR, Martinez, JA, Severin, K, Ghadiri, MR 1996A self-replicating peptide.Nature382525528CrossRefPubMedGoogle Scholar
  33. 33.
    Lee, DH, Severin, K, Ghadiri, MR 1997Autocatalytic networks: The transition from molecular self-replication to molecular ecosystems.Curr Opin Chem Biol1491496CrossRefPubMedGoogle Scholar
  34. 34.
    Lee, GU, Chrisey, LA, Colton, RJ 1994Direct measurement of the forces between complementary strands of DNA.Science266771773PubMedGoogle Scholar
  35. 35.
    Lewontin, R 1992The dream of the human genome.NY Rev Books28 March3140Google Scholar
  36. 36.
    Maizels, N, Weiner, AM 1994Phylogeny from function: Evidence from the molecular fossil record that tRNA originated in replication, not translation.Proc Natl Acad Sci USA9167296734PubMedGoogle Scholar
  37. 37.
    Maynard Smith, J 1990Models of a dual inheritance system.J Theor Biol1434153PubMedGoogle Scholar
  38. 38.
    Maynard Smith, J, Szathmáry, E 1995The major transitions in evolution.FreemanNew YorkGoogle Scholar
  39. 39.
    Morowitz, HJ, Heinz, B, Deamer, DW 1988The chemical logic of a minimum protocell.Orig Life Evol Biosphere18281287Google Scholar
  40. 40.
    Orgel, LE 1998The origin of life — a review of facts and speculations.Trends Biochem Sci23491495CrossRefPubMedGoogle Scholar
  41. 41.
    Pohorille, A, Chipot, C, New, MH, Wilson, MA 1996Molecular modeling of protocellular functions.Proc Symp Biocomput1996550569Google Scholar
  42. 42.
    Poole, AM, Jeffares, DC, Penny, D 1998The path from the RNA world.J Mol Evol46117PubMedGoogle Scholar
  43. 43.
    Poyton, RO 1983Memory and membranes: The expression of genetic and spatial memory during the assembly of organelle microcompartments.Modern Cell Biol21572Google Scholar
  44. 44.
    Rief, MH, Clausen-Schaumann, H, Gaub, HE 1999Sequence-dependent mechanics of single DNA molecules.Nature Struct Biol6346349CrossRefGoogle Scholar
  45. 45.
    Root-Bernstein, RS, Dillon, PF 1997Molecular complementarity I: The complementarity theory of the origin and evolution of life.J Theor Biol188447479CrossRefPubMedGoogle Scholar
  46. 46.
    Segré, D, Ben-Eli, D, Deamer, DW, Lancet, D 2001The lipid world.Orig Life Evol Biosphere31119145CrossRefGoogle Scholar
  47. 47.
    Shapiro, R 1986Origins: A skeptic’s guide to the creation of life on Earth.Simon & SchusterNew YorkGoogle Scholar
  48. 48.
    Szostak, JW, Bartel, DP, Luisi, PL 2001Synthesizing life.Nature409387390CrossRefGoogle Scholar
  49. 49.
    Tahirov, TH, Temiakov, D, Anikin, M, Patian, V, McAllister, WT, Vassylyev, DG, Yokoyama, S 2002Structure of a T7 RNA polymerase elongation complex at 2.9 Å resolution.Nature4204350CrossRefPubMedGoogle Scholar
  50. 50.
    Taylor, C, Jefferson, D 1994Artificial life as a tool for biological inquiry.Artificial Life1113Google Scholar
  51. 51.
    Thaxton, CB, Bradley, WL, Olsen, RL 1992The mystery of life origin.Lewis and StanleyDallasGoogle Scholar
  52. 52.
    Vaneechoutte M (1988) The replicator: A misnomer. Conceptual implications for genetics ad memetics.
  53. 53.
    Van Nimwegen, E, Crutchfield, JP, Huynen, M 1999Neutral evolution of mutational robustness.Proc Natl Acad Sci USA9697169720CrossRefPubMedGoogle Scholar
  54. 54.
    Von Hippel, PH, Delagoutte, E 2001A general model for nucleic acid helicases and their “coupling” within macromolecular machines.Cell104177119PubMedGoogle Scholar
  55. 55.
    Von Kiedrowski, G 1986A self-replicating hexadeoxynucleotide.Angew Chem Int Ed Engl25932934CrossRefGoogle Scholar
  56. 56.
    Von Neumann, J 1966The theory of self-reproducing automata.University of Illinois PressUrbanaGoogle Scholar
  57. 57.
    Wächtershäuser, G 1990Evolution of the first metabolic cycles.Proc Natl Acad Sci USA87200204Google Scholar
  58. 58.
    Walde, P, Wick, R, Fresta, M, Mangone, A, Luisi, PL 1994Autopoietic self-reproduction of fatty acid vesicles.J Am Chem Soc1161164911654Google Scholar
  59. 59.
    Wilson, TH, Lin, ECC 1980Evolution of membrane bioenergetics.J Supramol Struct1342l446Google Scholar
  60. 60.
    Winter, EA, Rebek Jr, J 1996Autocatalysis and the generation of self-replicating systems.Acta Chim Scand50469485Google Scholar
  61. 61.
    Weiss, A 1981Replication and evolution in inorganic systems.Angew Chem Int Ed Engl20850860CrossRefGoogle Scholar
  62. 62.
    Wills, C, Bada, J 2000The spark of life: Darwin and the primeval soup.PerseusCambridge, MAGoogle Scholar
  63. 63.
    Woese, C 1998The universal ancestor.Proc Nat Acad Sci USA9568546859CrossRefPubMedGoogle Scholar
  64. 64.
    Woese, CR 2002On the evolution of cells.Proc Nat Acad Sci USA9987428747PubMedGoogle Scholar
  65. 65.
    Yanagawa, H, Ogawa, Y, Kojima, K, Ito, M 1988Construction of protocellular structures under simulated primitive earth conditions.Orig Life Evol Biosphere18179207Google Scholar

Copyright information

© Springer-Verlag New York LLC 2003

Authors and Affiliations

  • Ladislav Kováč
    • 1
  • Jozef Nosek
    • 1
  • L’ubomír Tomáška
    • 1
  1. 1.Departments of Biochemistry and GeneticsComenius University, Mlynská dolina, 842 15 BratislavaSlovakia

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