Origins of Life and Evolution of Biospheres

, Volume 39, Issue 6, pp 545–558 | Cite as

Protein-mediated Selective Enclosure of Early Replicators Inside of Membranous Vesicles: First Step Towards Cell Membranes

Hypothesis

Abstract

Containment in cell membranes is essential for all contemporary life, and apparently even the earliest life forms had to be somehow contained. It has been postulated that random enclosure of replicating molecules inside of spontaneously assembled vesicles would have formed the initial cellular ancestors. However, completely random re-formation or division of such primitive vesicles would have abolished the heritability of their contents, nullifying any selective advantage to them. We propose that the containment of the early replicators in membranous vesicles was adopted only after the invention of genetically encoded proteins, and that selective enclosure of target molecules was mediated by specific proteins. A similar containment process is still utilised by various RNA- and retroviruses to isolate their replication complexes from the host’s intracellular environment. Such selective encapsulation would have protected the replicators against competitor and parasitic sequences, and provided a strong positive selection within the replicator communities.

Keywords

Origin of life Amphiphiles Fatty acids Vesicles Selective encapsulation Defence against parasitic sequences 

Notes

Acknowledgements

We wish to thank the anonymous referee for his very profound questions and suggestions, which have essentially helped to clarify and focus this manuscript.

References

  1. Ahlquist P (2006) Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses. Nature Rev Microbiol 4:371382CrossRefGoogle Scholar
  2. Apel CL, Deamer DW (2005) The formation of glycerol monodecanoate by a dehydration/condensation reaction: increasing the chemical complexity of amphiphiles on the early Earth. Orig Life Evol Biosph 35:323–332CrossRefPubMedGoogle Scholar
  3. Apel CL, Deamer DW, Mautner MN (2002) Self-assembled vesicles of monocarboxylic acids and alcohols: conditions for stability and for the encapsulation of biopolymers. Biochim Biophys Acta 1559:1–9CrossRefPubMedGoogle Scholar
  4. Ariga K, Yuki H, Kikuchi J, Dannemuller O, Albrecht-Gary A, Nakatani Y, Ourisson G (2005) Monolayer studies of single-chain polyprenyl phosphates. Langmuir 21:4578–4583CrossRefPubMedGoogle Scholar
  5. Baross JA, Hoffman SE (1983) Submarina hydrothermal vents and associated gradient environments as sites for the origin and evolution of life. Orig Life 15:327–345Google Scholar
  6. Biebricher CK, Eigen M (2005) The error threshold. Virus Res 107:117–127CrossRefPubMedGoogle Scholar
  7. Braun D, Goddart NL, Libchaber A (2003) Exponential DNA replication by laminar convection. Phys Rev Lett 91:158103CrossRefPubMedGoogle Scholar
  8. Chakrabarti AC, Breaker RR, Joyce GF, Deamer DW (1994) Production of RNA by a polymerase protein encapsulated within phospholipid vesicles. J Mol Evol 39:555–559CrossRefPubMedGoogle Scholar
  9. Chen IA, Szostak JW (2004a) Membrane growth can generate a transmembrane pH gradient in fatty acid vesicles. Proc Natl Acad Sci 101:7965–7970CrossRefPubMedGoogle Scholar
  10. Chen IA, Szostak JW (2004b) A kinetic study of the growth of fatty acid vesicles. Biophys J 87:988–998CrossRefPubMedGoogle Scholar
  11. Chen IA, Roberts RW, Szostak JW (2004) The emergence of competition between model protocells. Science 305:1474–1476CrossRefPubMedGoogle Scholar
  12. Chyba CF, Sagan C (1992) Endogenous production, exogenous delivery and impact-shock synthesis of organic molecules: an inventory for the origin of life. Nature 355:125–1331CrossRefPubMedGoogle Scholar
  13. Deamer DW (1997) The first living systems: a bioenergetic perspective. Microbiol Mol Biol Rev 61:239–261PubMedGoogle Scholar
  14. Deamer DW (1998) Membrane compartments in prebiotic evolution. In: Brack A (ed) The molecular origins of life: assembling the pieces of the puzzle. Cambridge University Press, Cambridge, UK, pp 189–205CrossRefGoogle Scholar
  15. Deamer DW, Oró J (1980) Role of lipids in prebiotic structures. BioSystems 12:167–175CrossRefPubMedGoogle Scholar
  16. Deamer DW, Dworkin JP, Sandford SA, Berstein MP, Allamandola LJ (2002) The first cell membranes. Astrobiology 2:371–381CrossRefPubMedGoogle Scholar
  17. Delsemme AH (1998) Cosmic origin of the biosphere. In: Andre B (ed) The molecular origins of life: assembling the pieces of the puzzle. Cambridge University Press, Cambridge, UK, pp 100–118CrossRefGoogle Scholar
  18. Dworkin JP, Deamer DW, Sandford SA, Allamandola LJ (2001) Self-assembling amphiphilic molecules: synthesis in simulated interstellar/precometary ices. Proc Natl Acad Sci USA 98:815–819CrossRefPubMedGoogle Scholar
  19. Eigen M (1993) The origin of genetic information: viruses as models. Gene 135:37–47CrossRefPubMedGoogle Scholar
  20. Ferris JP (2002) Montmorillonite catalysis of 30–50 mer oligonucleotides: Laboratory demonstration of potential steps in the origin of the RNA world. Orig Life Evol Biosph 32:311–332CrossRefPubMedGoogle Scholar
  21. Furuuchi R, Imai EI, Honda H, Hatori K, Matsuno K (2005) Evolving lipid vesicles in prebiotic hydrothermal environments. Orig Life Evol Biosph 35:333–343CrossRefPubMedGoogle Scholar
  22. Hanczyc MM, Szostak JW (2004) Replicating vesicles as models of primitive cell growth and division. Curr Opin Chem Biol 8:660–664CrossRefPubMedGoogle Scholar
  23. Hanczyc MM, Fujikawa SM, Szostak JW (2003) Experimental models of primitive cellular compartments: encapsulation, growth, and division. Science 302:618CrossRefPubMedGoogle Scholar
  24. Hanczyc MM, Mansy SS, Szostak JW (2006) Mineral surface directed membrane assembly. Orig Life Evol Biosph 37:67–82CrossRefPubMedGoogle Scholar
  25. Hargreaves WR, Deamer DW (1978) Liposomes from ionic, single-chain amphiphiles. Biochem 17:3759–3768CrossRefGoogle Scholar
  26. Hazen RM, Deamer DW (2007) Hydrothermal reactions of pyruvic acid: synthesis, selection, and self assembly of amphiphilic molecules. Orig Life Evol Biosph 37:143–152CrossRefPubMedGoogle Scholar
  27. Hitz T, Luisi PL (2001) Liposome-assisted selective polycondensation of α-amino acids and peptides. Biopolymers 55:381–390CrossRefPubMedGoogle Scholar
  28. Joyce GF (2002) The antiquity of RNA-based evolution. Nature 418:214–221CrossRefPubMedGoogle Scholar
  29. Koonin EV, Martin W (2005) On the origin of genomes and cells within inorganic compartments. Trends Genet 21:647–654CrossRefPubMedGoogle Scholar
  30. Koonin EV, Senkevich TG, Dolja V (2006) The ancient viral world and evolution of cells. Biol Direct 1:29CrossRefPubMedGoogle Scholar
  31. Koonin EV, Wolf YI, Nagasaki K, Dolja VI (2008) A Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nature Rev Microbiol 6:925–939CrossRefGoogle Scholar
  32. Lee W-M, Ahlquist P (2003) Membrane synthesis, specific lipid requirements, and localized lipid composition changes associated with a positive-strand RNA virus RNA replication protein. J Virol 77:12819–12828CrossRefPubMedGoogle Scholar
  33. Lincoln TA, Joyce GF (2009) Self-sustained replication of an RNA enzyme. Science 323:1229–1232Google Scholar
  34. Mansy SS, Szostak JW (2008) Thermostability of model protocell membranes. Proc Natl Acad Sci USA 105:13351–13355CrossRefPubMedGoogle Scholar
  35. Mansy SS, Schrum JP, Krishnamurthy M, Tobé S, Treco DA, Szostak JW (2008) Template-directed synthesis of a genetic polymer in a model protocell. Nature 454:122–125CrossRefPubMedGoogle Scholar
  36. Martin W, Russell MJ (2003) On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Phil Trans R Soc Lond B 358:59–83CrossRefGoogle Scholar
  37. Monnard P-A, Deamer DW (2002) Membrane self-assembly processes: steps toward the first cellular life. Anat Rec 268:197CrossRefGoogle Scholar
  38. Monnard P-A, Deamer DW (2003) Preparation of vesicles from nonphospholipid amphiphiles. Methods Enzymol 372:133–151CrossRefPubMedGoogle Scholar
  39. Monnard P-A, Apel CL, Kanavarioti A, Deamer DW (2002) Influence of ionic inorganic solutes on selfassembly and polymerization processes related to early forms of life: implications for a prebiotic aqueous medium. Astrobiol 2:139–152CrossRefGoogle Scholar
  40. Morowitz HJ, Heinz B, Deamer DW (1988) The chemical logic of a minimum protocell. Orig Life Evol Biosph 18:281–287CrossRefPubMedGoogle Scholar
  41. Mulkidjanian AY, Galperin MY, Koonin EV (2009) Co-evolution of primordial membranes and membrane proteins. Trends Biochem Sci 34:206–215CrossRefPubMedGoogle Scholar
  42. Namani T, Deamer DW (2008) Stability of model membranes in extreme environments. Orig Life Evol Biosph 38:329–341CrossRefPubMedGoogle Scholar
  43. Noireaux V, Libchaber AA (2004) Vesicle bioreactor as a step toward an artificial cell assembly. Proc Nat Acad Sci USA 101:17669–17674CrossRefPubMedGoogle Scholar
  44. Nomura SM, Yoshikawa Y, Yoshikawa K, Dannenmuller O, Chasserot-Golaz S, Ourrisson G, Nakatani Y (2001) Towards proto-cells: “primitive” lipid vesicles encapsulating giant DNA and its histone complex. Chem Biochem 6:457–459Google Scholar
  45. Ourrisson G, Nakatani Y (1999) Origins of cellular life: molecular foundations and new approaches. Tetrahedron 55:3183–3190CrossRefGoogle Scholar
  46. Paula S, Volkov G, Van Hoek AN, Haines TH, Deamer DW (1996) Permeation of protons, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness. Biophys J 70:339–348CrossRefPubMedGoogle Scholar
  47. Pereto J, Lopez-Garcıa P, Moreira D (2004) Ancestral lipid biosynthesis and early membrane evolution. Trends Biochem Sci 29:469–477CrossRefPubMedGoogle Scholar
  48. Pietrini AV, Luisi PL (2004) Cell-free protein synthesis through solubilisate exchange in water/oil emulsion compartments. ChemBioChem 5:1055–1062CrossRefPubMedGoogle Scholar
  49. Pohorille A, Schweighofer K, Wilson MA (2005) The origin and early evolution of membrane channels. Astrobiology 5:1–17CrossRefPubMedGoogle Scholar
  50. Poole AM, Jeffares D, Penny D (1998) The path from the RNA world. J Mol Evol 46:1–17CrossRefPubMedGoogle Scholar
  51. Poole A, Penny D, Sjöberg BM (2000) Methyl-RNA: an evolutionary bridge between RNA and DNA? Chem Biol 7:R207–R216CrossRefPubMedGoogle Scholar
  52. Rao M, Eichberg J, Oró J (1982) Synthesis of phosphatidylcholine under possible primitive Earth conditions. J Mol Evol 18:196–202CrossRefPubMedGoogle Scholar
  53. Rao M, Eichberg J, Oró J (1987) Synthesis of phosphatidyethanolamine under possible primitive Earth conditions. J Mol Evol 25:1–6CrossRefPubMedGoogle Scholar
  54. Rushdi AI, Simoneit BRT (2001) Lipid formation by aqueous Fischer–Tropsch-type synthesis over a temperature range of 100 to 400°C. Orig Life Evol Biosph 31:103–118CrossRefPubMedGoogle Scholar
  55. Rushdi AI, Simoneit BRT (2006) Abiotic condensation synthesis of glyceride lipids and wax esters under simulated hydrothermal conditions. Orig Life Evol Biosph 36:93–108CrossRefPubMedGoogle Scholar
  56. Sacerdote MG, Szostak JW (2005) Semipermeable lipid bilayers exhibit diastereoselectivity favoring ribose. Proc Natl Acad Sci 102:6004–6008CrossRefPubMedGoogle Scholar
  57. Schwartz M, Cheng J, Janda M, Sullivan M, den Boon J, Ahlquist P (2002) A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol Cell 9:505–514CrossRefPubMedGoogle Scholar
  58. Schwartz M, Cheng J, Lee W-M, Janda M, Ahlquist P (2004) Alternate, virus-induced membrane rearrangements support positive-strand virus genome replication. Proc Natl Acad Sci USA 101:11263–11268CrossRefPubMedGoogle Scholar
  59. Segré D, Ben-Eli D, Lancet D (2000) Compositional genomes: prebiotic information transfer in mutually catalytic non-covalent assemblies. Proc Natl Acad Sci USA 97:4112–4117CrossRefPubMedGoogle Scholar
  60. Segré D, Ben-Eli D, Deamer D, Lancet D (2001) The lipid world. Orig Life Evol Biosph 31:119–145CrossRefPubMedGoogle Scholar
  61. Spuul P, Salonen A, Merits A, Jokitalo E, Kääriäinen L, Ahola T (2007) Role of the amphiphilic peptide of Semliki Forest virus replicase protein nsP1 in membrane association and virus replication. J Virol 81:872–883CrossRefPubMedGoogle Scholar
  62. Stephan T, Jessberger EK, Heiss CH, Ross D (2003) TOF-SIMS analysis of Polycyclic aromatic hydrocarbons in Alan Hills 84001. Meteorit Plant Sci 38:109–116CrossRefGoogle Scholar
  63. Sunami T, Sato K, Matsuura T, Tsukada K, Urabe I, Yomo T (2006) Femtoliter compartment in liposomes for in vitro selection of proteins. Anal Biochem 357:128–136CrossRefPubMedGoogle Scholar
  64. Szathmary E, Maynard Smith JM (1997) From replicators to reproducers: the first major transitions leading to life. J Theor Biol 187:555–571CrossRefPubMedGoogle Scholar
  65. Szostak JW, Bartel DP, Luisi PL (2001) Synthesizing life. Nature 409:387–390CrossRefPubMedGoogle Scholar
  66. Taylor WR (2006) A molecular model for the origin of protein translation in an RNA world. J Theor Biol 243:393–406CrossRefPubMedGoogle Scholar
  67. Thomas JA, Rana FR (2007) The influence of environmental conditions, lipid composition, and phase behavior on the origin of cell membranes. Orig Life Evol Biosph 37:267–285CrossRefPubMedGoogle Scholar
  68. Vetsigian K, Woese C, Goldenfeld N (2006) Collective evolution and the genetic code. Proc Natl Acad Sci USA 103:10696–10701CrossRefPubMedGoogle Scholar
  69. Woese CR (1998) The universal ancestor. Proc Natl Acad Sci USA 95:6854–6859CrossRefPubMedGoogle Scholar
  70. Woese CR (2002) On the evolution of cells. Proc Natl Acad Sci USA 99:8742–8747CrossRefPubMedGoogle Scholar
  71. Zhang B, Cech TR (1997) Peptide bond formation by in vitro selected ribozymes. Nature 390:96–100CrossRefPubMedGoogle Scholar
  72. Zubay G (2000) Orgins of life on the earth and in the cosmos, 2nd edn. Academic, San Diego, CA, p 347Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Laboratory of Plant Physiology and Molecular BiologyUniversity of TurkuTurkuFinland

Personalised recommendations