Membrane Self-Assembly Processes: Steps Toward the First Cellular Life

Chapter

Abstract

This review addresses the question of the origin of life, with emphasis on plausible boundary structures that may have initially provided cellular compartmentation. Some form of compartmentation is a necessary prerequisite for maintaining the integrity of interdependent molecular systems that are associated with metabolism, and for permitting variations required for speciation. The fact that lipid-bilayer membranes define boundaries of all contemporary living cells suggests that protocellular compartments were likely to have required similar, self-assembled boundaries. Amphiphiles such as short-chain fatty acids, which were presumably available on the early Earth, can self-assemble into stable vesicles that encapsulate hydrophilic solutes with catalytic activity. Their suspensions in aqueous media have therefore been used to investigate nutrient uptake across simple membranes and encapsulated catalyzed reactions, both of which would be essential processes in protocellular life forms.

References

  1. Apel CL, Mautner MN, Deamer DW (2002) Self-assembled vesicles of monocarboxylic acids and alcohols: conditions for stability and for encapsulation of biopolymers. Biochim Biophys Acta 1559:1–9PubMedGoogle Scholar
  2. Baaske P, Weinert FM, Duhr S, Lemke KH, Russell MJ, Braun D (2007) Extreme accumulation of nucleotides in simulated hydrothermal pore systems. Proc Natl Acad Sci USA 104:9346–9351PubMedGoogle Scholar
  3. Bachmann PA, Luisi PL, Lang J (1992) Autocatalytic self-replicating micelles as models for prebiotic structures. Nature 357:57–59Google Scholar
  4. Bangham AD, Standish MM, Miller N (1965) Diffusion of univalent ions across the lamellae of swollen phospholipids. J Mol Biol 13:238–252PubMedGoogle Scholar
  5. Bernal JD (1951) The physical basis of life. Routledge, LondonGoogle Scholar
  6. Chakrabarti AC, Breaker RR, Joyce GF, Deamer DW (1994) Production of RNA by polymerase protein encapsulated within phospholipid vesicles. J Mol Evol 39:555–559PubMedGoogle Scholar
  7. Chen IA, Roberts RW, Szostak JW (2004) The emergence of competition between model protocells. Science 305:1474–1476PubMedGoogle Scholar
  8. Chen IA, Szostak JW (2004) A kinetic study of the growth of fatty acid vesicles. Biophys J 87:988–998PubMedGoogle Scholar
  9. Clark TD, Buehler LK, Ghadiri MR (1998) Self-assembling cyclic b3-peptide nanotubes as artificial transmembrane ion channels. J Am Chem Soc 120:651–656Google Scholar
  10. Cody GD, Boctor NZ, Filley TR, Hazen RM, Scott JH, Sharma A, Yoder HS Jr (2000) Primordial carbonylated iron-sulfur compounds and synthesis of pyruvate. Science 289:1337–1340PubMedGoogle Scholar
  11. Cronin JR, Pizzarello S, Cruickshank DP (1988) Organic matter in carbonaceous chondrites, planetary satellites, asteroids and comets. In: Matthews MS (ed) Meteorites and the early solar system. University of Arizona Press, Tucson, pp 819–857Google Scholar
  12. Deamer DW, Oro J (1980) Role of lipids in prebiotic structures. Biosystems 12:167–175PubMedGoogle Scholar
  13. Deamer DW, Barchfeld GL (1982) Encapsulation of macromolecules by lipid vesicles under simulated prebiotic conditions. J Mol Evol 18:203–206PubMedGoogle Scholar
  14. Deamer DW (1985) Boundary structures are formed by organic components of the Murchison carbonaceous chondrites. Nature 317:792–794Google Scholar
  15. Deamer DW, Bramhall J (1986) Permeability of lipid bilayers to water and ionic solutes. Chem Phys Lipids 40:167–188PubMedGoogle Scholar
  16. Deamer DW, Pashley RM (1989) Amphiphilic components of the Murchison carbonaceous chondrite: surface properties and membrane formation. Orig Life Evol Biosph 19:21–38PubMedGoogle Scholar
  17. Deamer DW (1992) Polycyclic aromatic hydrocarbons: primitive pigment systems in the prebiotic environment. Adv Space Res 12(4):183–189PubMedGoogle Scholar
  18. Deamer DW, Mahon EH, Bosco G (1994) Self-assembly and function of primitive membrane structures. In: Bengtson S (ed) Early life on earth. Columbia University Press, New York/Chichester/West Sussex, pp 107–123Google Scholar
  19. Deamer DW (1997) The first living systems: a bioenergetic perspective. Microbiol Mol Biol Rev 61:230–261Google Scholar
  20. Deamer DW, Dworkin JP, Sandford SA, Bernstein MP, Allamandola LJ (2002) The first cell membranes. Astrobiology 2:371–382PubMedGoogle Scholar
  21. DeClue MS, Monnard P-A, Bailey JA, Maurer SE, Collis GE, Ziock H-J, Rasmussen S, Boncella JM (2009) Nucleobase mediated, photocatalytic vesicle formation from an ester precursor. J Am Chem Soc 131:931–933PubMedGoogle Scholar
  22. De Rosa M, Trincone A, Nicolaus B, Gambacorta A (1991) Archeabacteria: lipids, membrane structures, and adaptations to environmental stresses. In: Di Prisco G, Federation of European Biochemical Societies. Meeting (eds) Life under extreme conditions: biochemical adaptation, pp vii, 144. Springer, Berlin/New YorkGoogle Scholar
  23. Dobson CM, Ellison GB, Tuck AF, Vaida V (2000) Atmospheric aerosols as prebiotic chemical reactors. Proc Nat Acad Sci USA V97:11864–11868Google Scholar
  24. Ferris JP (1994) The prebiotic synthesis and replication of RNA oligomers: the transition from prebiotic molecules to the RNA world. In: Fleischaker GR (ed) Self-production of supramolecular structures, pp 89–98. Kluwer, DordrechtGoogle Scholar
  25. Ferris JP (1999) Prebiotic synthesis on minerals: bridging the prebiotic and RNA worlds. Biological Bull 196:311–314Google Scholar
  26. Ferris JP, Hill AR Jr, Liu R, Orgel LE (1996) Synthesis of long prebiotic oligomers on mineral surfaces. Nature 381:59–61PubMedGoogle Scholar
  27. Gavino V, Deamer DW (1982) Purification of acyl CoA: 1-acyl-sn-glycerophosphorylcholine acyltrasnferase. J Bioenerg Biomembr 14:513–526PubMedGoogle Scholar
  28. Gebicki JM, Hicks M (1973) Ufasomes are stable particles surrounded by unsaturated fatty acid membranes. Nature 243:232–234PubMedGoogle Scholar
  29. Gebicki JM, Hicks M (1976) Preparation and properties of vesicles enclosed by fatty acid membranes. Chem Phys Lipid 16:142–160Google Scholar
  30. Ghadiri MR, Granja JR, Buehler LK (1994) Artificial transmembrane ion channels from self-assembling peptide nanotubes. Nature 369:301–304PubMedGoogle Scholar
  31. Giese B (2002) Electron transfer in DNA. Curr Opin Chem Biol 6:612–618PubMedGoogle Scholar
  32. Goldacre RJ (1958) Surface films: their collapse on compression, the shapes and sizes of cells, and the origin of life. In: Danielli JF, Pankhurst KGA, Riddiford AC (eds) Surface phenomena in biology and chemistry. Pergamon Press, New York, pp 12–27Google Scholar
  33. Gotoh M, Miki A, Nagano H, Ribeiro N, Elhabiri M, Gumienna-Konteck E, Albrecht-Gary A-M, Schmutz M, Ourisson G, Nakatani Y (2006) Membrane properties of branched polyprenyl phosphates, postulated as primitive membrane constituents. Chem Biodiv 3:434–455Google Scholar
  34. Haines TH (1983) Anionic lipid headgroups as a proton-conducting pathway along the surface of membranes: a hypothesis. Proc Natl Acad Sci USA 80:160–164PubMedGoogle Scholar
  35. Haldane JBS (1929) The origin of life. Rat Ann 148:3–10Google Scholar
  36. Hanczyc MM, Fujikawa SM, Szostak JW (2003) Experimental models of primitive cellular compartments: encapsulation, growth, and division. Science 302:618–622PubMedGoogle Scholar
  37. Hanczyc MM, Szostak JW (2004) Replicating vesicles as models of primitive cell growth and division. Curr Opin Chem Biol 8:660–664PubMedGoogle Scholar
  38. Hargreaves WR, Mulvihill SJ, Deamer DW (1977) Synthesis of phophosplipids and membranes in prebiotic conditions. Nature 266:78–80PubMedGoogle Scholar
  39. Hargreaves WR, Deamer DW (1978) Liposomes from ionic, single-chain amphiphiles. Biochemistry 17:3759–3768PubMedGoogle Scholar
  40. Johnston WK, Unrau PJ, Lawrence MS, Glasner ME, Bartel DP (2001) RNA-catalyzed RNA polymerization: accurate and general RNA-templated primer extension. Science 292:1319–1325PubMedGoogle Scholar
  41. Joyce GF (1998) Nucleic acid enzymes: playing with a fuller deck. Proc Natl Acad Sci USA 95:5845–5847PubMedGoogle Scholar
  42. Kagen P, Cech TR, Golden BL (1999) Building a catalytic active site using only RNA. In: Atkins JF (ed) The RNA world, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 321–349Google Scholar
  43. Kanehisa MI, Tsong TY (1978) Cluster model of lipid phase transition with application to passive permeation of molecules and structures relaxations in lipid bilayers. J Am Chem Soc 100:424–432Google Scholar
  44. Khvorova A, Kwak Y-G, Tamkun M, Majerfeld I, Yarus M (1999) RNAs that bind and change the permeability of phospholipid membranes. Proc Nat Acad Sci USA 96:10649–10654Google Scholar
  45. Kim HS, Hartgerink JD, Ghadiri MR (1998) Oriented self-assembly of cyclic peptide nanotubes in lipid membranes. J Am Chem Soc V120:4417–4424Google Scholar
  46. Kita H, Matsuura T, Sunami T, Hosoda K, Ichihashi N, Tsukada K, Urabe I, Yomo T (2008) Replication of genetic information with self-encoded replicase in liposomes. Chem Bio Chem 9:2403–2410PubMedGoogle Scholar
  47. Knauth LP (2005) Temperature and salinity history of Precambrian ocean: implications for the course of microbial evolution. Palaeogeogr Palaeoclimatol Palaeoecol 219:53–69Google Scholar
  48. Komiya M, Shimoyama A, Harada K (1993) Examination of organic compounds from insoluble organic matter isolated from some Antarctic carbonaceous chondrites by heating experiments. Geochim Cosmochim Acta 57:907–914Google Scholar
  49. Kuruma Y, Stano P, Ueda T, Luisi PL (2009) A synthetic biology approach to the construction of membrane proteins in semi-synthetic minimal cells. Biochim Biophys Acta 1788:567–574PubMedGoogle Scholar
  50. Kvenvolden KA, Lawless J, Pering K, Peterson E, Flores J, Ponnamperuma C, Kaplan IR, Moore C (1970) Evidence for extraterrestrial amino acids and hydrocarbons in the Murchison meteorite. Nature 228:923–926PubMedGoogle Scholar
  51. Langner M, Hui SW (1993) Dithionite penetration through phospholipid bilayers as a measure of defects in lipid molecular packing. Chem Phys Lipids 65:23–30PubMedGoogle Scholar
  52. Lawless JG, Yuen GU (1979) Quantitation of monocarboxylic acids in the Murchison carbonaceous meteorite. Nature 282:431–454Google Scholar
  53. Lazcano A (1994a) The transition from nonliving too living. In: Bengtson S (ed) Early life on earth. Columbia University Press, New York/Chichester/West Sussex, pp 60–69Google Scholar
  54. Lazcano A (1994b) The RNA world, its predecessors, and its descendants. In: Bengtson S (ed) Early life on earth. Columbia University Press, New York/Chichester/West Sussex, pp 70–80Google Scholar
  55. Luisi PL, Varela FJ (1989) Self-replicating micelles - a chemical version of a minimal autopoietic system. Orig Life Evol Biosph 19:633–643Google Scholar
  56. Luisi PL, Walde P, Oberholzer T (1999) Lipid vesicles as possible intermediates in the origin of life. Curr Opin Colloid Interface Sci 4:33–38Google Scholar
  57. Luisi PL (2006) The emergence of life: from chemical origins to synthetic biology. Cambridge University Press, CambridgeGoogle Scholar
  58. 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 454:122–125PubMedGoogle Scholar
  59. Mansy SS, Szostak JW (2008) Thermostability of model protocell membranes. Proc Natl Acad Sci 105:13351–13355PubMedGoogle Scholar
  60. 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. Philos Trans R Soc Lond B Biol Sci 358:59–83PubMedGoogle Scholar
  61. Maurer SE, Deamer DW, Boncella JM, Monnard PA (2009) Chemical evolution of amphiphiles: glycerol monoacyl derivatives stabilize plausible prebiotic membranes. Astrobiology (in press)Google Scholar
  62. Mautner M, Leonard RL, Deamer DW (1995) Meteorite organics in planetary environments: hydrothermal release, surface activity and microbial utilization. Planetary Space Sci 43:139–147Google Scholar
  63. McCollom TM, Ritter G, Simoneit BRT (1999) Lipid synthesis under hydrothermal conditions by Fischer-Tropsch-type reactions. Orig Life Evol Biosph 29:153–166PubMedGoogle Scholar
  64. McKay DB, Wedekind JE (1999) Small ribozymes. In: Atkins JF (ed) The RNA world, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 265–286Google Scholar
  65. Miller SL (1953) Production of amino acids under possible primitive Earth conditions. Science 117:528–529PubMedGoogle Scholar
  66. Monnard P-A, Oberholzer T, Luisi PL (1997) Encapsulation of polynucleotides in liposomes. Biochim Biophys Acta 1329:39–50PubMedGoogle Scholar
  67. Monnard P-A, Deamer DW (2001) Nutrient uptake by protocells: a liposome model system. Orig Life Evol Biosph 31:147–155PubMedGoogle Scholar
  68. Monnard P-A, Apel CL, Kanavarioti A, Deamer DW (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 2:139–152PubMedGoogle Scholar
  69. Monnard P-A, Luptak A, Deamer DW (2007) Models of primitive cellular life: polymerases and templates in liposomes. Philos Trans R Soc B Biol Sci 362:1741–1750Google Scholar
  70. Monnard P-A, Ziock H-J, Declue MS (2008) Organic nano-compartments as biomimetic reactors, and protocells. Curr Nanosci 4:71–87Google Scholar
  71. Morigaki K, Dallavalle S, Walde P, Colonna S, Luisi PL (1997) Autopoietic self-reproduction of chiral fatty acid vesicles. J Am Chem Soc 119:292–301Google Scholar
  72. Morowitz HJ (1992) Beginnings of cellular life. Metabolism recapitulates biogenesis. Yale University Press, New Haven, CTGoogle Scholar
  73. Mouritsen OG, Jorgenseb K, Honger T (1995) Permeability of lipid bilayers near the phase transition. In: Simon SA (ed) Permeability and stability of lipid bilayers. CRC Press, Boca Raton, pp 137–160Google Scholar
  74. Namani T, Deamer DW (2008) Stability of model membranes in extreme environments. Orig Life Evol Biosph 38:329–341PubMedGoogle Scholar
  75. Nomura S-iM, Yoshikawa K, Dannenmuller O, Chasserot-Golaz S, Ourisson G, Nakatani Y. 2001. Towards proto-cells: “Primitive” lipid vesicles encapsulating giant DNA and its histone complex. Chembiochem:457–459.Google Scholar
  76. Oberholzer T, Wick R, Luisi PL, Biebricher CK (1995a) Enzymatic RNA replication in self-reproducing vesicles: an approach to a minimal cell. Biochim Biophys Res Commun 207:250–257Google Scholar
  77. Oberholzer T, Albrizio M, Luisi PL (1995b) Polymerase chain reaction in liposomes. Chem Biol 2:677–682PubMedGoogle Scholar
  78. Oberholzer T, Meyer E, Amato I, Lustig A, Monnard P-A (1999) Enzymatic reactions in liposomes using the detergent-induced liposome loading method. Biochim Biophys Acta 1416:57–68PubMedGoogle Scholar
  79. Oliver AE, Deamer DW (1994) a-Helical hydrophobic polypeptides form proton-selective channels in lipid bilayers. Biophys J 66:1364–1379PubMedGoogle Scholar
  80. Oparin AI (1924) The origin of life. Moscow: Izd. Moskovshii Rabochii. English translation in: J. D. Bernal. 1967. The origin of life, pp 199–234. Weidenfeld and Nicolson, LondonGoogle Scholar
  81. Oparin AI (1957) The origin of life on the earth. Academic Press, New YorkGoogle Scholar
  82. Oparin AI, Orlovskii AF, Bukhlaeva VY, Gladilin KL (1976) Influence of the enzymatic synthesis of polyadenylic acid on a coacervate system. Dokl Akad Nauk SSSR 226:972–974PubMedGoogle Scholar
  83. Oro J, Sherwood E, Eichberg J, Epps D (1978) Formation of phospholipids under primitive earth conditions and roles of membranes in prebiological evolution. In: Deamer DW (ed) Light transducing membranes. Academic Press, London, pp 1–22Google Scholar
  84. Ourisson G, Nakatani Y (1999) Origins of cellular life: molecular foundations and new approaches. Tetrahedron 55:3183–3190Google Scholar
  85. Paula S, Volkov AG, Van Hoek AN, Haines TH, Deamer DW (1996) Permeation of proton, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness. Biophys J 70:339–348PubMedGoogle Scholar
  86. Rasmussen S, Chen L, Nilsson M, Abe S (2003) Bridging nonliving and living matter. Artif Life 9(3):269–316PubMedGoogle Scholar
  87. Rasmussen S, Chen L, Deamer DW, Krakauer DC, Packard NH, Stadler PF, Bedau MA (2004) Evolution. Transitions from nonliving to living matter. Science 303:963–965PubMedGoogle Scholar
  88. Rogers J, Joyce GF (1999) A ribozyme that lacks cytidine. Nature 402:323–325PubMedGoogle Scholar
  89. Rosano HL, Christodolou AP, Feinstein ME (1969) Competition of cations at charged micelle and monolayer interfaces. J Colloid Interface Sci 29:335–344PubMedGoogle Scholar
  90. Rosenquist K, Gabran T, Rydhag L (1981) Studies of permeability across bilayers of lecithin. In: Sfflrat L (ed) 11th Scandinavian symposium on lipids, pp 85–89. Lipidforum, Scandinavian forum for lipid research and technology, Bergen, NorwayGoogle Scholar
  91. Rushdi AI, Simoneit BR (2001) Lipid formation by aqueous Fischer-Tropsch-type synthesis over a temperature range of 100 to 400 degrees C. Orig Life Evol Biosph 31:103–118PubMedGoogle Scholar
  92. Sacerdote MG, Szostak JW (2005) Semi-permeable lipid bilayers exhibit diastereoselectivity favoring ribose; implications for the origins of life. Proc Nat Acad Sci 102:6004–6008PubMedGoogle Scholar
  93. Segre D, Ben-Eli D, Deamer DW, Lancet D (2001) The lipid world. Orig Life Evol Biosph 31:119–145PubMedGoogle Scholar
  94. Shew RL, Deamer DW (1985) A novel method for encapsulation of macromolecules in liposomes. Biochim Biophys Acta 816:1–8PubMedGoogle Scholar
  95. Skurtveit R, Sjoblom J, Hoiland H (1989) Emulsions under elevated-temperature and pressure conditions. 1. The model system water hexadecanoic acid sodium hexadecanoate decane at 70-degrees-C. J Colloid Interf Sci 133:395–403Google Scholar
  96. Streiff S, Ribeiro N, Wu Z, Gumienna-Konteck E, Elhabiri M, Albrecht-Gary A-M, Ourisson G, Nakatani Y (2007) “Primitive” membrane from polyprenyl phosphates and polyprenyl alcohols. Chem Biol 14:313–319PubMedGoogle Scholar
  97. Szostak JW, Bartel DP, Luisi PL (2001) Synthesizing life. Nature 409:387–390PubMedGoogle Scholar
  98. Tawfik DS, Griffiths AD (1998) Man-made cell-like compartments for molecular evolution. Nat Biotech 16:652–656Google Scholar
  99. Varela FJ, Maturana HR, Uribe R (1974) Autopoiesis: the organization of living systems, its characterization and a model. Biosystems 5:287–296Google Scholar
  100. Voytek SB, Joyce GF (2007) Emergence of a fast-reacting ribozyme that is capable of undergoing continuous evolution. Proc Natl Acad Sci 104:15288–15293PubMedGoogle Scholar
  101. Vlassov A, Khvorova A, Yarus M (2001) Binding and disruption of phospholipid bilayers by supramolecular RNA complexes. Proc Nat Acad Sci USA V98:7706–7711Google Scholar
  102. Wächtershäuser G (1988) Before enzyme and template: theory of surface metabolism. Microbiol Rev 52:452–484PubMedGoogle Scholar
  103. Walde P, Goto A, Monnard P-A, Wessicken M, Luisi PL (1994a) Oparin’s reaction revisited: enzymatic synthesis of poly(adenyl acid) in micelles and self-reproducing vesicles. J Am Chem Soc 116:7541–7547Google Scholar
  104. Walde P, Wick R, Fresta M, Mangone A, Luisi PL (1994b) Autopoietic self-reproduction of fatty acid vesicles. J Am Chem Soc 116:11649–11654Google Scholar
  105. Walde P, Ichikawa S (2001) Review. Enzyme inside lipid vesicles: preparation, reactivity and applications. Biomol Eng 18:143–177PubMedGoogle Scholar
  106. Walde P, Wick R, Fresta M, Mangone A, Luisi PL (1994c) Autopoietic self-reproduction of fatty acid vesicles. J Am Chem Soc 116:11649–11654Google Scholar
  107. Wilson TH, Maloney PC (1976) Speculations on the evolution of ion transport mechanisms. Fed Am Soc Exp Biol Proc 35:2174–2179Google Scholar
  108. Woese C (1968) in The Genetic Code. Harper & Row Google Scholar
  109. Zaher HS, Unrau PJ (2007) Selection of an improved RNA polymerase ribozyme with superior extension and fidelity. RNA 13:1017–1026PubMedGoogle Scholar
  110. Zhu TF, Szostak JW (2009) Coupled growth and division of model protocell membranes. J Am Chem Soc 131:5705–5713PubMedGoogle Scholar

Copyright information

© Springer Netherlands 2011

Authors and Affiliations

  1. 1.FLinT Center, Institute for Physics and ChemistryUniversity of Southern DenmarkOdense MDenmark
  2. 2.Department of Biomolecular EngineeringUniversity of California, Santa Cruz (UCSC)Santa CruzUSA

Personalised recommendations