Skip to main content

The Influence of Environmental Conditions, Lipid Composition, and Phase Behavior on the Origin of Cell Membranes

Abstract

At some point in life’s development, membranes formed, providing barriers between the environment and the interior of the ‘cell.’ This paper evaluates the research to date on the prebiotic origin of cell membranes and highlights possible areas of continuing study. A careful review of the literature uncovered unexpected factors that influence membrane evolution. The major stages in primitive membrane formation and the transition to contemporary cell membranes appear to require an exacting relationship between environmental conditions and amphiphile composition and phase behavior. Also, environmental and compositional requirements for individual stages are in some instances incompatible with one another, potentially stultifying the pathway to contemporary membranes. Previous studies in membrane evolution have noted the effects composition and environment have on membrane formation but the crucial dependence and interdependence on these two factors has not been emphasized. This review makes clear the need to focus future investigations away from proof-of-principle studies towards developing a better understanding of the roles that environmental factors and lipid composition and polymorphic phase behavior played in the origin and evolution of cell membranes.

This is a preview of subscription content, access via your institution.

References

  1. 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 35:323–332

    PubMed  CAS  Google Scholar 

  2. 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 1559:1–9

    PubMed  CAS  Google Scholar 

  3. Ariga K, Yuki H, Kikuchi J, Dannemuller O, Albrecht-Gary A, Nakatani Y, Ourisson G (2005) Monolayer studies of single-chain polyprenyl phosphates. Langmuir 21:4578–4583

    PubMed  CAS  Google Scholar 

  4. Bachmann PA, Walde P, Luisi PL, Lang J (1991) Self-replicating micelles:aqueous micelles and enzymatically driven reactions in reverse micelles. J Am Chem Soc 113:8204–8209

    CAS  Google Scholar 

  5. Bachmann PA, Luisi PL, Lang J (1992) Autocatalytic self-replicating micelles as models for prebiotic structures. Nature 357:57–59

    CAS  Google Scholar 

  6. Bada JL (2004) How life began on Earth: a status report. Earth Planet Sci Letters 226:1–15

    CAS  Google Scholar 

  7. Baeza I, Ibañez M, Santiago JC, Wong C, Lazcano A, Oró J (1986) Studies on precellular evolution: the encapsulation of polyribonucleotides by liposomes. Adv Space Res 6(11):39–43

    PubMed  CAS  Google Scholar 

  8. Bangham AD, Standish MM, Miller N (1965) Diffusion of univalent ions across the lamellae of swollen phospholipids. J Mol Biol 13:238–252

    PubMed  CAS  Article  Google Scholar 

  9. Berclaz N, Müller M, Walde P, Luisi PL (2001) Growth and transformation of vesicles studied by ferritin labeling and cryotransmission electron microscopy. J Phys Chem 105:1056–1064

    CAS  Google Scholar 

  10. Blöchliger E, Blocher M, Walde P, Luisi PL (1998) Matrix effect in the size distribution of fatty acid vesicles. J Phys Chem 102:10383–10390

    Google Scholar 

  11. Božic B, Svetina S (2004) A relationship between membrane properties forms the basis of a selectivity mechanism for vesicle self-reproduction. Eur Biophys J 33:565–571

    PubMed  CAS  Google Scholar 

  12. Chakrabarti AC, Deamer DW (1992) Permeability of lipid bilayers to amino acids and phosphate. Biochim Biophys Acta 111:171–177

    Google Scholar 

  13. Chakrabarti AC, Deamer DW (1994) Permeation of membranes by the neutral form of amino acids and peptides: relevance to the origin of peptide translocation. J Mol Evol 39:1–5

    PubMed  Google Scholar 

  14. Chakrabarti AC, Breaker RR, Joyce GF, Deamer DW (1994) Production of RNA by a polymerase protein encapsulated within phospholipid vesicles. J Mol Evol 39:555–559

    PubMed  CAS  Google Scholar 

  15. Chen IA, Szostak JW (2004a) Membrane growth can generate a transmembrane pH gradient in fatty acid vesicles. Proc Natl Acad Sci 101:7965–7970

    PubMed  CAS  Google Scholar 

  16. Chen IA, Szostak JW (2004b) A kinetic study of the growth of fatty acid vesicles. Biophys J 87:988–998

    PubMed  CAS  Google Scholar 

  17. Chen IA, Roberts RW, Szostak JW (2004) The emergence of competition between model protocells. Science 305:1474–1476

    PubMed  CAS  Google Scholar 

  18. Chen IA, Salehi-Ashtiani K, Szostak JW (2005) RNA catalysis in model protocell vesicles. J Am Chem Soc 127:13213–13219

    PubMed  CAS  Google Scholar 

  19. Cronin JR (1998) Clues from the origin of the solar system: meteorites. In: Andre B (ed) The molecular origin of life: assembling pieces of the puzzle. Cambridge University Press, Cambridge, UK, pp 119–146

    Google Scholar 

  20. Cronin JR, Pizzarello S, Cruickshank DP (1988) Organic matter in carbonaceous chondrites, planetary satellites, asteroids and comets. In: Kerridge JF, Matthews MS (eds) Meteorites and the early solar system. University of Arizona Press, Tucson, pp 819–857

    Google Scholar 

  21. Deamer DW (1985) Boundary structures are formed by organic compounds of the Murchinson carbonaceous chondrites. Nature 317:792–794

    CAS  Google Scholar 

  22. Deamer DW (1992) Polycyclic aromatic hydrocarbons: primitive pigment systems in the prebiotic environment. Adv Space Res 12(4):183–189

    PubMed  CAS  Google Scholar 

  23. Deamer DW (1997) The first living systems: a bioenergetic perspective. Microbiol Mol Biol Rev 61(2):239–261 (June)

    PubMed  CAS  Google Scholar 

  24. Deamer DW (1998) Membrane compartments in prebiotic evolution. In: Andre B (ed) The molecular origins of life: assembling the pieces of the puzzle. Cambridge University Press, Cambridge, UK, pp 189–205

    Google Scholar 

  25. Deamer DW, Barchfield GL (1982) Encapsulation of macromolecules by lipid vesicles under simulated prebiotic conditions. J Mol Evol 18:203–206

    PubMed  CAS  Google Scholar 

  26. Deamer DW, Harang E (1990) Light-dependent pH gradients are generated in liposomes containing ferrocyanide. Biosystems 24:1–4

    PubMed  CAS  Google Scholar 

  27. Deamer DW, Oró J (1980) Role of lipids in prebiotic structures. BioSystems 12:167–175

    PubMed  CAS  Google Scholar 

  28. Deamer DW, Pashley RM (1989) Amphiphilic components of the Murchinson carbonaceous chondrite: surface properties and membrane formation. Orig Life Evol Biosph 19:21–38

    PubMed  CAS  Google Scholar 

  29. Deamer DW, Mahon EH, Bosco G (1994) Self-assembling and function of primitive membrane structures. In: Bengtson S (ed) Early life on Earth, Nobel Symposium, No. 84. Columbia University Press, New York, pp 107–115

    Google Scholar 

  30. Deamer DD, Jason P, Sandford SA, Berstein MP, Allamandola LJ (2002) The first cell membranes. Astrobiology 2(4):375

    Google Scholar 

  31. Dworkin JP, Deamer DW, Sandford SA, Allamandola LJ (2001) Self-assembling amphiphilic molecules: synthesis in simulated interstellar/precometary ices. Proc Natl Acad Sci 98(3):815–819

    PubMed  CAS  Google Scholar 

  32. Eichberg J, Sherwood E, Epps DE, Oró J (1977) Cyanamide mediated syntheses under plausible primitive Earth conditions. IV. The synthesis of acylglycerols. J Mol Evol 10:221–230

    PubMed  CAS  Google Scholar 

  33. Epps DE, Sherwood E, Eichberg J, Oró J (1978) Cyanamide mediated syntheses under plausible primitive Earth conditions. V. The synthesis of phosphatadic acid. J Mol Evol 11:279–292

    PubMed  CAS  Google Scholar 

  34. Epps DE, Nooner DW, Eichberg J, Sherwood E, Oró J (1979) Cyanamide mediated syntheses under plausible primitive Earth conditions. VI. The synthesis of glycerol and glycerolphosphates. J Mol Evol 14:235–241

    PubMed  CAS  Google Scholar 

  35. Furuuchi R, Imai E-I, Honda H, Hatori K, Matsuno K (2005) Evolving lipid vesicles in prebiotic hydrothermal environments. Orig Life Evol Biosph 35:333–343

    PubMed  CAS  Google Scholar 

  36. Gershfeld NL (1989a) The critical unilamellar lipid state: a perspective for membrane bilayer assembly. Biochim Biophys Acta 988:335–350

    PubMed  CAS  Google Scholar 

  37. Gershfeld NL (1989b) Spontaneous assembly of a phospholipid bilayer as a critical phenomenon: influence of temperature, composition, and physical state. J Phys Chem 93:5256–5264

    CAS  Google Scholar 

  38. Gershfeld NL, Murayama M (1988) Thermal instability of red blood cell membrane bilayers: temperature dependence of hemolysis. J Mem Biol 101:67–72

    CAS  Google Scholar 

  39. Gershfeld NL, Mudd CP, Tajima K, Berger RL (1993) Critical temperature for unilamellar vesicle formation in dimyristoyl phosphatidylcholine dispersions from specific heat measurements. Biophys J 65:1174–1179

    PubMed  CAS  Article  Google Scholar 

  40. Ginsberg L, Gilbert DL, Gershfeld NL (1991) Membrane bilayer assembly in neural tissue of rat and squid as a critical phenomena: influence of temperature and membrane proteins. J Mem Biol 119:65–73

    CAS  Google Scholar 

  41. 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, New York, pp 12–27

    Google Scholar 

  42. Gotoh M, Mike A, Nagano H, Ribeiro N, Elhabiri M, Gumienna-Kontecka E, Albrecht-Gary A, Schmutz M, Ourisson G, Nakatani Y (2006) Mambrane properties of branched polyprenyl phosphates, postulated as primitive membrane constituents. Chem Bio Diversity 3:434–455

    CAS  Google Scholar 

  43. Gutknecht J (1988) Proton conductance caused by long-chain fatty acids in phospholipid bilayer membranes. J Mem Biol 106:83–93

    CAS  Google Scholar 

  44. Haldane JBS (1929) The origin of life. The Rationalist Annual 148:3–10

    Google Scholar 

  45. Hanczyc MM, Szostak JW (2004) Replicating vesicles as models of primitive cell growth and division. Curr Opin Chem Biol 8:660–664

    PubMed  CAS  Google Scholar 

  46. Hanczyc MM, Fujikawa SM, Szostak JW (2003) Experimental models of primitive cellular compartments: encapsulation, growth, and division. Science 302:618

    PubMed  CAS  Google Scholar 

  47. Hargreaves WR, Deamer DW (1978) Liposomes from ionic, single-chain amphiphiles. Biochemistry 17:3759–3768

    PubMed  CAS  Google Scholar 

  48. Hargreaves WR, Mulvihill S, Deamer DW (1977) Synthesis of phospholipids and membranes in prebiotic conditions. Nature 266:78–80

    PubMed  CAS  Google Scholar 

  49. Hazen RM, Deamer DW (2006) Hydrothermal reactions of pyruvic acid:synthesis, selection, and self-assembly of amphiphilic molecules. Orig Life Evol Biosph [Epub ahead of print]

  50. Israelachvili JN, Marčelja S, Horn RG (1980) Physical principles of membrane organization. Q Rev Biophys 13:121–200

    PubMed  CAS  Google Scholar 

  51. Janas T, Janas T, Yarus M (2004) A membrane transporter for tryptophan composed of RNA. RNA 10:1541–1549

    PubMed  CAS  Google Scholar 

  52. Jin AJ, Edidin M, Nossal R, Gershfeld NL (1999) A singular state of membrane lipids at cell growth temperatures. Biochemistry 38:13275–13278

    PubMed  CAS  Google Scholar 

  53. Keefe AD, Miller SL (1995) Are polyphoshates or phosphate esters prebiotic reagents? J Molec Evol 41:693–702

    PubMed  CAS  Google Scholar 

  54. Khvorova A, Kwak Y-G, Tamkun M, Majerfeld I, Yarus M (1999) RNA’s that bind and change the permeability of phospolipid membranes. Proc Natl Acad Sci U S A 96:10649–10654

    PubMed  CAS  Google Scholar 

  55. Lasic DD (1988) The mechanism of vesicle formation. Biochemistry J 256:1–11

    CAS  Google Scholar 

  56. Lentz BR, Carpenter TJ, Alford DR (1987) Spontaneous fusion of posphatidylcholine small unilamellar vesicles in the fluid phase. Biochemistry 26:5389–5397

    PubMed  CAS  Google Scholar 

  57. Lindahl PA (2002) Stepwise evolution of nonliving to living chemical systems. Orig Life Evol Biosph 34:371–389

    Google Scholar 

  58. Lindblom G, Rilfors L (1989) Cubic phases and isotropic structures formed by membrane lipids-possible biological relevance. Biochim Biophys Acta 988:221–256

    CAS  Google Scholar 

  59. Luisi PL, Stano P, Rasi S, Mavelli F (2004) A possible route to prebiotic vesicle reproduction. Artif Life 10:297–308

    PubMed  Google Scholar 

  60. Maddox J (1994) Origin of the first membrane? Nature 371:101

    PubMed  CAS  Google Scholar 

  61. 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 358:62–63

    Google Scholar 

  62. Miller SL (1953) Production of amino acids under possible primitive Earth conditions. Science 117:528–529

    PubMed  CAS  Google Scholar 

  63. Monnard P-A, Deamer DW (2002) Membrane self-assembly processes: steps toward the first cellular life. Anat Rec 268:197

    Google Scholar 

  64. Monnard P-A, Deamer DW (2003) Preparation of vesicles from nonphospholipid amphiphiles. Methods Enzymol 372:133–151

    PubMed  CAS  Article  Google Scholar 

  65. 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 2:139–152

    PubMed  CAS  Google Scholar 

  66. Morigaki K, Dallavalle S, Walde P, Colonna S, Luisi PL (1997) Autopoietic self-reproduction of chiral fatty acid vesicles. J Am Chem Soc 119:292–301

    CAS  Google Scholar 

  67. Morowitz HJ (1992) The beginnings of cellular life: metabolism recapitulates biogenesis. Yale University Press, New Haven, CT

    Google Scholar 

  68. Morowitz HJ, Heinz B, Deamer DW (1988) The chemical logic of a minimum protocell. Orig Life Evol Biosph 18:281–287

    PubMed  CAS  Google Scholar 

  69. Namani T, Walde P (2005) From decanoate micelles to decanoic acid/dodecylbenzenesulfonate vesicles. Langmuir 21:6210–6219

    PubMed  CAS  Google Scholar 

  70. Namini T, Ishikawa T, Morigaki K, Walde P (2007) Vesicles from docosahexaenoic acid. Colloids Surf 54:118–123

    Google Scholar 

  71. Nomura SM, Yoshikawa Y, 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 6:457–459

    Google Scholar 

  72. Oparin AI (1924) The origin of life. Moscow: Izd. Moskovshii Robochii. English translation: Vernal JD (1967). The origin of life. Weidenfeld and Nicolson, London, pp 199–234

    Google Scholar 

  73. Oparin, AI (1957) The origin of life on earth. Academic, New York

    Google Scholar 

  74. Oparin, AI, Orlovskii AF, Bukhlaeve VY, Gladilin KL (1976) Influence of the enzymatic synthesis of polyadenylic acid on a coacervate system. Dokl Akad Nauk SSSR 226:972–974

    PubMed  CAS  Google Scholar 

  75. Orgel LE (1986) RNA catalysis and the origins of life. J Theor Biol 123:127–149

    PubMed  CAS  Google Scholar 

  76. Ourisson G, Nakatani T (1994) The terpenoid theory of the origin of cellular life: the evolution of terpenoids to cholesterol. Chem Biol 1:11–23

    PubMed  CAS  Google Scholar 

  77. Ourisson G, Nakatani Y (1999) Origins of cellular life: molecular foundations and new approaches. Tetrahedron 55:3183–3190

    CAS  Google Scholar 

  78. 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 70:339–348

    PubMed  CAS  Google Scholar 

  79. Pohl EE, Peterson U, Sun J, Pohl P (2000) Changes of intrinsic membrane potentials induced by flip-flop of long-chain fatty acids. Biochemistry 39:1834–1839

    PubMed  CAS  Google Scholar 

  80. Rana FR (1990) Structure and function of outer membranes and LPS from Wild-Type and LPS-Mutant strains of Salmonella typhimurium and their interaction with Magainins and Polymyxin B. Dissertation, Ohio University

  81. Rao M, Eichberg J, Oró, J (1982) Synthesis of phosphatidylcholine under possible primitive Earth conditions. J Mol Evol 18:196–202

    PubMed  CAS  Google Scholar 

  82. Rao M, Eichberg J, Oró J (1987) Synthesis of phosphatidyethanolamine under possible primitive Earth conditions. J Mol Evol 25:1–6

    PubMed  CAS  Google Scholar 

  83. Rasi S, Mavelli F, Luisi PL (2004) Matrix effect in oleate micelles-vesicles transformation. Orig Life Evol Biosph 34:214–224

    Google Scholar 

  84. Rottem S (1982) Transbilayer distribution of lipids in microbial membranes. In: Rezin S, Ralter R (eds) Current topics in membranes and transport 17. Academic, New York, pp 235–261

    Google Scholar 

  85. 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 31:103–118

    PubMed  CAS  Google Scholar 

  86. Rushdi AI, Simoneit BRT (2006) Abiotic condensation synthesis of glyceride lipids and wax esters under simulated hydrothermal conditions. Orig Life Evol Biosph 36:93–108

    PubMed  CAS  Google Scholar 

  87. Sacerdote MG, Szostak JW (2005) Semipermeable lipid bilayers exhibit diastereoselectivity favoring ribose. Proc Natl Acad Sci 102(17):6004–6008

    PubMed  CAS  Google Scholar 

  88. Seddon JM (1990) Structure of the inverted hexagonal (H11) phase, and non-lamellar phase transitions of lipids. Biochim Biophys Acta 1031:1–69

    PubMed  CAS  Google Scholar 

  89. Segré D, Lancet D (2000) Composing Life. EMBO Rep 11:218

    Google Scholar 

  90. Segré D, Ben-Eli D, Lancet D (2000) Compositional genomes: prebiotic information transfer in mutually catalytic non-covalent assemblies. Proc Natl Acad Sci U S A 97(8):4112–4117

    PubMed  Google Scholar 

  91. Segré D, Ben-Eli D, Deamer D, Lancet D (2001) The lipid world. Orig Life Evol Biosph 31:119–145

    PubMed  Google Scholar 

  92. Shew RL, Deamer DW (1985) A novel method for encapsulation of macromolecules in liposomes. Biochim Biophys Acta 816:1–8

    PubMed  CAS  Google Scholar 

  93. Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175:720–731

    PubMed  CAS  Google Scholar 

  94. Szostak JW, Bartel DP, Luisi PL (2001) Synthesizing life. Nature 409:387–390

    PubMed  CAS  Google Scholar 

  95. Takajo S, Nagano H, Dannenmuller O, Ghosh S, Albrecht AM, Nakatanni Y, Ourisson, G (2001) Membrane properties of sodium 2- and 6-(poly)prenyl-substituted polyprenyl phosphates. New J Chem 25:917–929

    CAS  Google Scholar 

  96. Tremper KE, Gershfeld NL (1999) Temperature dependence of membrane lipid composition in early blastula embryos of Lutechinus pictus: selective sorting of phospholipids into nascent plasma membranes. J Membrane Biol 171:47–53

    CAS  Google Scholar 

  97. Trevors JT (2003) Possible origin of a membrane in the subsurface of the Earth. Cell Biol Int 27:451–457

    PubMed  CAS  Google Scholar 

  98. Vlassov A (2005) How was membrane permeability produced in an RNA world? Orig Life Evol Biosph 35:135–149

    PubMed  CAS  Google Scholar 

  99. Vlassov A, Khvorova A, Yarus M (2001) Binding and disruption of phospholipids bilayers by supramolecular RNA complexes. Proc Natl Acad Sci 98(14):7706–7711

    PubMed  CAS  Google Scholar 

  100. Walde P (2006) Surfactant assemblies and their various possible roles for the origin(s) of life. Orig Life Evol Biosph 36:109–150

    PubMed  CAS  Google Scholar 

  101. Walde P, Wick R, Fresta M, Mangone A, Luisi PL (1994) Autopoietic self-reproduction of fatty acid vesicles. J Am Chem Soc 116:11649–11654

    CAS  Google Scholar 

  102. Weber AL (1987) The triose model: glyceraldehyde as a source of energy and monomers for prebiotic condensation reactions. Orig Life 17:107–119

    CAS  Google Scholar 

  103. Weber AL (1991) Origin of fatty acid synthesis: thermodynamics and kinetics of reaction pathways. J Mol Evol 32:93–100

    PubMed  CAS  Google Scholar 

  104. Wieslander A, Christiansson A, Rilfors L, Lindblom, G (1980) Lipid bilayer stability in membranes, regulation of lipid composition in Acholeplasma laidlawii as governed by molecular shape. Biochemistry 19:3650–3655

    PubMed  CAS  Google Scholar 

  105. Zhang F, Kamp F, Hamilton JA (1996) Dissociation of long and very long chain fatty acids from phospholipid bilayers. Biochemistry 35:16055–16060

    PubMed  CAS  Google Scholar 

  106. Zubay G (2000) Orgins of Life on the Earth and in the Cosmos, 2nd edn. Academic, San Diego, CA, p 347

    Google Scholar 

Download references

Acknowledgements

We wish to acknowledge the Southwestern College Sabbatical Committee and School Board, and RTB for their financial support for JT and FRR, respectively.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jacquelyn A. Thomas.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Thomas, J.A., Rana, F.R. The Influence of Environmental Conditions, Lipid Composition, and Phase Behavior on the Origin of Cell Membranes. Orig Life Evol Biosph 37, 267–285 (2007). https://doi.org/10.1007/s11084-007-9065-6

Download citation

Keywords

  • Amphiphile
  • Bilayer
  • Encapsulation
  • Fatty acid
  • Membrane
  • Origin of life
  • Passive transport
  • Phospholipid
  • Prebiotic
  • Vesicle