Advertisement

Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Energy Transduction Inside of Amphiphilic Vesicles: Encapsulation of Photochemically Active Semiconducting Particles

  • 229 Accesses

  • 24 Citations

Abstract

Amphiphilic bilayer membrane structures (vesicles) have been postulated to have been abiotically formed and spontaneously assemble on the prebiotic Earth, providing compartmentalization for the origin of life. These vesicles are similar to modern cellular membranes and can serve to contain water-soluble species, concentrate species, and have the potential to catalyze reactions. The origin of the use of photochemical energy in metabolism (i.e. energy transduction) is one of the central issues in the origin of life. This includes such questions as how energy transduction may have occurred before complex enzymatic systems, such as required by contemporary photosynthesis, had developed and how simple a photochemical system is possible. It has been postulated that vesicle structures developed the ability to capture and transduce light, providing energy for reactions. It has also been shown that pH gradients across the membrane surface can be photochemically created, but coupling these to drive chemical reactions has been difficult. Colloidal semiconducting mineral particles are known to photochemically drive redox chemistry. We propose that encapsulation of these particles has the potential to provide a source of energy transduction inside vesicles, and thereby drive protocellular chemistry, and represents a model system for early photosynthesis. In our experiments we show that TiO2 particles, in the ~20 nm size range, can be incorporated into vesicles and retain their photoactivity through the dehydration/rehydration cycles that have been shown to concentrate species inside a vesicle.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

References

  1. Blankenship RE (2002) Chapter 11: Origin and evolution of photosynthesis, in, molecular mechanisms of photosynthesis. Blackwell Science, London, pp 220–257

  2. Bojarska E, Pawlicki K, Czochralska B (1997) Photocatalytic reduction of nicotinamide coenzymes in the presence of titanium dioxide: the influence of aliphatic aminoacids. J. Photochem. Photobiol. A 108:207–213

  3. Cavalier-Smith T (1987) The origins of cells: a symbiosis between genes, catalysts and membranes. Cold Spring Harbor Symp. Quant. Biol. 52:805–824

  4. Cuendet P, Grätzel M (1984) Photoreduction of NAD+ to NADH in Semiconductor Dispersions. Photochem. Photobiol. 39:609–612

  5. Cuendet P, Grätzel M (1985) Artificial photosynthesis. Ann. Proc. Phytochem. Soc. 26:187–196

  6. Deamer DW (1978) In, Light Transducting Membranes. Academic Press, NY, pp 1–19 and 23–60

  7. Deamer DW (1985) Boundary structures are formed by organic components of the Murchison carbonaceous chondrite. Nature 317:792–794

  8. Deamer DW (1997) The first living systems: a bioenergetic perspective. Microbiology and Molecular Biology Reviews 61:239–264

  9. Deamer DW (2008) How leaky were primitive cells? Nature 454:37–38

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

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

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

  13. Deamer DW, Harang ME, Bosco G (1994) Early life on earth. In: Bengtson S (ed) Nobel symposium No. 84. Columbia University Press, New York

  14. Deamer D, Dworkin JP, Sandford SA, Bernstein MP Allamandola LJ (2002) The first cell membranes. Astrobiology 2:371–381

  15. Delaye L, Lazcano A (2005) Prebiological evolution and the physics of the origin of life. Phys. Life Rev. 2:47–64

  16. Douglas T, Stark VT (2000) Nanophase cobalt oxyhydroxide mineral synthesized within the protein cage of ferritin. Inorg. Chem. 39:1828–30

  17. Driebergen RJ, Den Hartigh J, Holthuis JJM, Hulshoff A, Van Oort WJ, Postma Kelder SJ, Verboom W, Reinhoudt DN, Bos M, Van der Linden WE (1990) Electrochemistry of potentially bioreductive alkylating quinones: part 1. Electrochemical properties of relatively simple quinone, as model compounds of mitomycin- and aziridinylquinone-type antitumor agents. Anal. Chim. Acta 233:251–268

  18. Driebergen RJ, Moret EE, Janssen LHM, Blauw JS, Holthuis JJM, Postma Kelder SJ, Verboom W, Reinhoudt DN, Van der Linden WE (1992) Electrochemistry of potentially bioreductive alkylating quinones: part 3. Quantitative structure-electrochemistry relationships of aziridinyquinone. Anal. Chim. Acta 257:257–273

  19. Dryhurst G (1982) Biological electrochemistry. Academic Press, New York

  20. Duonghong D, Ramsden J, Grätzel M (1982) Dynamics of interfacial electron-transfer processes in colloidal semiconductor systems. J. Am. Chem. Soc. 104:2977–2985

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

  22. Epps DE, Sherwood E, Eichberg J, Oró J (1978) Cyanamide mediated syntheses under plausible primitive earth conditions. J. Mol. Evol. 11:279–292

  23. Fitzpatrick RW, Chittlebrorough DJ (2002) Titanium and zirconium minerals. In: Dixon JB, Schulze DG (eds) Soil mineralogy with environmental applications. Soil Science Society of America, Madison, WI, pp 667–691

  24. Fox MA, Dulay MT (1993) Heterogeneous photocatalysis. Chem. Rev. 93:341–357

  25. Goldberg ED, Arrhenius GOS (1958) Chemistry of pacific pelagic sedients. Geochim. Cosmochim. Acta 13:153–212

  26. Grätzel M (1982) Artificial photosynthesis, energy- and light-driven electron transfer in organized molecular assemblies and colloidal semiconductors. Biochim. Biophys. Acta 683:221–244

  27. Grätzel M (1983) Energy resources through photochemistry and catalysis. Academic Press, New York

  28. Gregor CB, Garrels RM, Mackenzie FT, Maynard JB (1988) Chemical cycles in the evolution of the earth. John Wiley & Sons, NY

  29. Hanczyc MM, Fujikawa SM, Szostak JW (2003) Experimental models of primitive cellular compartments: encapsulation, growth, and division. Science 302:618–622

  30. Hanczyc MM, Mansy SS, Szostak JW (2007) Mineral surface directed membrane assembly. Orig. Life Evol. Biosphere 37:67–82

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

  32. Harrison PM, Arosio P (1996) The ferritins: molecular properties, iron storage function and cellular regulation. Biochim. Biophys. Acta 1275:161–203

  33. Holland HD (1984) The chemical evolution of the atmosphere and oceans. Princeton University Press, Princeton, NJ

  34. Kasting JF (1993) Early evolution of the atmosphere and ocean. In: Greenberg JM, Menoza-Goméz, Pirronello CXV (eds) The Chemistry of LIfe’s Origins. Kluwer Academic Publishers, Dordrecth

  35. King CC (1990) Did membrane electrochemistry precede translation? Origins Life Evol. Biosphere 20:15–25

  36. Koch AL (1985) Primeval cells: possible energy-generating and cell-division mechanisms. J. Mol. Evol. 21:270–277

  37. Lanyi JK, Pohorille A (2001) Proton pumps: mechanism of action and applications. Trends in Biotechnology 19:140–144

  38. Lazcano A, Miller SL (1999) On the origin of metabolic pathways. J. Mol. Evol. 49:424–431

  39. Leland JK, Bard AJ (1987a) Electrochemical investigation of the electron-transfer kinetics and energetics of illuminated tungsten oxide colloids. J. Phys. Chem. 91:5083–5087

  40. Leland JK, Bard AJ (1987b) Photochemistry of colloidal semiconducting iron oxide polymorphs. J. Phys. Chem. 91:5076–5083

  41. Li Z, Guo Y, Scriven LE, Davis HT (1996) Stabilization of aqueous clay suspensions with AOT vesicular solutions. Colloids and Surfaces A 106:149–159

  42. Liu C-y, Bard AJ (1989) Irradiation-induced absorption edge shifts in colloidal particles of FeS2 (Pyrite). J. Phys. Chem. 93:7047–7049

  43. 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 454:122–125

  44. McCollom TM, Ritter G, Simoneit BRt (1999) Lipid synthesis under hydrothermal conditions by Fischer-tropsch-type reactions. Orig. Life Evol. Biosphere 29:153–166

  45. Mills A, Hunte SL (1997) An overview of semiconductor photocatalysis. J. Photochem. Photobiol. A 108:1–35

  46. Morowitz HJ (1992) Beginnings of Cellular Life. Yale University Press, New Haven, CT

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

  48. Moser J, Grätzel M (1983) Light-induced electron transfer in colloidal semiconductor dispersions: single vs. dielectronic reduction of acceptors by conduction-band electrons. J. Am. Chem. Soc. 105:6547–6555

  49. Pitard B, Richard P, Dunach M, Girault G, Rigaud JI (1996a) ATP synthesis by the F0f1 ATP synthase from thermophilic bacillus PS3 reconstituted into liposomes with bacteriorhodopsin .1. Factors defining the optimal reconstitution of ATP synthases with bacteriorhodopsin. European Journal Of Biochemistry 235:769–778

  50. Pitard B, Richard P, Dunach M, Rigaud JI (1996b) ATP Synthesis by the F0F1 ATP synthase from thermophilic bacillus PS3 reconstituted into liposomes with bacteriorhodopsin .2. Relationships between proton motive force and ATP synthesis. European Journal Of Biochemistry 235:779–788

  51. Pohorille A, Wilson MA (1995) Molecular dynamics studies of simple membrane-water interfaces: structure and functions in the beginnings of cellular life. Orig. Life Evol. Biosphere 25:21–46

  52. Quan M, Sanchez D, Wasylkiw MF, Smith DK (2007) Voltammetry of Quinones in unbuffered aqueous solution: reassessing the roles of proton transfer and hydrogen bonding in the aqueous electrochemistry of Quinones. J. Am. Chem. Soc. 129:12847–12865

  53. Rao M, Eichberg J, Oro J (1982) Synthesis of phosphatidylcholine under possible primitive earth conditions. J. Mol. Evol. 18:196–202

  54. Schoonen MAA, Xu Y, Strongin DR (1998) An introduction to geocatalysis. J. of Geochem. Expl. 62:201–215

  55. Schütz L, Rahn KA (1982) Trace-element concentrations in erodible soils. Atmos. Environ. 16:171–176

  56. Squyres SW, Arvidson RE, Ruff S, Gellert R, Morris RV, Ming DW, Crumpler L, Farmer JD, Marais DJD, Yen A, McLennan SM, Calvin W, Bell JF III, Clark BC, Want A, McCoy TJ, Schmidt ME, de Souza PA Jr (2008) Detection of silica-rich deposits on Mars. Science 320:1063–1067

  57. Steinberg-Yfrach G, Rigaud JL, Durantini EN, Moore AL, Gust D, Moore TA (1998) Light-driven production of ATP catalysed by F0F1-ATP synthase in an artificial photosynthetic membrane. Nature 392:479–482

  58. Stiles CA, Mora CI, Driese SG (2003) Pedogenic processes and domain boundaries in a Vertisol Climosequence: evidence from titanium and zirconium distribution and morphology. Geoderma 116:279–299

  59. Sun K, Mauzerall D (1996) A simple light-driven transmembrane proton pump. Proc. Nat. Acad. Sci. USA 93:10758–10762

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

  61. Taboada T, Cortizas AM, García C, García-Rodeja E (2006) Particle-size fractionation of titanium and zirconium during weathering and pedogenesis of granitic rocks in NW Spain. Geoderma 131:218–236

  62. Veizer J (1983) Geological evolution of the archean-early proterozoic earth. In: Schopf JW (ed) Earth’s earliest biosphere: Its origin and evolution. Princeton Univ. Press, Princeton, NJ, pp 240–259

  63. Walker JCG, Klein C, Schidlowski M, Schopf JW, Stevenson DJ, Walker MR (1983) Environmental evolution on the Archean-early proterozoic earth. In: Schopf JW (ed) Earth’s Earliest biosphere: Its origin and evolution. Princeton University Press, Princeton, NJ, pp 261–290

  64. Ward MD, Bard AJ (1982) Photocurrent enhancement via trapping of photogenerated electrons of TiO2 Particles. J. Phys. Chem. 86:3599–3605

  65. Xu Y, Schoonen MAA (2000) The absolute energy positions of conduction and valence bands of selected semiconducting minerals. American Mineralogist 85:543–556

  66. Yesodhara E, Grätzel M (1983) Photodecomposition of liquid water with TiO2-supported noble metal clusters. Helv. Chim. Acta 66:2145–2153

Download references

Acknowledgements

The authors would like to gratefully acknowledge Dr. David Deamer for his advice and assistance and NASA’s Astrobiology: Exobiology and Evolutionary Biology Program for financial support.

Author information

Correspondence to David P. Summers.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Summers, D.P., Noveron, J. & Basa, R.C.B. Energy Transduction Inside of Amphiphilic Vesicles: Encapsulation of Photochemically Active Semiconducting Particles. Orig Life Evol Biosph 39, 127–140 (2009). https://doi.org/10.1007/s11084-009-9160-y

Download citation

Keywords

  • Vesicles
  • Energy transduction
  • Photosynthesis
  • Semiconductors
  • Colloids
  • Protocells
  • Origin of life
  • Origin of photosynthesis