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Cell evolution and the problem of membrane topology

Nature Reviews Molecular Cell Biology volume 8, pages 1018–1024 (2007)Cite this article

Abstract

Cells somehow evolved from primordial chemistry and their emergence depended on the co-evolution of the cytoplasm, a genetic system and the cell membrane. It is widely believed that the cytoplasm evolved inside a primordial lipid vesicle, but here I argue that the earliest cytoplasm could have co-evolved to high complexity outside a vesicle on the membrane surface. An invagination of the membrane, aided by an early cytoskeletal system, may have formed the first cells — initially within primordial vesicles.

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Figure 1: Biosynthetic pathways for amino acids, phospholipids and central metabolism.
Figure 2: Surface interactions and the membrane problem.
Figure 3: The outside-in model of cellularization.

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References

  1. Doolittle, R. F. Searching for the common ancestor. Res. Microbiol. 151, 85–89 (2000).

    Article  CAS  Google Scholar 

  2. Poole, A., Jeffares, D. & Penny, D. Early evolution: prokaryotes, the new kids on the block. Bioessays 21, 880–889 (1999).

    Article  CAS  Google Scholar 

  3. Reichard, P. The evolution of ribonucleotide reduction. Trends Biochem. Sci. 22, 81–85 (1997).

    Article  CAS  Google Scholar 

  4. Gil, R., Silva, F. J., Pereto, J. & Moya, A. Determination of the core of a minimal bacterial gene set. Microbiol. Mol. Biol. Rev. 68, 518–537 (2004).

    Article  CAS  Google Scholar 

  5. Koonin, E. V. Comparative genomics, minimal gene-sets and the last universal common ancestor. Nature Rev. Microbiol. 1, 127–136 (2003).

    Article  CAS  Google Scholar 

  6. Glass, J. I. et al. Essential genes of a minimal bacterium. Proc. Natl Acad. Sci. USA 103, 425–430 (2006).

    Article  CAS  Google Scholar 

  7. Brasier, M., McLoughlin, N., Green, O. & Wacey, D. A fresh look at the fossil evidence for early Archaean cellular life. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 887–902 (2006).

    Article  CAS  Google Scholar 

  8. Kutschera, U. & Niklas, K. J. The modern theory of biological evolution: an expanded synthesis. Naturwissenschaften 91, 255–276 (2004).

    Article  CAS  Google Scholar 

  9. Miller, S. L., Schopf, J. W. & Lazcano, A. Oparin's “Origin of Life”: sixty years later. J. Mol. Evol. 44, 351–353 (1997).

    Article  CAS  Google Scholar 

  10. Haldane, J. The origin of life. Rationalist Annual 3, 148–153 (1929).

    Google Scholar 

  11. Ferris, J. P. Prebiotic synthesis: problems and challenges. Cold Spring Harb. Symp. Quant. Biol. 52, 29–35 (1987).

    Article  CAS  Google Scholar 

  12. Oro, J., Miller, S. L. & Lazcano, A. The origin and early evolution of life on Earth. Annu. Rev. Earth Planet. Sci. 18, 317–356 (1990).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  14. Kvenvolden, K. et al. Evidence for extraterrestrial amino-acids and hydrocarbons in the Murchison meteorite. Nature 228, 923–926 (1970).

    Article  CAS  Google Scholar 

  15. Oro, J., Mills, T. & Lazcano, A. Comets and the formation of biochemical compounds on the primitive Earth — a review. Orig. Life Evol. Biosph. 21, 267–277 (1992).

    Article  CAS  Google Scholar 

  16. Deamer, D. W. & Pashley, R. M. Amphiphilic components of the Murchison carbonaceous chondrite: surface properties and membrane formation. Orig. Life Evol. Biosph. 19, 21–38 (1989).

    Article  CAS  Google Scholar 

  17. Griffith, R. W. Freshwater or marine origin of the vertebrates? Comp. Biochem. Physiol. A 87, 523–531 (1987).

    Article  CAS  Google Scholar 

  18. Monnard, P. A. & Deamer, D. W. Membrane self-assembly processes: steps toward the first cellular life. Anat. Rec. 268, 196–207 (2002).

    Article  CAS  Google Scholar 

  19. Martin, W. & Russell, M. J. 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, 59–85 (2003).

    Article  CAS  Google Scholar 

  20. Deamer, D. W. & Dworkin, J. P. Chemistry and physics of primitive membranes. Top. Curr. Chem. 259, 1–27 (2005).

    Article  CAS  Google Scholar 

  21. Bernal, J. The Origin of Life (Weidenfeld and Nicholson, London, 1967).

    Google Scholar 

  22. Davis, B. Evolution of the genetic code. Prog. Biophys. Mol. Biol. 72, 157–243 (1999).

    Article  CAS  Google Scholar 

  23. Maden, B. E. No soup for starters? Autotrophy and the origins of metabolism. Trends Biochem. Sci. 20, 337–341 (1995).

    Article  CAS  Google Scholar 

  24. Wachtershauser, G. Groundworks for an evolutionary biochemistry: the iron-sulphur world. Prog. Biophys. Mol. Biol. 58, 85–201 (1992).

    Article  CAS  Google Scholar 

  25. Hanczyc, M. M., Mansy, S. S. & Szostak, J. W. Mineral surface directed membrane assembly. Orig. Life Evol. Biosph. 37, 67–82 (2007).

    Article  CAS  Google Scholar 

  26. Davis, B. Molecular evolution before the origin of species. Prog. Biophys. Mol. Biol. 79, 77–133 (2002).

    Article  CAS  Google Scholar 

  27. Deamer, D. W. & Oro, J. Role of lipids in prebiotic structures. Biosystems 12, 167–175 (1980).

    Article  CAS  Google Scholar 

  28. Hargreaves, W. R., Mulvihill, S. J. & Deamer, D. W. Synthesis of phospholipids and membranes in prebiotic conditions. Nature 266, 78–80 (1977).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  30. Baeza, I. et al. Liposomes with polyribonucleotides as model of precellular systems. Orig. Life Evol. Biosph. 17, 321–331 (1987).

    Article  CAS  Google Scholar 

  31. Morowitz, H. Beginnings of Cellular Life: Metabolism Recapitulates Biogenesis (Yale Univ. Press, New Haven, 1992).

    Google Scholar 

  32. Luisi, P. L., Ferri, F. & Stano, P. Approaches to semi-synthetic minimal cells: a review. Naturwissenschaften 93, 1–13 (2006).

    Article  CAS  Google Scholar 

  33. Monnard, P. A., Oberholzer, T. & Luisi, P. Entrapment of nucleic acids in liposomes. Biochim. Biophys. Acta 1329, 39–50 (1997).

    Article  CAS  Google Scholar 

  34. Yu, W. et al. Synthesis of functional protein in liposome. J. Biosci. Bioeng. 92, 590–593 (2001).

    Article  CAS  Google Scholar 

  35. Ishikawa, K., Sato, K., Shima, Y., Urabe, I. & Yomo, T. Expression of a cascading genetic network within liposomes. FEBS Lett. 576, 387–390 (2004).

    Article  CAS  Google Scholar 

  36. Trevors, J. T. & Pollack, G. H. Hypothesis: the origin of life in a hydrogel environment. Prog. Biophys. Mol. Biol. 89, 1–8 (2005).

    Article  CAS  Google Scholar 

  37. Segre, D., Ben-Eli, D., Deamer, D. W. & Lancet, D. The lipid world. Orig. Life Evol. Biosph. 31, 119–145 (2001).

    Article  CAS  Google Scholar 

  38. Blobel, G. Intracellular protein topogenesis. Proc. Natl Acad. Sci. USA 77, 1496–1500 (1980).

    Article  CAS  Google Scholar 

  39. Cavalier-Smith, T. Obcells as proto-organisms: membrane heredity, lithophosphorylation, and the origins of the genetic code, the first cells, and photosynthesis. J. Mol. Evol. 53, 555–595 (2001).

    Article  CAS  Google Scholar 

  40. Lowe, J., van den Ent, F. & Amos, L. A. Molecules of the bacterial cytoskeleton. Annu. Rev. Biophys. Biomol. Struct. 33, 177–198 (2004).

    Article  Google Scholar 

  41. Bork, P., Sander, C. & Valencia, A. An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and Hsp70 heat shock proteins. Proc. Natl Acad. Sci. USA 89, 7290–7294 (1992).

    Article  CAS  Google Scholar 

  42. Egelman, E. H. Actin's prokaryotic homologs. Curr. Opin. Struct. Biol. 13, 244–248 (2003).

    Article  CAS  Google Scholar 

  43. Li, J. Y. & Wu, C. F. Perspectives on the origin of microfilaments, microtubules, the relevant chaperonin system and cytoskeletal motors — a commentary on the spirochaete origin of flagella. Cell Res. 13, 219–227 (2003).

    Article  CAS  Google Scholar 

  44. Carballido-Lopez, R. & Errington, J. A dynamic bacterial cytoskeleton. Trends Cell Biol. 13, 577–583 (2003).

    Article  CAS  Google Scholar 

  45. Doolittle, R. F. & York, A. L. Bacterial actins? An evolutionary perspective. Bioessays 24, 293–296 (2002).

    Article  CAS  Google Scholar 

  46. Erickson, H. P. Evolution of the cytoskeleton. Bioessays 29, 668–677 (2007).

    Article  CAS  Google Scholar 

  47. DeRosier, D. J. & Tilney, L. G. F-actin bundles are derivatives of microvilli: what does this tell us about how bundles might form? J. Cell Biol. 148, 1–6 (2000).

    Article  CAS  Google Scholar 

  48. Janmey, P. A. & Lindberg, U. Cytoskeletal regulation: rich in lipids. Nature Rev. Mol. Cell Biol. 5, 658–666 (2004).

    Article  CAS  Google Scholar 

  49. Eitzen, G. Actin remodeling to facilitate membrane fusion. Biochim. Biophys. Acta 1641, 175–181 (2003).

    Article  CAS  Google Scholar 

  50. Kjeken, R. et al. Fusion between phagosomes, early and late endosomes: a role for actin in fusion between late, but not early endocytic organelles. Mol. Biol. Cell 15, 345–358 (2004).

    Article  CAS  Google Scholar 

  51. Kaksonen, M., Toret, C. P. & Drubin, D. G. Harnessing actin dynamics for clathrin-mediated endocytosis. Nature Rev. Mol. Cell Biol. 7, 404–414 (2006).

    Article  CAS  Google Scholar 

  52. Soldati, T. & Schliwa, M. Powering membrane traffic in endocytosis and recycling. Nature Rev. Mol. Cell Biol. 7, 897–908 (2006).

    Article  CAS  Google Scholar 

  53. Yarar, D., Waterman-Storer, C. M. & Schmid, S. L. SNX9 couples actin assembly to phosphoinositide signals and is required for membrane remodeling during endocytosis. Dev. Cell 13, 43–56 (2007).

    Article  CAS  Google Scholar 

  54. Massarwa, R., Carmon, S., Shilo, B. Z. & Schejter, E. D. WIP/WASp-based actin-polymerization machinery is essential for myoblast fusion in Drosophila. Dev. Cell 12, 557–569 (2007).

    Article  CAS  Google Scholar 

  55. Kandler, O. [Festival lecture. The position of microorganisms in the global phylogenetic system of three domains]. Mycoses 37 (Suppl. 1), 13–27 (1994).

    PubMed  Google Scholar 

  56. Schmelz, M. et al. Assembly of vaccinia virus: the second wrapping cisterna is derived from the trans Golgi network. J. Virol. 68, 130–147 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Rietdorf, J. et al. Kinesin-dependent movement on microtubules precedes actin-based motility of vaccinia virus. Nature Cell Biol. 3, 992–1000 (2001).

    Article  CAS  Google Scholar 

  58. Moreno-Borchart, A. C. & Knop, M. Prospore membrane formation: how budding yeast gets shaped in meiosis. Microbiol. Res. 158, 83–90 (2003).

    Article  CAS  Google Scholar 

  59. Kim, J. & Klionsky, D. J. Autophagy, cytoplasm-to-vacuole targeting pathway, and pexophagy in yeast and mammalian cells. Annu. Rev. Biochem. 69, 303–342 (2000).

    Article  CAS  Google Scholar 

  60. Wong, J. T. Coevolution theory of the genetic code at age thirty. Bioessays 27, 416–425 (2005).

    Article  CAS  Google Scholar 

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Acknowledgements

I thank T. Gibson, M. Knop, S. Trachtenberg, D. Lancet, G. van Meer, L. Mayorga and J. Reich for their comments and discussion, and C. Bleck for preparing the figures.

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  1. Gareth Griffiths is at the European Molecular Biology Laboratory, Heidelberg, Germany. gareth.griffiths@embl-heidelberg.de,

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Griffiths, G. Cell evolution and the problem of membrane topology. Nat Rev Mol Cell Biol 8, 1018–1024 (2007). https://doi.org/10.1038/nrm2287

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