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Competition between model protocells driven by an encapsulated catalyst

Nature Chemistry volume 5, pages 495–501 (2013)Cite this article

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A Corrigendum to this article was published on 20 June 2013

This article has been updated

Abstract

The advent of Darwinian evolution required the emergence of molecular mechanisms for the heritable variation of fitness. One model for such a system involves competing protocell populations, each consisting of a replicating genetic polymer within a replicating vesicle. In this model, each genetic polymer imparts a selective advantage to its protocell by, for example, coding for a catalyst that generates a useful metabolite. Here, we report a partial model of such nascent evolutionary traits in a system that consists of fatty-acid vesicles containing a dipeptide catalyst, which catalyses the formation of a second dipeptide. The newly formed dipeptide binds to vesicle membranes, which imparts enhanced affinity for fatty acids and thus promotes vesicle growth. The catalysed dipeptide synthesis proceeds with higher efficiency in vesicles than in free solution, which further enhances fitness. Our observations suggest that, in a replicating protocell with an RNA genome, ribozyme-catalysed peptide synthesis might have been sufficient to initiate Darwinian evolution.

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Figure 1: Schematic representation of adaptive changes and competition between protocell vesicles.
Figure 2: Ser-His catalysis in the presence of fatty-acid vesicles results in increased synthesis of the hydrophobic dipeptide product and decreased substrate hydrolysis.
Figure 3: Competition between vesicles with and without the hydrophobic dipeptide AcPheLeuNH2.
Figure 4: Competition between populations of protocell vesicles.
Figure 5: Inhibitory effect of salt and buffer on competitive growth of vesicles.
Figure 6: Vesicle growth and division.
Figure 7: Transmembrane pH gradient generated by growth of vesicles during competitive micelle uptake.

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Change history

  • 03 June 2013

    In the version of this Article originally published, in Fig 3a, the description for the open triangle should have read: '1 equiv. dye-labelled empty vesicles + vesicles without dipeptide'. This has been corrected in the HTML and PDF versions of the Article.

References

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

    Article  CAS  Google Scholar 

  2. Szathmary, E. & Demeter, L. Group selection of early replicators and the origin of life. J. Theor. Biol. 128, 463–486 (1987).

    Article  CAS  Google Scholar 

  3. Szostak, J. W., Bartel, D. P. & Luisi, P. L. Synthesizing life. Nature 409, 387–390 (2001).

    Article  CAS  Google Scholar 

  4. Budin, I. & Szostak, J. W. Expanding roles for diverse physical phenomena during the origin of life. Ann. Rev. Biophys. 39, 245–263 (2010).

    Article  CAS  Google Scholar 

  5. Gebicki, J. M. & Hicks, M. Ufasomes are stable particles surrounded by unsaturated fatty acid membranes. Nature 243, 232–234 (1973).

    Article  CAS  Google Scholar 

  6. Hargreaves, W. R. & Deamer, D. W. Liposomes from ionic, single-chain amphiphiles. Biochemistry 17, 3759–3768 (1978).

    Article  CAS  Google Scholar 

  7. Oberholzer, T., Wick, R., Luisi, P. L. & Biebricher, C. K. Enzymatic RNA replication in self-reproducing vesicles: an approach to a minimal cell. Biochem. Biophys. Res. Commun. 207, 250–257 (1995).

    Article  CAS  Google Scholar 

  8. Apel, C. L., Deamer, D. W. & Mautner, M. N. Self-assembled vesicles of monocarboxylic acids and alcohols: conditions for stability and for the encapsulation of biopolymers. Biochim. Biophys. Acta 1559, 1–9 (2002).

    Article  CAS  Google Scholar 

  9. Noireaux, V. & Libchaber, A. A vesicle bioreactor as a step toward an artificial cell assembly. Proc. Natl Acad. Sci. USA 101, 17669–17674 (2004).

    Article  CAS  Google Scholar 

  10. Stano, P. & Luisi, P. L. Achievements and open questions in the self-reproduction of vesicles and synthetic minimal cells. Chem. Commun. 46, 3639–3653 (2010).

    Article  CAS  Google Scholar 

  11. Kurihara, K. et al. Self-reproduction of supramolecular giant vesicles combined with the amplification of encapsulated DNA. Nature Chem. 3, 775–781 (2011).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  13. Deamer, D. W. & Barchfeld, G. L. Encapsulation of macromolecules by lipid vesicles under simulated prebiotic conditions. J. Molecul. Evol. 18, 203–206 (1982).

    Article  CAS  Google Scholar 

  14. Chiruvolu, S. et al. A phase of liposomes with entangled tubular vesicles. Science 266, 1222–1225 (1994).

    Article  CAS  Google Scholar 

  15. Bard, M., Albrecht, M. R., Gupta, N., Guynn, C. J. & Stillwell, W. Geraniol interferes with membrane functions in strains of Candida and Saccharomyces. Lipids 23, 534–538 (1988).

    Article  CAS  Google Scholar 

  16. Suzuki, K., Toyota, T., Takakura, K. & Sugawara, T. Sparkling morphological changes and spontaneous movements of self-assemblies in water induced by chemical reactions. Chem. Lett. 38, 1010–1015 (2009).

    Article  CAS  Google Scholar 

  17. Chen, I. A., Roberts, R. W. & Szostak, J. W. The emergence of competition between model protocells. Science 305, 1474–1476 (2004).

    Article  CAS  Google Scholar 

  18. Budin, I. & Szostak, J. W. Physical effects underlying the transition from primitive to modern cell membranes. Proc. Natl Acad. Sci. USA 108, 5249–5254 (2011).

    Article  CAS  Google Scholar 

  19. Gorlero, M. et al. Ser-His catalyses the formation of peptides and PNAs. FEBS Lett. 583, 153–156 (2009).

    Article  CAS  Google Scholar 

  20. Wieczorek, R., Dorr, M., Chotera, A., Luisi, P. L. & Monnard, P. A. Formation of RNA phosphodiester bond by histidine-containing dipeptides. ChemBioChem 14, 217–223 (2013).

    Article  CAS  Google Scholar 

  21. Chen, I. A. & Szostak, J. W. Membrane growth can generate a transmembrane pH gradient in fatty acid vesicles. Proc. Natl Acad. Sci. USA 101, 7965–7970 (2004).

    Article  CAS  Google Scholar 

  22. Zhu, T. F. & Szostak, J. W. Coupled growth and division of model protocell membranes. J. Am. Chem. Soc. 131, 5705–5713 (2009).

    Article  CAS  Google Scholar 

  23. Zhu, T. F., Adamala, K., Zhang, N. & Szostak, J. W. Photochemically driven redox chemistry induces protocell membrane pearling and division. Proc. Natl Acad. Sci. USA 109, 9828–9832 (2012).

    Article  CAS  Google Scholar 

  24. Moore, P. B. & Steitz, T. A. The roles of RNA in the synthesis of protein. Cold Spring Harb. Perspect. Biol. 3, a003780 (2011).

    Article  Google Scholar 

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Acknowledgements

J.W.S. is an Investigator of the Howard Hughes Medical Institute. This work was supported in part by National Aeronautics and Space Administration Exobiology grant NNX07AJ09G. We thank A. Engelhart, C. Hentrich, I. Budin and R. Wieczorek for discussions and help with manuscript preparation.

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Authors and Affiliations

  1. Department of Molecular Biology, Howard Hughes Medical Institute, and Center for Computational and Integrative Biology, Massachusetts General Hospital, Boston, 02114, Massachusetts, USA

    Katarzyna Adamala & Jack W. Szostak

  2. Dipartimento di Biologia, Università degli Studi di Roma Tre, Rome, Italy

    Katarzyna Adamala

Authors
  1. Katarzyna Adamala
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  2. Jack W. Szostak
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Both authors contributed to the design of the experiments and to writing the paper. Experiments were conducted by K.A.

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Correspondence to Jack W. Szostak.

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The authors declare no competing financial interests.

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Adamala, K., Szostak, J. Competition between model protocells driven by an encapsulated catalyst. Nature Chem 5, 495–501 (2013). https://doi.org/10.1038/nchem.1650

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