Abstract
The construction of a protocell from a materials point of view is important in understanding the origin of life. Both self-reproduction of a compartment and self-replication of an informational substance have been studied extensively, but these processes have typically been carried out independently, rather than linked to one another. Here, we demonstrate the amplification of DNA (encapsulated guest) within a self-reproducible cationic giant vesicle (host). With the addition of a vesicular membrane precursor, we observe the growth and spontaneous division of the giant vesicles, accompanied by distribution of the DNA to the daughter giant vesicles. In particular, amplification of the DNA accelerated the division of the giant vesicles. This means that self-replication of an informational substance has been linked to self-reproduction of a compartment through the interplay between polyanionic DNA and the cationic vesicular membrane. Our self-reproducing giant vesicle system therefore represents a step forward in the construction of an advanced model protocell.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Luisi, P. L. The Emergence of Life: From Chemical Origins to Synthetic Biology (Cambridge Univ. Press, 2006).
Gardner, P. M., Winzer, K. & Davis, B. D. Sugar synthesis in a protocellular model leads to a cell signaling response in bacteria. Nature Chem. 1, 377–383 (2009).
Gibson, D. G. et al. Creation of bacterial cell controlled by a chemically synthesized genome. Science 329, 52–56 (2010).
Walde, P. Building artificial cells and protocell models: experimental approaches with lipid vesicles. Bioessays 32, 296–303 (2010).
Luisi, P. L., Ferri, F. & Stano, P. Approaches to semi-synthetic minimal cells: a review. Naturwissenschaften 93, 1–13 (2006).
Stano, P. & Luisi, P. L. Achievement and open questions in the self-reproduction of vesicles and synthetic minimal cells. Chem. Commun. 46, 3639–3653 (2010).
Fleischaker, G. R., Colonna, S. & Luisi, P. L. (eds) Self-Production of Supramolecular Structures: From Synthetic Structures to Models of Minimal Living Systems (Kluwer, 1994).
Hanczyc, M. M., Fujikawa, S. M. & Szostak, J. W. Experimental models of primitive cellular compartments: encapsulation, growth, and division. Science 302, 618–622 (2003).
Szostak, J. W., Bartel, D. P. & Luisi P. L. Synthesizing life. Nature 409, 387–390 (2001).
Gesteland, R. F., Cech, T. R. & Atkins, J. F. (eds) The RNA World 3rd edn (Cold Spring Harbor Laboratory Press, 2005).
Lee, D. H., Granja, J. R., Martinez, J. A., Severin, K. & Ghadiri, M. R. A self-replicating peptide. Nature 382, 525–528 (1996).
Segré, D., Ben-Eli, D., Deamer, D. & Lancet, D. The lipid world. Orig. Life Evol. Biosph. 1–2, 119–145 (2001).
Mansy, S. S., Schrum, J. P., Krishnamurthy, M., Tobé S., Treco, D. A. & Szostak, J. W. Template-directed synthesis of a genetic polymer in a model protocell. Nature 454, 122–125 (2008).
Mansy, S. S. & Szostak, J. W. Thermostability of model protocell membranes. Proc. Natl. Acad. Sci. USA 105, 13351–13355 (2008).
Powner, M. W., Gerland, B. & Sutherland, J. D. Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible condition. Nature 459, 239–242 (2009).
Powner, M. W., Sutherland, J. D. & Szostak, J. W. Chemoselective multicomponent one-pot assembly of purine precursors in water. J. Am. Chem. Soc. 132, 16677–16688 (2010).
Oberholzer, T., Albrizio, M. & Luisi, P. L. Polymerase chain reaction in liposome. Chem. Biol. 2, 677–682 (1995).
Chakrabarti, A. C., Breaker, R. R., Joyce, G. F. & Deamer, D. W. Production of RNA by a polymerase protein encapsulated within phospholipid vesicles. J. Mol. Evol. 39, 555–559 (1994).
Walde, P., Goto, A., Monnard, P-A., Wessicken, M. & Luisi, P. L. Oparin's reactions revisited: enzymatic synthesis of poly(adenylic acid) in micelles and self-reproducing vesicles. J. Am. Chem. Soc. 116, 7541–7547 (1994).
Zepik, H. H. & Walde, P. Achievements and challenges in generating protocell models. ChemBioChem 9, 2771–2772 (2008).
Chiarabelli, C., Stano, P. & Luisi, P. L. Chemical approaches to synthetic biology. Curr. Opin. Biotechnol. 20, 492–497 (2009).
Kuruma, Y., Stano, P., Ueda, T. & Luisi, P. L. A synthetic biology approach to the construction of membrane proteins in semi-synthetic minimal cells. Biochim. Biophys. Acta. 1788, 567–574 (2009).
Sunami, T., Hosoda, K., Suzuki, H., Matsuura, T. & Yomo, T. Cellular compartment model for exploring the effect of the lipidic membrane on the kinetics of encapsulated biochemical reactions. Langmuir 26, 8544–8551 (2010).
Nomura, S. M. et al. Gene expression within cell-sized lipid vesicles. ChemBioChem. 4, 1172–1175 (2003).
Kita, H. et al. Replication of genetic information with self-encoded replicase in liposomes. ChemBioChem. 9, 2403–2410 (2008).
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. Comm. 207, 250–257 (1995).
Atwood, J. L., Davies, J. E. D., Macnicol, D. D., Vögtle, F. & Lehn, J-M. (eds) Comprehensive Supramolecular Chemistry (Pergamon, 1996).
Lehn, J-M. Supramolecular Chemistry: Concepts and Perspectives (Wiley-VCH, 1995).
Ariga, K. & Kunitake, T. Supramolecular Chemistry—Fundamentals and Applications (Springer, 2006).
Muraoka, T., Kinbara, K. & Aida, T. Mechanical twisting of a guest by a photoresponsive host. Nature 440, 512–515 (2006).
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).
Takakura, K., Toyota, T. & Sugawara, T. A novel system of self-reproducing giant vesicles. J. Am. Chem. Soc. 125, 8134–8140 (2003).
Takakura, K. & Sugawara, T. Membrane dynamics of a myelin-like giant multilamellar vesicle applicable to a self-reproducing system. Langmuir 20, 3832–3834 (2004).
Toyota, T. et al. Population study of sizes and components of self-reproducing giant multilamellar vesicles. Langmuir 24, 3037–3044 (2008).
Kurihara, K., Takakura, K., Suzuki, K., Toyota, T. & Sugawara, T. Cell-sorting of robust self-reproducing giant vesicles tolerant to a highly ionic medium. Soft Matter 6, 1888–1891 (2010).
Shohda, K. et al. Compartment size dependence of performance of polymerase chain reaction inside giant vesicle. Soft Matter 7, 3750–3753 (2011).
Gánti, T. The Principles of Life (Oxford Univ. Press, 2003).
de Souza, T. P., Stano, P. & Luisi, P. L. The minimal size of liposome-based model cells brings about remarkably enhanced entrapment and protein synthesis. ChemBioChem 11, 1056–1063 (2010).
Zipper, H., Brunner, H., Bernhagen, J. & Vitzthum, F. Investigations on DNA intercalation and surface binding by SYBR Green I, its structure determination and methodological implications. Nucleic Acids Res. 32, e103 (2004).
Fuhrhop, J-H. & Wang, T. Bolaamphiphiles. Chem. Rev. 104, 2901–2937 (2004).
Rädler, J. O., Koltover, I., Salditt, T., & Safinya, C. R. Structure of DNA–cationic liposome complexes: DNA intercalation in multilamellar membranes in distinct interhelical packing regimes. Science 275, 810–814 (1997).
Angelova, M. I. & Tsoneva, I. Interactions of DNA with giant liposomes. Chem. Phys. Lipids 101, 123–137 (1999).
Angelova, M. I., Histova, N. & Tsoneva, I. DNA-induced endocytosis upon local microinjection to giant unilamellar cationic vesicles. Eur. Biophys. J. 28, 142–150 (1999).
Ogden, G. B., Pratt, M. J. & Schaechter, M. The replicative origin of the E. coli chromosome binds to cell membranes only when hemimethylated. Cell 54, 127–135 (1988).
Maru, N., Shohda, K. & Sugawara, T. Successive fusion of vesicles aggregated by DNA duplex formation in the presence of Triton X-100. Chem. Lett. 37, 340–341 (2008).
Pantos, A., Tsiourvas, D., Paleos, C. M. & Nounesis, G. Enhanced drug transport from unilamellar liposomes induced by molecular recognition of their lipid membranes. Langmuir 21, 6696–6702 (2005).
Acknowledgements
The authors acknowledge financial support from KAKENHI (Grant-in Aid for Scientific Research) for Priority Area ‘Soft Matter Physics’ (area no. 463) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan. The authors also thank M.M. Hanczyc for helpful discussions.
Author information
Authors and Affiliations
Contributions
T.S., K.K. and K.Su. conceived and designed the experiments. K.K. performed experiments. M.T. contributed the protocol. K.Su. contributed analysis. T.T. and K.Sh. contributed discussion of the data. T.S. wrote the paper. All authors discussed the results and commented on the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary information
Supplementary information (PDF 859 kb)
Supplementary information
Supplementary Movie S1 (MOV 16976 kb)
Rights and permissions
About this article
Cite this article
Kurihara, K., Tamura, M., Shohda, Ki. et al. Self-reproduction of supramolecular giant vesicles combined with the amplification of encapsulated DNA. Nature Chem 3, 775–781 (2011). https://doi.org/10.1038/nchem.1127
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nchem.1127
This article is cited by
-
Superstructural ordering in self-sorting coacervate-based protocell networks
Nature Chemistry (2024)
-
Investigation of artificial cells containing the Par system for bacterial plasmid segregation and inheritance mimicry
Nature Communications (2024)
-
Small-molecule autocatalysis drives compartment growth, competition and reproduction
Nature Chemistry (2024)
-
From autocatalysis to survival of the fittest in self-reproducing lipid systems
Nature Reviews Chemistry (2023)
-
Synthesising a minimal cell with artificial metabolic pathways
Communications Chemistry (2023)