Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Exponential growth and selection in self-replicating materials from DNA origami rafts

Nature Materials volume 16, pages 993–997 (2017)Cite this article

Subjects

Abstract

Self-replication and evolution under selective pressure are inherent phenomena in life, and but few artificial systems exhibit these phenomena1,2,3,4,5,6,7,8,9,10,11,12,13,14,15,16,17. We have designed a system of DNA origami rafts that exponentially replicates a seed pattern, doubling the copies in each diurnal-like cycle of temperature and ultraviolet illumination, producing more than 7 million copies in 24 cycles. We demonstrate environmental selection in growing populations by incorporating pH-sensitive binding in two subpopulations. In one species, pH-sensitive triplex DNA bonds enable parent–daughter templating, while in the second species, triplex binding inhibits the formation of duplex DNA templating. At pH 5.3, the replication rate of species I is ∼1.3–1.4 times faster than that of species II. At pH 7.8, the replication rates are reversed. When mixed together in the same vial, the progeny of species I replicate preferentially at pH 7.8; similarly at pH 5.3, the progeny of species II take over the system. This addressable selectivity should be adaptable to the selection and evolution of multi-component self-replicating materials in the nanoscopic-to-microscopic size range.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: DNA origami raft design and self-replication cycling.
Figure 2: Self-replication of DNA seeds.
Figure 3: Self-replication controlled by intra- and inter-molecular DNA triplex.
Figure 4: Self-replication enabling selection.

Similar content being viewed by others

References

  1. Lincoln, T. A. & Joyce, G. F. Self-sustained replication of an RNA enzyme. Science 323, 1229–1232 (2009).

    Article  CAS  Google Scholar 

  2. Wintner, E. A., Conn, M. M. & Rebek, J. Jr Studies in molecular replication. Acc. Chem. Res. 27, 198–203 (1994).

    Article  CAS  Google Scholar 

  3. Mast, C. B., Schink, S., Gerland, U. & Braun, D. Escalation of polymerization in a thermal gradient. Proc. Natl Acad. Sci. USA 110, 8030–8035 (2013).

    Article  CAS  Google Scholar 

  4. Schulman, R., Yurke, B. & Winfree, E. Robust self-replication of combinatorial information via crystal growth and scission. Proc. Natl Acad. Sci. USA 109, 6405–6410 (2012).

    Article  CAS  Google Scholar 

  5. Lin, C. et al. In vivo cloning of artificial DNA nanostructures. Proc. Natl Acad. Sci. USA 105, 17626–17631 (2008).

    Article  CAS  Google Scholar 

  6. Lee, D. H., Severin, K., Yokobayashi, Y. & Ghadiri, M. R. Emergence of symbiosis in peptide self-replication through a peptide hypercyclic network. Nature 390, 591–594 (1997).

    Article  CAS  Google Scholar 

  7. Eckardt, L. H. et al. Chemical copying of connectivity. Nature 420, 286 (2002).

    Article  CAS  Google Scholar 

  8. Wang, T. et al. Self-replication of information-bearing nanoscale patterns. Nature 478, 225–228 (2011).

    Article  CAS  Google Scholar 

  9. Leunissen, M. E. et al. Towards self-replicating materials of DNA-functionalized colloids. Soft Matter 5, 2422–2430 (2009).

    Article  CAS  Google Scholar 

  10. Levy, M. & Ellington, A. D. Exponential growth by cross-catalytic cleavage of deoxyribozymogens. Proc. Natl Acad. Sci. USA 100, 6416–6421 (2003).

    Article  CAS  Google Scholar 

  11. Wochner, A., Attwater, J., Coulson, A. & Holliger, P. Ribozyme-catalyzed transcription of an active ribozyme. Science 332, 209–212 (2011).

    Article  CAS  Google Scholar 

  12. Kim, J., Lee, J., Hamada, S., Murata, S. & Park, S. H. Self-replication of DNA rings. Nat. Nanotech. 10, 528–533 (2015).

    Article  CAS  Google Scholar 

  13. Vaidya, N. et al. Spontaneous network formation among cooperative RNA replicators. Nature 491, 72–77 (2012).

    CAS  Google Scholar 

  14. Adamala, K. & Szostak, J. W. Nonenzymatic template-directed RNA synthesis inside model protocells. Science 342, 1098–1100 (2013).

    Article  CAS  Google Scholar 

  15. Li, T. & Nicolaou, K. C. Chemical self-replication of palindromic duplex DNA. Nature 369, 218–221 (1994).

    Article  CAS  Google Scholar 

  16. Luther, A., Brandsch, R. & von Kiedrowski, G. Surface-promoted replication and exponential amplification of DNA analogues. Nature 396, 245–248 (1998).

    Article  CAS  Google Scholar 

  17. Colomb-Delsuc, M., Mattia, E., Sadownik, J. W. & Otto, S. Exponential self-replication enabled through a fibre elongation/breakage mechanism. Nat. Commun. 6, 7427 (2015).

    Article  CAS  Google Scholar 

  18. Ellington, A. D. & Szostak, J. W. In vitro selection of RNA molecules that bind to specific ligands. Nature 346, 818–822 (1990).

    Article  CAS  Google Scholar 

  19. Tuerk, C. & Gold, L. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249, 505–510 (1990).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  21. Rothemund, P. W. K. Folding DNA to create nanoscale shapes and patterns. Nature 440, 297–302 (2006).

    Article  CAS  Google Scholar 

  22. Yoshimura, R. & Fujimoto, K. Ultrafast reversible photo-cross-linking reaction: toward in situ DNA manipulation. Org. Lett. 10, 3227–3230 (2008).

    Article  CAS  Google Scholar 

  23. Rusling, D. A. et al. Functionalizing designer DNA crystals with a triple-helical veneer. Angew. Chem. Int. Ed. 53, 3979–3982 (2014).

    Article  CAS  Google Scholar 

  24. Amodio, A. et al. Rational design of pH-controlled DNA strand displacement. J. Am. Chem. Soc. 136, 16469–16472 (2014).

    Article  CAS  Google Scholar 

  25. Wu, N. & Willner, I. pH-stimulated reconfiguration and structural isomerization of origami dimer and trimer systems. Nano Lett. 16, 6650–6655 (2016).

    Article  CAS  Google Scholar 

  26. Adleman, L. M. Molecular computation of solutions to combinatorial problems. Science 266, 1021–1024 (1994).

    Article  CAS  Google Scholar 

  27. Sacanna, S., Irvine, W. T. M., Chaikin, P. M. & Pine, D. J. Lock and key colloids. Nature 464, 575–578 (2010).

    Article  CAS  Google Scholar 

  28. Douglas, S. M. et al. Rapid prototyping of 3D DNA-origami shapes with caDNAno. Nucleic Acids Res. 37, 5001–5006 (2009).

    Article  CAS  Google Scholar 

  29. Wei, B., Wang, Z. & Mi, Y. Uniquimer: a de novo DNA sequence generation computer software for DNA self-assembly. J. Comput. Theoret. Nanosci. 4, 133–141 (2007).

    CAS  Google Scholar 

Download references

Acknowledgements

We would like to acknowledge W. Liu, D. Niu and Y. Zhang for useful discussions. This research has been supported primarily by DOE DE-SC0007991 (PMC, NCS) for initiation, design, analysis and imaging, and partially by grant GBMF3849 from the Gordon and Betty Moore Foundation (PMC, NCS) for origami preparation and characterization, GM-29554 from NIGMS, grants CMMI-1120890 and CCF-1117210 from the NSF, MURI W911NF-11-1-0024 from ARO, grants N000141110729 and N000140911118 from ONR (NCS) for sequence design, DNA synthesis, purification and characterization. Y.M. and X.H. acknowledge the support by the Earmarked Grant from the University Grant Council of the Hong Kong Government, RGC 16302415, and the China 985 Grant of Tongji University. X.H. was supported partially by the MRSEC Program of the National Science Foundation under Award Number DMR-1420073 for pH-sensitive sequence design and characterization. We also wish to acknowledge the support of the National Science Foundation Academic Research Infrastructure program through Award No. CMMI-0957834.

Author information

Authors and Affiliations

  1. Department of Chemistry, New York University, New York, New York, 10003, USA

    Xiaojin He, Ruojie Sha, Rebecca Zhuo & Nadrian C. Seeman

  2. Center for Soft Matter Research, New York University, New York, New York 10003, USA

    Xiaojin He, Rebecca Zhuo & Paul M. Chaikin

  3. Department of Chemical and Biomolecular Engineering, Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong

    Xiaojin He & Yongli Mi

  4. Department of Chemistry, Tongji University, Shanghai, 100024, China

    Xiaojin He & Yongli Mi

Authors
  1. Xiaojin He
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ruojie Sha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rebecca Zhuo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yongli Mi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paul M. Chaikin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nadrian C. Seeman
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

X.H., R.S., N.C.S. and P.M.C. designed the experiments. X.H., R.S. and R.Z. performed the experiments, and all of the authors analysed data and wrote the manuscript.

Corresponding authors

Correspondence to Paul M. Chaikin or Nadrian C. Seeman.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 1296 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

He, X., Sha, R., Zhuo, R. et al. Exponential growth and selection in self-replicating materials from DNA origami rafts. Nature Mater 16, 993–997 (2017). https://doi.org/10.1038/nmat4986

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nmat4986

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing