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.

  • Article
  • Published:

Step-defect guided delivery of DNA to a graphene nanopore

Nature Nanotechnology volume 14, pages 858–865 (2019)Cite this article

Subjects

Abstract

Precision placement and transport of biomolecules are critical to many single-molecule manipulation and detection methods. One such method is nanopore sequencing, in which the delivery of biomolecules towards a nanopore controls the method’s throughput. Using all-atom molecular dynamics, here we show that the precision transport of biomolecules can be realized by utilizing ubiquitous features of graphene surface-step defects that separate multilayer domains. Subject to an external force, we found that adsorbed DNA moved much faster down a step defect than up, and even faster along the defect edge, regardless of whether the motion was produced by a mechanical force or a solvent flow. We utilized this direction dependency to demonstrate a mechanical analogue of an electric diode and a system for delivering DNA molecules to a nanopore. The defect-guided delivery principle can be used for the separation, concentration and storage of scarce biomolecular species, on-demand chemical reactions and nanopore sensing.

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

Fig. 1: DNA displacement and aggregation at defects along the surface of HOPG imaged using AFM.
Fig. 2: Forced migration of a DNA strand over a step defect.
Fig. 3: Robustness of the step-defect-induced asymmetry of forced displacement.
Fig. 4: Hydrophobic origin of the direction dependence of a defect crossing.
Fig. 5: Rectification of DNA displacement on a step-defect ladder.
Fig. 6: Guided delivery of ssDNA to a graphene nanopore.

Similar content being viewed by others

Data availability

The data that support the plots within this paper and other findings of this study are available from the corresponding author upon reasonable request.

References

  1. Han, J. & Craighead, H. G. Separation of long DNA molecules in a microfabricated entropic trap array. Science 288, 1026–1029 (2000).

    Article  CAS  Google Scholar 

  2. Huang, L. R., Cox, E. C., Austin, R. H. & Sturm, J. C. Continuous particle separation through deterministic lateral displacement. Science 304, 987–990 (2004).

    Article  CAS  Google Scholar 

  3. Fu, J., Schoch, R. B., Stevens, A. L., Tannenbaum, S. R. & Han, J. A patterned anisotropic nanofluidic sieving structure for continuous-flow separation of DNA and proteins. Nat. Nanotechnol. 2, 121–128 (2007).

    Article  CAS  Google Scholar 

  4. Hong, J. W., Studer, V., Hang, G., Anderson, W. F. & Quake, S. R. A nanoliter-scale nucleic acid processor with parallel architecture. Nat. Biotechnol. 22, 435 (2004).

    Article  CAS  Google Scholar 

  5. Sarkar, A., Kolitz, S., Lauffenburger, D. A. & Han, J. Microfluidic probe for single-cell analysis in adherent tissue culture. Nat. Commun. 5, 3421 (2014).

    Article  Google Scholar 

  6. Fan, X. & White, I. M. Optofluidic microsystems for chemical and biological analysis. Nat. Photon. 5, 591 (2011).

    Article  CAS  Google Scholar 

  7. Wang, C. et al. Wafer-scale integration of sacrificial nanofluidic chips for detecting and manipulating single DNA molecules. Nat. Commun. 8, 14243 (2017).

    Article  CAS  Google Scholar 

  8. Branton, D. et al. The potential and challenges of nanopore sequencing. Nat. Biotechnol. 26, 1146–1153 (2008).

    Article  CAS  Google Scholar 

  9. Wanunu, M., Morrison, W., Rabin, Y., Grosberg, A. Y. & Meller, A. Electrostatic focusing of unlabelled DNA into nanoscale pores using a salt gradient. Nat. Nanotechnol. 5, 165–169 (2010).

    Google Scholar 

  10. Kasianowicz, J. J., Brandin, E., Branton, D. & Deamer, D. W. Characterization of individual polynucleotide molecules using a membrane channel. Proc. Natl Acad. Sci. USA 93, 13770–13773 (1996).

    Article  CAS  Google Scholar 

  11. Akeson, M., Branton, D., Kasianowicz, J. J., Brandin, E. & Deamer, D. W. Microsecond time-scale discrimination among polycytidylic acid, polyadenylic acid, and polyuridylic acid as homopolymers or as segments within single RNA molecules. Biophys. J. 77, 3227–3233 (1999).

    Article  CAS  Google Scholar 

  12. Meller, A., Nivon, L., Brandin, E., Golovchenko, J. & Branton, D. Rapid nanopore discrimination between single polynucleotide molecules. Proc. Natl Acad. Sci. USA 97, 1079–1084 (2000).

    Article  CAS  Google Scholar 

  13. Manrao, E. A. et al. Reading DNA at single-nucleotide resolution with a mutant MspA nanopore and phi29 DNA polymerase. Nat. Biotechnol. 30, 349–353 (2012).

    Article  CAS  Google Scholar 

  14. Schneider, G. F. et al. Tailoring the hydrophobicity of graphene for its use as nanopores for DNA translocation. Nat. Commun. 4, 3619 (2013).

    Google Scholar 

  15. Garaj, S., Liu, S., Golovchenko, J. A. & Branton, D. Molecule-hugging graphene nanopores. Proc. Natl Acad. Sci. USA 110, 12192–12196 (2013).

    Article  CAS  Google Scholar 

  16. Shan, Y. P. et al. Surface modification of graphene nanopores for protein translocation. Nanotechnology 24, 495102 (2013).

    Article  CAS  Google Scholar 

  17. Laszlo, A. H. et al. Decoding long nanopore sequencing reads of natural DNA. Nat. Biotechnol. 32, 829–833 (2014).

    Article  CAS  Google Scholar 

  18. Jain, M. et al. Improved data analysis for the MinION nanopore sequencer. Nat. Methods 12, 351–356 (2015).

    Article  CAS  Google Scholar 

  19. Lagerqvist, J., Zwolak, M. & Di Ventra, M. Fast DNA sequencing via transverse electronic transport. Nano Lett. 6, 779–782 (2006).

    Article  CAS  Google Scholar 

  20. Gracheva, M. E. et al. Simulation of the electric response of DNA translocation through a semiconductor nanopore-capacitor. Nanotechnology 17, 622–633 (2006).

    Article  CAS  Google Scholar 

  21. Postma, H. W. C. Rapid sequencing of individual DNA molecules in graphene nanogaps. Nano Lett. 10, 420–425 (2010).

    Article  CAS  Google Scholar 

  22. Huang, S. et al. Identifying single bases in a DNA oligomer with electron tunnelling. Nat. Nanotechnol. 5, 868–873 (2010).

    Article  CAS  Google Scholar 

  23. Saha, K., Drndić, M. & Nikolić, B. K. DNA base-specific modulation of microampere transverse edge currents through a metallic graphene nanoribbon with a nanopore. Nano Lett. 12, 50–55 (2012).

    Article  CAS  Google Scholar 

  24. Kim, M. J., Wanunu, M., Bell, D. C. & Meller, A. Rapid fabrication of uniform size nanopores and nanopore arrays for parallel DNA analysis. Adv. Mater. 18, 3149–3153 (2006).

    Article  CAS  Google Scholar 

  25. Dekker, C. Solid-state nanopores. Nat. Nanotechnol. 2, 209–215 (2007).

    Article  CAS  Google Scholar 

  26. Liu, K., Feng, J., Kis, A. & Radenovic, A. Atomically thin molybdenum disulfide nanopores with high sensitivity for DNA translocation. ACS Nano 8, 2504–2511 (2014).

    Article  CAS  Google Scholar 

  27. Zhou, Z. et al. DNA translocation through hydrophilic nanopore in hexagonal boron nitride. Sci. Rep. 3, 3287 (2013).

    Article  Google Scholar 

  28. Garaj, S. et al. Graphene as a subnanometre trans-electrode membrane. Nature 467, 190–193 (2010).

    Article  CAS  Google Scholar 

  29. Merchant, C. A. et al. DNA translocation through graphene nanopores. Nano Lett. 10, 2915–2921 (2010).

    Article  CAS  Google Scholar 

  30. Schneider, G. F. et al. DNA translocation through graphene nanopores. Nano Lett. 10, 3163–3167 (2010).

    Article  CAS  Google Scholar 

  31. Traversi, F. et al. Detecting the translocation of DNA through a nanopore using graphene nanoribbons. Nat. Nanotechnol. 8, 939–945 (2013).

    Article  CAS  Google Scholar 

  32. Novoselov, K. S. et al. Electric field effect in atomically thin carbon films. Science 306, 666–669 (2004).

    Article  CAS  Google Scholar 

  33. Brett, A. M. O. & Paquim, A.-M. C. DNA imaged on a HOPG electrode surface by AFM with controlled potential. Bioelectrochemistry 66, 117–124 (2005).

    Article  Google Scholar 

  34. Adamcik, J., Klinov, D. V., Witz, G., Sekatskii, S. K. & Dietler, G. Observation of single-stranded DNA on mica and highly oriented pyrolytic graphite by atomic force microscopy. FEBS Lett. 580, 5671–5675 (2006).

    Article  CAS  Google Scholar 

  35. Wells, D. B., Belkin, M., Comer, J. & Aksimentiev, A. Assessing graphene nanopores for sequencing DNA. Nano Lett. 12, 4117–4123 (2012).

    Article  CAS  Google Scholar 

  36. Kim, H. S., Farmer, B. L. & Yingling, Y. G. Effect of graphene oxidation rate on adsorption of poly-thymine single stranded DNA. Adv. Mater. Interfaces 4, 1601168 (2017).

    Article  Google Scholar 

  37. Evans, E. & Ritchie, K. Dynamic strength of molecular adhesion bonds. Biophys. J. 72, 1541–1555 (1997).

    Article  CAS  Google Scholar 

  38. Wang, C. et al. Hydrodynamics of diamond-shaped gradient nanopillar arrays for effective DNA translocation into nanochannels. ACS Nano 9, 1206–1218 (2015).

    Article  CAS  Google Scholar 

  39. Manohar, S. et al. Peeling single-stranded DNA from graphite surface to determine oligonucleotide binding energy by force spectroscopy. Nano Lett. 8, 4365–4372 (2008).

    Article  CAS  Google Scholar 

  40. Lee, J.-H., Choi, Y.-K., Kim, H.-J., Scheicher, R. H. & Cho, J.-H. Physisorption of DNA nucleobases on h-BN and graphene: vdW-corrected DFT calculations. J. Phys. Chem. C 117, 13435–13441 (2013).

    Article  CAS  Google Scholar 

  41. Astumian, R. D. Thermodynamics and kinetics of a Brownian motor. Science 276, 917–922 (1997).

    Article  CAS  Google Scholar 

  42. Freedman, K. J., Ahn, C. W. & Kim, M. J. Detection of long and short DNA using nanopores with graphitic polyhedral edges. ACS Nano 7, 5008–5016 (2013).

    Article  CAS  Google Scholar 

  43. Wilson, J., Sloman, L., He, Z. & Aksimentiev, A. Graphene nanopores for protein sequencing. Adv. Funct. Mater. 26, 4830–4838 (2016).

    Article  CAS  Google Scholar 

  44. Viovy, J. L. Electrophoresis of DNA and other polyelectrolytes: physical mechanisms. Rev. Mod. Phys. 72, 813–872 (2000).

    Article  CAS  Google Scholar 

  45. Stein, D., van der Heyden, F. H., Koopmans, W. J. & Dekker, C. Pressure-driven transport of confined DNA polymers in fluidic channels. Proc. Natl Acad. Sci. USA 103, 15853–15858 (2006).

    Article  CAS  Google Scholar 

  46. Squires, T. M. & Quake, S. R. Microfluidics: fluid physics at the nanoliter scale. Rev. Mod. Phys. 77, 977–1026 (2005).

    Article  CAS  Google Scholar 

  47. Salaita, K. et al. Massively parallel dip–pen nanolithography with 55 000-pen two-dimensional arrays. Angew. Chem. Int. Ed. 118, 7378–7381 (2006).

    Article  Google Scholar 

  48. Jin, Z. et al. Metallized DNA nanolithography for encoding and transferring spatial information for graphene patterning. Nat. Commun. 4, 1663 (2013).

    Article  Google Scholar 

  49. Russo, C. J. & Golovchenko, J. A. Atom-by-atom nucleation and growth of graphene nanopores. Proc. Natl Acad. Sci. USA 109, 5953–5957 (2012).

    Article  CAS  Google Scholar 

  50. Sahin, R., Simsek, E. & Akturk, S. Nanoscale patterning of graphene through femtosecond laser ablation. Appl. Phys. Lett. 104, 053118 (2014).

    Article  Google Scholar 

  51. Nećas, D. & Klapetek, P. Gwyddion: an open-source software for SPM data analysis. Open Phys. 10, 181–188 (2012).

    Article  Google Scholar 

  52. Phillips, J. C. et al. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781–1802 (2005).

    Article  CAS  Google Scholar 

  53. MacKerell, A. D. Jr. Empirical force fields for biological macromolecules: overview and issues. J. Comput. Chem. 25, 1584–1604 (2004).

    Article  CAS  Google Scholar 

  54. Darden, T. A., York, D. & Pedersen, L. Particle mesh Ewald: an N log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089–10092 (1993).

    Article  CAS  Google Scholar 

  55. Koopman, E. A. & Lowe, C. P. Advantages of a Lowe–Andersen thermostat in molecular dynamics simulations. J. Chem. Phys. 124, 204103 (2006).

    Article  CAS  Google Scholar 

  56. Martyna, G. J., Tobias, D. J. & Klein, M. L. Constant pressure molecular dynamics algorithms. J. Chem. Phys. 101, 4177–4189 (1994).

    Article  CAS  Google Scholar 

  57. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 14, 33–38 (1996).

    Article  CAS  Google Scholar 

  58. He, Y. et al. Enhanced DNA sequencing performance through edge-hydrogenation of graphene electrodes. Adv. Funct. Mater. 21, 2674–2679 (2011).

    Article  CAS  Google Scholar 

  59. van Dijk, M. & Bonvin, A. M. J. J. 3D-DART: a DNA structure modelling server. Nucleic Acids Res. 37, W235–W239 (2009).

    Article  Google Scholar 

Download references

Acknowledgements

Research reported in this publication was supported by the National Human Genome Research Institute of the National Institutes of Health under award no. R01-HG007406, National Science Foundation under award no. DMR-0955959 and through a cooperative research agreement with Oxford Nanopore Technologies. The authors acknowledge supercomputer time provided through XSEDE Allocation Grant MCA05S028 and the Blue Waters petascale supercomputer system at the University of Illinois at Urbana–Champaign. A.A. thanks G. Schneider, A. Katan and C. Dekker for their help with setting up the AFM measurements, the Department of Bionanosciences at the Delft University of Technology for their hospitality and the Netherlands Organization for Scientific Research (NWO) for financial support.

Author information

Authors and Affiliations

  1. Department of Physics, University of Illinois, Urbana, IL, USA

    Manish Shankla

  2. Department of Physics, Beckman Institute for Advanced Science and Technology, University of Illinois, Urbana, IL, USA

    Aleksei Aksimentiev

Authors
  1. Manish Shankla
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aleksei Aksimentiev
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

A.A. conceived the project and carried out all the AFM measurements. M.S. carried out all the MD simulations and developed a theoretical model. A.A. and M.S. designed the computational experiments, analysed the data and co-wrote the manuscript.

Corresponding author

Correspondence to Aleksei Aksimentiev.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information: Nature Nanotechnology thanks Ralph H. Scheicher and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–9, Supplementary Note 1, captions to Supplementary Movies 1–16 and Supplementary refs. 1–3.

Supplementary Movie 1

Displacement of M13 ssDNA on freshly cleaved HOPG imaged in air using AFM. Prior to imaging, the HOPG sample was incubated with 0.1 ng ml–1 of M13 ssDNA. Still images from this animation are shown in Supplementary Fig. 1.

Supplementary Movie 2

Zoomed-in view on ssDNA aggregation and displacement. The sequence of images is the same as in Supplementary Video 1.

Supplementary Movie 3

Displacement of M13 ssDNA on freshly cleaved HOPG imaged in solution using AFM. Prior to imaging, the HOPG sample was incubated with 0.1 ng ml–1 of M13 ss-DNA. Still images from this video are shown in Fig. 1c of the main text and analysed quantitatively in Supplementary Fig. 2.

Supplementary Movie 4

Forced migration of poly(dT)20 down a step defect on a graphene membrane (grey). The CoM of the ssDNA molecule is attached to a spring and pulled with a constant velocity of 1.0 nm ns−1. The DNA molecule is shown using van der Waals (vdW) spheres coloured according to the atom type: blue (nitrogen), red (oxygen), white (hydrogen), carbon (cyan) and gold (phosphorous). The video illustrates a 25 ns fragment of an MD trajectory.

Supplementary Movie 5

Forced migration of poly(dT)20 up a step defect on a graphene membrane (grey). The CoM of the ssDNA molecule is attached to a spring and pulled with a constant velocity of 1.0 nm ns−1. The DNA molecule is shown using vdW spheres coloured according to the atom type: blue (nitrogen), red (oxygen), white (hydrogen), carbon (cyan) and gold (phosphorous). The video illustrates a 25 ns fragment of an MD trajectory.

Supplementary Movie 6

Forced migration of poly(dT)20 parallel to a step defect on a graphene membrane (grey). The CoM of the ssDNA molecule is attached to a spring and pulled with a constant velocity of 1.0 nm ns−1. The DNA molecule is shown using vdW spheres coloured according to the atom type: blue (nitrogen), red (oxygen), white (hydrogen), carbon (cyan) and gold (phosphorous). The video illustrates a 20 ns fragment of an MD trajectory.

Supplementary Movie 7

Directional displacement of a poly(dT)20 strand along a graphene membrane (grey) driven by water flow that periodically reverses direction. Multiple images of the unit cell are shown for clarity. The flow was produced by the application of a ±9.2 bar nm−1 pressure gradient. The direction of the flow alternates between pointing down (orange arrows) and up (cyan arrows) the step defect. The DNA is shown using vdW spheres coloured according to the atom type: blue (nitrogen), red (oxygen), white (hydrogen), carbon (cyan) and gold (phosphorous). The video illustrates a 110 ns MD trajectory.

Supplementary Movie 8

Forced migration of poly(dT)20 along a nanopore array in a four-layer graphene membrane (grey). Each nanopore is surrounded by three concentric single-atom step defects. The direction of the 200 pN magnitude force reverses every 3 ns. A 500 mV transmembrane bias is applied throughout the simulation. The DNA is shown using vdW spheres coloured according to the atom type: blue (nitrogen), red (oxygen), white (hydrogen), carbon (cyan) and gold (phosphorous). The video illustrates a 21 ns MD trajectory.

Supplementary Movie 9

Forced migration of poly(dT)20 along a nanopore array in a four-layer graphene membrane (grey). Each nanopore is surrounded by three concentric single-atom step defects. The direction of the 200 pN magnitude force reverses every 10 ns. A 500 mV transmembrane bias is applied throughout the simulation. The DNA is shown using vdW spheres coloured according to the atom type: blue (nitrogen), red (oxygen), white (hydrogen), carbon (cyan) and gold (phosphorous). The video illustrates a 50 ns MD trajectory.

Supplementary Movie 10

Forced migration of poly(dT)20 along a nanopore array in a four-layer graphene membrane (grey). Each nanopore is surrounded by three concentric single-atom step defects. The direction of the 400 pN magnitude force reverses every 10 ns. A 500 mV transmembrane bias is applied throughout the simulation. The DNA is shown using vdW spheres coloured according to the atom type: blue (nitrogen), red (oxygen), white (hydrogen), carbon (cyan) and gold (phosphorous). The video illustrates a 50 ns MD trajectory.

Supplementary Movie 11

Guided transport of poly(dT)20 to and from a nanopore at the centre of the spiral structure. The graphene nanostructure consists of a three-layer graphene membrane that has an atom-depth spiral pattern cutout in the outer two layers (yellow, blue). An external force of 300 pN magnitude is applied to the DNA molecule. The direction of the force changes by 90 degrees clockwise every 5 ns for a total of 26 constant force fragments. A transmembrane potential of 500 mV is applied throughout the simulation. The DNA is shown using vdW spheres coloured according to the atom type: blue (nitrogen), red (oxygen), white (hydrogen), carbon (cyan) and gold (phosphorous). The video illustrates a 130 ns MD trajectory.

Supplementary Movie 12

Guided transport of poly(dT)20 to and from a nanopore at the centre of the spiral structure. The graphene nanostructure consists of a three-layer graphene membrane that has an atom-depth spiral pattern cutout in the outer two layers (yellow, blue). An external force of 200 pN magnitude is applied to the DNA molecule. The direction of the force changes by 90 degrees clockwise every 7.5 ns for the first five constant force fragments and every 15 ns for the rest of the simulation. One accidental force reversal occurred at step 6. A transmembrane potential of 500 mV is applied throughout the simulation. The DNA is shown using vdW spheres coloured red. The video illustrates a 328 ns MD trajectory.

Supplementary Movie 13

Guided transport of poly(dT)20 to and from a nanopore at the centre of the spiral structure driven by a flow of solvent. The graphene nanostructure consists of a three-layer graphene membrane that has an atom-depth spiral pattern cutout in the outer two layers (yellow, blue). A solvent flow is produced by a pressure gradient of 3.0 bar nm−1. The direction of the force changes by 90 degrees clockwise every 5 ns. A transmembrane potential of 500 mV is applied throughout the simulation. The DNA is shown using vdW spheres coloured according to the atom type: blue (nitrogen), red (oxygen), white (hydrogen), carbon (cyan) and gold (phosphorous). The video illustrates a 234 ns MD trajectory.

Supplementary Movie 14

Guided transport of a 20-residue fragment of the α-haemolysin protein (residues 110 to 130) to the nanopore at the centre of the spiral structure. The graphene nanostructure consists of a three-layer graphene membrane that has an atom-depth spiral pattern cutout in the outer two layers (yellow, blue). An external force of 300 pN magnitude is applied to the protein fragment. The direction of the force changes by 90 degrees clockwise every 7.5 ns. The protein is shown using vdW spheres coloured according to the atom type: blue (nitrogen), red (oxygen), white (hydrogen), carbon (cyan) and yellow (sulfur). The video illustrates a 234 ns MD trajectory.

Supplementary Movie 15

Guided transport of poly(dT)20 to a nanopore at the centre of a right-angled spiral structure. The graphene nanostructure consists of a two-layer graphene membrane that has an atom-depth right-angled spiral pattern cut in the top layer (blue). An external force of 300 pN magnitude is applied to the DNA molecule. The direction of the force (indicated by the arrow in the animation) changes by 90 degrees clockwise every 5 ns. The DNA is shown using vdW spheres coloured according to the atom type: blue (nitrogen), red (oxygen), white (hydrogen), carbon (cyan) and gold (phosphorous). The video illustrates a 50 ns MD trajectory.

Supplementary Movie 16

Guided transport of poly(dT)20 to a nanopore at the centre of a right-angled spiral structure of increasing depth. The graphene nanostructure consists of eight graphene layers. Each layer contains a segment of a rectangular spiral, starting from the outermost segment. The spiral pattern increases in depth by a single atomic layer with each right-angle turn. An external force of 300 pN magnitude is applied to the DNA molecule. The direction of the force (indicated by the arrow in the animation) changes by 90 degrees clockwise every 7 ns. The DNA is shown using vdW spheres coloured according to the atom type: blue (nitrogen), red (oxygen), white (hydrogen), carbon (cyan) and gold (phosphorous). The video illustrates a 154 ns MD trajectory.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shankla, M., Aksimentiev, A. Step-defect guided delivery of DNA to a graphene nanopore. Nat. Nanotechnol. 14, 858–865 (2019). https://doi.org/10.1038/s41565-019-0514-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41565-019-0514-y

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