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Step-defect guided delivery of DNA to a graphene nanopore

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.

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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.

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.

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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

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Authors

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.

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The authors declare no competing interests.

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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.

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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.

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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

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