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DNA gold nanoparticle motors demonstrate processive motion with bursts of speed up to 50 nm per second

DNA gold nanoparticle motors demonstrate processive motion with bursts of speed up to 50 nm per second
DNA gold nanoparticle motors demonstrate processive motion with bursts of speed up to 50 nm per second

Synthetic motors that consume chemical energy to produce mechanical work offer potential applications in many fields that span from computing to drug delivery and diagnostics. Among the various synthetic motors studied thus far, DNA-based machines offer the greatest programmability and have shown the ability to translocate micrometer-distances in an autonomous manner. DNA motors move by employing a burnt-bridge Brownian ratchet mechanism, where the DNA "legs"hybridize and then destroy complementary nucleic acids immobilized on a surface. We have previously shown that highly multivalent DNA motors that roll offer improved performance compared to bipedal walkers. Here, we use DNA-gold nanoparticle conjugates to investigate and enhance DNA nanomotor performance. Specifically, we tune structural parameters such as DNA leg density, leg span, and nanoparticle anisotropy as well as buffer conditions to enhance motor performance. Both modeling and experiments demonstrate that increasing DNA leg density boosts the speed and processivity of motors, whereas DNA leg span increases processivity and directionality. By taking advantage of label-free imaging of nanomotors, we also uncover Lévy-Type motion where motors exhibit bursts of translocation that are punctuated with transient stalling. Dimerized particles also demonstrate more ballistic trajectories confirming a rolling mechanism. Our work shows the fundamental properties that control DNA motor performance and demonstrates optimized motors that can travel multiple micrometers within minutes with speeds of up to 50 nm/s. The performance of these nanoscale motors approaches that of motor proteins that travel at speeds of 100-1000 nm/s, and hence this work can be important in developing protocellular systems as well next generation sensors and diagnostics.

burnt bridge Brownian ratchet, dynamic DNA nanotechnology, gold nanoparticle, spherical nucleic acids, synthetic DNA motors
1936-0851
8427-8438
Bazrafshan, Alisina
27aff2d4-dcff-4358-b3a2-77b00314d38a
Kyriazi, Maria-Eleni
01916df9-2aa2-424e-9e58-4d0db900e456
Holt, Brandon Alexander
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Deng, Wenxiao
3abee492-41b9-4578-b789-4f66a9c75f4a
Piranej, Selma
707d18d3-baf0-43f3-b168-079270e5599b
Su, Hanquan
825e2a56-2dad-4770-b8c4-1c4e54e6d81c
Hu, Yuesong
40837d56-f436-49a9-a5ce-c58b25749ad7
El-Sagheer, Afaf
05b8295a-64ad-4fdf-ad57-c34934a46c04
Brown, Tom
1cd7df32-b945-4ca1-8b59-a51a30191472
Kwong, Gabriel A.
b98fb36b-4d6f-4773-97a2-6b16ad8d4c09
Kanaras, Antonios G.
667ecfdc-7647-4bd8-be03-a47bf32504c7
Salaita, Khalid
ed85abdd-3cbd-4262-9dc3-a03fc731df5d
Bazrafshan, Alisina
27aff2d4-dcff-4358-b3a2-77b00314d38a
Kyriazi, Maria-Eleni
01916df9-2aa2-424e-9e58-4d0db900e456
Holt, Brandon Alexander
a75d75ad-1581-4a7d-a2e2-12b73cefb95d
Deng, Wenxiao
3abee492-41b9-4578-b789-4f66a9c75f4a
Piranej, Selma
707d18d3-baf0-43f3-b168-079270e5599b
Su, Hanquan
825e2a56-2dad-4770-b8c4-1c4e54e6d81c
Hu, Yuesong
40837d56-f436-49a9-a5ce-c58b25749ad7
El-Sagheer, Afaf
05b8295a-64ad-4fdf-ad57-c34934a46c04
Brown, Tom
1cd7df32-b945-4ca1-8b59-a51a30191472
Kwong, Gabriel A.
b98fb36b-4d6f-4773-97a2-6b16ad8d4c09
Kanaras, Antonios G.
667ecfdc-7647-4bd8-be03-a47bf32504c7
Salaita, Khalid
ed85abdd-3cbd-4262-9dc3-a03fc731df5d

Bazrafshan, Alisina, Kyriazi, Maria-Eleni, Holt, Brandon Alexander, Deng, Wenxiao, Piranej, Selma, Su, Hanquan, Hu, Yuesong, El-Sagheer, Afaf, Brown, Tom, Kwong, Gabriel A., Kanaras, Antonios G. and Salaita, Khalid (2021) DNA gold nanoparticle motors demonstrate processive motion with bursts of speed up to 50 nm per second. ACS Nano, 15 (5), 8427-8438. (doi:10.1021/acsnano.0c10658).

Record type: Article

Abstract

Synthetic motors that consume chemical energy to produce mechanical work offer potential applications in many fields that span from computing to drug delivery and diagnostics. Among the various synthetic motors studied thus far, DNA-based machines offer the greatest programmability and have shown the ability to translocate micrometer-distances in an autonomous manner. DNA motors move by employing a burnt-bridge Brownian ratchet mechanism, where the DNA "legs"hybridize and then destroy complementary nucleic acids immobilized on a surface. We have previously shown that highly multivalent DNA motors that roll offer improved performance compared to bipedal walkers. Here, we use DNA-gold nanoparticle conjugates to investigate and enhance DNA nanomotor performance. Specifically, we tune structural parameters such as DNA leg density, leg span, and nanoparticle anisotropy as well as buffer conditions to enhance motor performance. Both modeling and experiments demonstrate that increasing DNA leg density boosts the speed and processivity of motors, whereas DNA leg span increases processivity and directionality. By taking advantage of label-free imaging of nanomotors, we also uncover Lévy-Type motion where motors exhibit bursts of translocation that are punctuated with transient stalling. Dimerized particles also demonstrate more ballistic trajectories confirming a rolling mechanism. Our work shows the fundamental properties that control DNA motor performance and demonstrates optimized motors that can travel multiple micrometers within minutes with speeds of up to 50 nm/s. The performance of these nanoscale motors approaches that of motor proteins that travel at speeds of 100-1000 nm/s, and hence this work can be important in developing protocellular systems as well next generation sensors and diagnostics.

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DNA Gold Nanoparticle Motors Demonstrate Processive Motion with Bursts of Speed Up to 50 nm Per Second - Accepted Manuscript
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Accepted paper _ACS Nano_Alisina
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Accepted/In Press date: 22 April 2021
Published date: 25 May 2021
Additional Information: Funding Information: We thank Armina Fani for her help in creating the artwork demonstrating the Scheme in Figure 1a and the TOC figure. We thank Dr. Justin Burton for access to the laser cutter in his lab. Furthermore, we acknowledge support from Robert P. Apkarian Integrated Electron Microscopy Core and Emory University Integrated Cellular Imaging Microscopy Core. We thank Dr. Guram Gogia (Guga) for insightful conversations that led us to the literature and physical principles of Lévy flights. K.S. acknowledges support from NSF DMR 1905947, NIH R01 GM124472, and NSF- CHE 2004126. A.G.K. acknowledges financial support from the Biotechnology and Biological Sciences Research Council (BB/P017711/1). B.A.H. acknowledges support from the NSF GRFP and the Georgia Tech President’s Fellowship. This material is based upon work supported by the National Science Foundation Graduate Research Fellowship under Grant No. DGE-1650044 (B.A.H.). G.A.K. holds a Career Award at the Scientific Interface from the Burroughs Wellcome Fund. Publisher Copyright: © 2021 American Chemical Society. All rights reserved.
Keywords: burnt bridge Brownian ratchet, dynamic DNA nanotechnology, gold nanoparticle, spherical nucleic acids, synthetic DNA motors

Identifiers

Local EPrints ID: 450356
URI: http://eprints.soton.ac.uk/id/eprint/450356
ISSN: 1936-0851
PURE UUID: cc6cd022-48bb-408d-a553-162af895ee08
ORCID for Afaf El-Sagheer: ORCID iD orcid.org/0000-0001-8706-1292
ORCID for Antonios G. Kanaras: ORCID iD orcid.org/0000-0002-9847-6706

Catalogue record

Date deposited: 23 Jul 2021 18:14
Last modified: 06 Jun 2024 04:13

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Contributors

Author: Alisina Bazrafshan
Author: Maria-Eleni Kyriazi
Author: Brandon Alexander Holt
Author: Wenxiao Deng
Author: Selma Piranej
Author: Hanquan Su
Author: Yuesong Hu
Author: Afaf El-Sagheer ORCID iD
Author: Tom Brown
Author: Gabriel A. Kwong
Author: Khalid Salaita

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