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
  
  
  8427-8438
  
    
      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
      
     
  
  
   
  
  
    
    
  
    
      25 May 2021
    
    
  
  
    
      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), .
  
   (doi:10.1021/acsnano.0c10658). 
  
  
   
  
  
  
  
  
   
  
    
    
      
        
          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.
         
      
      
        
          
            
  
    Text
 DNA Gold Nanoparticle Motors Demonstrate Processive Motion with Bursts of Speed Up to 50 nm Per Second
     - Accepted Manuscript
   
  
  
    
  
 
          
            
          
            
           
            
           
        
          
            
  
    Text
 Accepted paper _ACS Nano_Alisina
    
   
  
  
    
  
 
          
            
          
            
           
            
           
        
        
       
    
   
  
  
  More information
  
    
      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
        
  
    
        
          
        
    
        
          
        
    
        
          
        
    
        
          
        
    
        
          
        
    
        
          
        
    
        
          
        
    
        
          
            
              
            
          
        
    
        
          
        
    
        
          
        
    
        
          
            
              
            
          
        
    
        
          
        
    
  
  Catalogue record
  Date deposited: 23 Jul 2021 18:14
  Last modified: 28 Aug 2024 04:01
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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
              
              
                 
              
            
            
          
         
      
          
          Author:
          
            
            
              Tom Brown
            
          
        
      
          
          Author:
          
            
            
              Gabriel A. Kwong
            
          
        
      
        
      
          
          Author:
          
            
            
              Khalid Salaita
            
          
        
      
      
      
    
  
   
  
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