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Research Article

Elucidating the dynamics of polymer transport through nanopores using asymmetric salt concentrations

Martin Charron§Lucas Philipp§Liqun HeVincent Tabard-Cossa( )
Department of Physics, University of Ottawa, Ottawa, ON K1N 6N5, Canada

§ Martin Charron and Lucas Philipp contributed equally to this work.

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Graphical Abstract

Asymmetric salt concentrations are used to modulate the electrophoretic and diffusiophoretic forces inside and outside nanopores. Studying the capture and translocation of polymers through a nanopore under an applied voltage and a salt gradient lets us elucidate the complex dynamics of the polymer transport processes through nanopores.

Abstract

While notable progress has been made in recent years both experimentally and theoretically in understanding the highly complex dynamics of polymer capture and transport through nanopores, there remains significant disagreement between experimental observation and theoretical prediction that needs to be resolved. Asymmetric salt concentrations, where the concentrations of ions on each side of the membrane are different, can be used to enhance capture rates and prolong translocation times of electrophoretically driven polymers translocating through a nanopore from the low salt concentration reservoir, which are both attractive features for single-molecule analysis. However, since asymmetric salt concentrations affect the electrophoretic pull inside and outside the pore differently, it also offers a useful control parameter to elucidate the otherwise inseparable physics of the capture and translocation process. In this work, we attempt to paint a complete picture of the dynamics of polymer capture and translocation in both symmetric and asymmetric salt concentration conditions by reporting the dependence of multiple translocation metrics on voltage, polymer length, and salt concentration gradient. Using asymmetric salt concentration conditions, we experimentally observe the predictions of tension propagation theory, and infer the significant impact of the electric field outside the pore in capturing polymers and in altering polymer conformations prior to translocation.

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References

[1]

Deamer, D.; Akeson, M.; Branton, D. Three decades of nanopore sequencing. Nat. Biotechnol. 2016, 34, 518–524.

[2]

Logsdon, G. A.; Vollger, M. R.; Eichler, E. E. Long-read human genome sequencing and its applications. Nat. Rev. Genet. 2020, 21, 597–614.

[3]

Garalde, D. R.; Snell, E. A.; Jachimowicz, D.; Sipos, B.; Lloyd, J. H.; Bruce, M.; Pantic, N.; Admassu, T.; James, P.; Warland, A. et al. Highly parallel direct RNA sequencing on an array of nanopores. Nat. Methods 2018, 15, 201–206.

[4]

Branton, D.; Deamer, D. W.; Marziali, A.; Bayley, H.; Benner, S. A.; Butler, T.; Di Ventra, M.; Garaj, S.; Hibbs, A.; Huang, X. H. et al. The potential and challenges of nanopore sequencing. Nat. Biotechnol. 2008, 26, 1146–1153.

[5]

Lindsay, S. The promises and challenges of solid-state sequencing. Nat. Nanotechnol. 2016, 11, 109–111.

[6]

Xue, L.; Yamazaki, H.; Ren, R.; Wanunu, M.; Ivanov, A. P.; Edel, J. B. Solid-state nanopore sensors. Nat. Rev. Mater. 2020, 5, 931–951.

[7]

Bell, N. A. W.; Keyser, U. F. Digitally encoded DNA nanostructures for multiplexed, single-molecule protein sensing with nanopores. Nat. Nanotechnol. 2016, 11, 645–651.

[8]

Chuah, K.; Wu, Y. F.; Vivekchand, S. R. C.; Gaus, K.; Reece, P. J.; Micolich, A. P.; Gooding, J. J. et al. Nanopore blockade sensors for ultrasensitive detection of proteins in complex biological samples. Nat. Commun. 2019, 10, 2109.

[9]

Sze, J. Y. Y.; Ivanov, A. P.; Cass, A. E. G.; Edel, J. B. Single molecule multiplexed nanopore protein screening in human serum using aptamer modified DNA carriers. Nat. Commun. 2017, 8, 1552.

[10]

Raveendran, M.; Lee, A. J.; Sharma, R.; Wälti, C.; Actis, P. Rational design of DNA nanostructures for single molecule biosensing. Nat. Commun. 2020, 11, 4384.

[11]

Morin, T. J.; Mckenna, W. L.; Shropshire, T. D.; Wride, D. A.; Deschamps, J. D.; Liu, X.; Stamm, R.; Wang, H. Y.; Dunbar, W. B. A handheld platform for target protein detection and quantification using disposable nanopore strips. Sci. Rep. 2018, 8, 14834.

[12]

Varongchayakul, N.; Song, J. X.; Meller, A.; Grinstaff, M. W. Single-molecule protein sensing in a nanopore: A tutorial. Chem. Soc. Rev. 2018, 47, 8512–8524.

[13]

Yusko, E. C.; Bruhn, B. R.; Eggenberger, O. M.; Houghtaling, J.; Rollings, R. C.; Walsh, N. C.; Nandivada, S.; Pindrus, M.; Hall, A. R.; Sept, D. et al. Real-time shape approximation and fingerprinting of single proteins using a nanopore. Nat. Nanotechnol. 2017, 12, 360–367.

[14]

Ouldali, H.; Sarthak, K.; Ensslen, T.; Piguet, F.; Manivet, P.; Pelta, J.; Behrends, J. C.; Aksimentiev, A.; Oukhaled, A. Electrical recognition of the twenty proteinogenic amino acids using an aerolysin nanopore. Nat. Biotechnol. 2020, 38, 176–181.

[15]

Nivala, J.; Marks, D. B.; Akeson, M. Unfoldase-mediated protein translocation through an α-hemolysin nanopore. Nat. Biotechnol. 2013, 31, 247–250.

[16]

Alfaro, J. A.; Bohländer, P.; Dai, M. J.; Filius, M.; Howard, C. J.; Van Kooten, X. F.; Ohayon, S.; Pomorski, A.; Schmid, S.; Aksimentiev, A. et al. The emerging landscape of single-molecule protein sequencing technologies. Nat. Methods 2021, 18, 604–617.

[17]

Brinkerhoff, H.; Kang, A. S. W.; Liu, J. Q.; Aksimentiev, A.; Dekker, C. Multiple rereads of single proteins at single-amino acid resolution using nanopores. Science 2021, 374, 1509–1513.

[18]

Schmid, S.; Stömmer, P.; Dietz, H.; Dekker, C. Nanopore electro-osmotic trap for the label-free study of single proteins and their conformations. Nat. Nanotechnol. 2021, 16, 1244–1250.

[19]

Lucas, F. L. R.; Versloot, R. C. A.; Yakovlieva, L.; Walvoort, M. T. C.; Maglia, G. Protein identification by nanopore peptide profiling. Nat. Commun. 2021, 12, 5795.

[20]

Chen, K. K.; Kong, J. L.; Zhu, J. B.; Ermann, N.; Predki, P.; Keyser, U. F. Digital data storage using DNA nanostructures and solid-state nanopores. Nano Lett. 2019, 19, 1210–1215.

[21]

Cao, C.; Krapp, L. F.; Al Ouahabi, A.; König, N. F.; Cirauqui, N.; Radenovic, A.; Lutz, J. F.; Peraro, M. D. Aerolysin nanopores decode digital information stored in tailored macromolecular analytes. Sci. Adv. 2020, 6, eabc2661.

[22]

Boukhet, M.; König, N. F.; Ouahabi, A. A.; Baaken, G.; Lutz, J. F.; Behrends, J. C. Translocation of precision polymers through biological nanopores. Macromol. Rapid Commun. 2017, 38, 1700680.

[23]

Muthukumar, M. Theory of capture rate in polymer translocation. J. Chem. Phys. 2010, 132, 195101.

[24]

Rowghanian, P.; Grosberg, A. Y. Electrophoretic capture of a DNA chain into a nanopore. Phys. Rev. E 2013, 87, 042722.

[25]

Rowghanian, P.; Grosberg, A. Y. Force-driven polymer translocation through a nanopore: An old problem revisited. J. Phys. Chem. B 2011, 115, 14127–14135.

[26]

Saito, T.; Sakaue, T. Dynamical diagram and scaling in polymer driven translocation. Eur. Phys. J. E 2011, 34, 135.

[27]

Ikonen, T.; Bhattacharya, A.; Ala-Nissila, T.; Sung, W. Influence of non-universal effects on dynamical scaling in driven polymer translocation. J. Chem. Phys. 2012, 137, 085101.

[28]

Sarabadani, J.; Ikonen, T.; Ala-Nissila, T. Iso-flux tension propagation theory of driven polymer translocation: The role of initial configurations. J. Chem. Phys. 2014, 141, 214907.

[29]

Palyulin, V. V.; Ala-Nissila, T.; Metzler, R. Polymer translocation: The first two decades and the recent diversification. Soft Matter 2014, 10, 9016–9037.

[30]

Dubbeldam, J. L. A.; Rostiashvili, V. G.; Milchev, A.; Vilgis, T. A. Forced translocation of a polymer: Dynamical scaling versus molecular dynamics simulation. Phys. Rev. E 2012, 85, 041801.

[31]

Davenport, M.; Healy, K.; Pevarnik, M.; Teslich, N.; Cabrini, S.; Morrison, A. P.; Siwy, Z. S.; Létant, S. E. The role of pore geometry in single nanoparticle detection. ACS Nano 2012, 6, 8366–8380.

[32]

Bell, N. A. W.; Muthukumar, M.; Keyser, U. F. Translocation frequency of double-stranded DNA through a solid-state nanopore. Phys. Rev. E 2016, 93, 022401.

[33]

Charron, M.; Briggs, K.; King, S.; Waugh, M.; Tabard-Cossa, V. Precise DNA concentration measurements with nanopores by controlled counting. Anal. Chem. 2019, 91, 12228–12237.

[34]

Storm, A. J.; Storm, C.; Chen, J. H.; Zandbergen, H.; Joanny, J. F.; Dekker, C. Fast DNA translocation through a solid-state nanopore. Nano Lett. 2005, 5, 1193–1197.

[35]

Van Dorp, S.; Keyser, U. F.; Dekker, N. H.; Dekker, C.; Lemay, S. G. Origin of the electrophoretic force on DNA in solid-state nanopores. Nat. Phys. 2009, 5, 347–351.

[36]

Carson, S.; Wilson, J.; Aksimentiev, A.; Wanunu, M. Smooth DNA transport through a narrowed pore geometry. Biophys. J. 2014, 107, 2381–2393.

[37]

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. 2010, 5, 160–165.

[38]

Chen, K. K.; Jou, I.; Ermann, N.; Muthukumar, M.; Keyser, U. F.; Bell, N. A. W. Dynamics of driven polymer transport through a nanopore. Nat. Phys. 2021, 17, 1043–1049.

[39]

Jeon, B. J.; Muthukumar, M. Polymer capture by α-hemolysin pore upon salt concentration gradient. J. Chem. Phys. 2014, 140, 015101.

[40]

Ivica, J.; Williamson, P. T. F.; De Planque, M. R. R. Salt gradient modulation of microRNA translocation through a biological nanopore. Anal. Chem. 2017, 89, 8822–8829.

[41]

Nova, I. C.; Derrington, I. M.; Craig, J. M.; Noakes, M. T.; Tickman, B. I.; Doering, K.; Higinbotham, H.; Laszlo, A. H.; Gundlach, J. H. Investigating asymmetric salt profiles for nanopore DNA sequencing with biological porin MspA. PLoS One 2017, 12, e0181599.

[42]

Bello, J.; Mowla, M.; Troise, N.; Soyring, J.; Borgesi, J.; Shim, J. Increased dwell time and occurrence of dsDNA translocation events through solid state nanopores by LiCl concentration gradients. Electrophoresis 2019, 40, 1082–1090.

[43]

He, Y. H.; Tsutsui, M.; Scheicher, R.; Fan, C.; Taniguchi, M.; Kawai, T. Mechanism of how salt-gradient-induced charges affect the translocation of DNA molecules through a nanopore. Biophys. J. 2013, 105, 776–782.

[44]

Chou, T. Enhancement of charged macromolecule capture by nanopores in a salt gradient. J. Chem. Phys. 2009, 131, 034703.

[45]

He, Y. H.; Tsutsui, M.; Scheicher, R. H.; Miao, X. S.; Taniguchi, M. Salt-gradient approach for regulating capture-to-translocation dynamics of DNA with nanochannel sensors. ACS Sensors 2016, 1, 807–816.

[46]

Kowalczyk, S. W.; Wells, D. B.; Aksimentiev, A.; Dekker, C. Slowing down DNA translocation through a nanopore in lithium chloride. Nano Lett. 2012, 12, 1038–1044.

[47]

Rivas, F.; DeAngelis, P. L.; Rahbar, E.; Hall, A. R. Optimizing the sensitivity and resolution of hyaluronan analysis with solid-state nanopores. Sci. Rep. 2022, 12, 4469.

[48]

Verschueren, D. V.; Jonsson, M. P.; Dekker, C. Temperature dependence of DNA translocations through solid-state nanopores. Nanotechnology 2015, 26, 234004.

[49]

Farahpour, F.; Maleknejad, A.; Varnik, F.; Ejtehadi, M. R. Chain deformation in translocation phenomena. Soft Matter 2013, 9, 2750–2759.

[50]

Vollmer, S. C.; De Haan, H. W. Translocation is a nonequilibrium process at all stages: Simulating the capture and translocation of a polymer by a nanopore. J. Chem. Phys. 2016, 145, 154902.

[51]
Qiao, L.; Slater, G. W. Ratcheting charged polymers through symmetric nanopores using pulsed fields: Designing a low pass filter for concentrating DNA. 2021, arXiv:2101.12712. arXiv.org e-Print archive. https://doi.org/10.48550/arXiv.2101.12712 (accessed Jun 10, 2021).
[52]

Seth, S.; Bhattacharya, A. How capture affects polymer translocation in a solitary nanopore. J. Chem. Phys. 2022, 156, 244902.

[53]

Nakane, J.; Akeson, M.; Marziali, A. Evaluation of nanopores as candidates for electronic analyte detection. Electrophoresis 2002, 23, 2592–2601.

[54]

Gershow, M.; Golovchenko, J. A. Recapturing and trapping single molecules with a solid-state nanopore. Nat. Nanotechnol. 2007, 2, 775–779.

[55]

Wong, C. T. A.; Muthukumar, M. Polymer capture by electro-osmotic flow of oppositely charged nanopores. J. Chem. Phys. 2007, 126, 164903.

[56]

McMullen, A.; Araujo, G.; Winter, M.; Stein, D. Osmotically driven and detected DNA translocations. Sci. Rep. 2019, 9, 15065.

[57]

Rankin, D. J.; Bocquet, L.; Huang, D. M. Entrance effects in concentration-gradient-driven flow through an ultrathin porous membrane. J. Chem. Phys. 2019, 151, 044705.

[58]

Lee, C.; Cottin-Bizonne, C.; Biance, A. L.; Joseph, P.; Bocquet, L.; Ybert, C. Osmotic flow through fully permeable nanochannels. Phys. Rev. Lett. 2014, 112, 244501.

[59]

Anderson, J. L. Colloid transport by interfacial forces. Annu. Rev. Fluid Mech. 1989, 21, 61–99.

[60]

Ikonen, T.; Bhattacharya, A.; Ala-Nissila, T.; Sung, W. Influence of pore friction on the universal aspects of driven polymer translocation. Europhys. Lett. 2013, 103, 38001.

[61]

Ikonen, T.; Bhattacharya, A.; Ala-Nissila, T.; Sung, W. Unifying model of driven polymer translocation. Phys. Rev. E 2012, 85, 051803.

[62]

Sakaue, T. Dynamics of polymer translocation: A short review with an introduction of weakly-driven regime. Polymers (Basel) 2016, 8, 424.

[63]

Meller, A.; Nivon, L.; Branton, D. Voltage-driven DNA translocations through a nanopore. Phys. Rev. Lett. 2001, 86, 3435–3438.

[64]

Stellwagen, N. C.; Gelfi, C.; Righetti, P. G. The free solution mobility of DNA. Biopolymers 1997, 42, 687–703.

[65]

Tanaka, K.; Tamamushi, R. A Physico-chemical study of concentrated aqueous solutions of lithium chloride. Z. Naturforsch. A 1991, 46, 141–147.

[66]

He, L. Q.; Karau, P.; Tabard-Cossa, V. Fast capture and multiplexed detection of short multi-arm DNA stars in solid-state nanopores. Nanoscale 2019, 11, 16342–16350.

[67]

Briggs, K.; Madejski, G.; Magill, M.; Kastritis, K.; De Haan, H. W.; Mcgrath, J. L.; Tabard-Cossa, V. DNA translocations through nanopores under nanoscale preconfinement. Nano Lett. 2018, 18, 660–668.

[68]

Mihovilovic, M.; Hagerty, N.; Stein, D. Statistics of DNA capture by a solid-state nanopore. Phys. Rev. Lett. 2013, 110, 028102.

[69]

Bell, N. A. W.; Chen, K. K.; Ghosal, S.; Ricci, M.; Keyser, U. F. Asymmetric dynamics of DNA entering and exiting a strongly confining nanopore. Nat. Commun. 2017, 8, 380.

[70]

Sarabadani, J.; Ikonen, T.; Mökkönen, H.; Ala-Nissila, T.; Carson, S.; Wanunu, M. Driven translocation of a semi-flexible polymer through a nanopore. Sci. Rep. 2017, 7, 7423.

[71]

Lu, B.; Albertorio, F.; Hoogerheide, D. P.; Golovchenko, J. A. Origins and consequences of velocity fluctuations during DNA passage through a nanopore. Biophys. J. 2011, 101, 70–79.

[72]

De Haan, H. W.; Sean, D.; Slater, G. W. Reducing the variance in the translocation times by prestretching the polymer. Phys. Rev. E 2018, 98, 022501.

[73]

Sean, D.; De Haan, H. W.; Slater, G. W. Translocation of a polymer through a nanopore starting from a confining nanotube. Electrophoresis 2015, 36, 682–691.

[74]

Bandara, Y. M. N. D. Y.; Karawdeniya, B. I.; Hagan, J. T.; Chevalier, R. B.; Dwyer, J. R. Chemically functionalizing controlled dielectric breakdown silicon nitride nanopores by direct photohydrosilylation. ACS Appl. Mater. Interfaces 2019, 11, 30411–30420.

[75]

Eggenberger, O. M.; Ying, C. F.; Mayer, M. Surface coatings for solid-state nanopores. Nanoscale 2019, 11, 19636–19657.

[76]

Waugh, M.; Briggs, K.; Gunn, D.; Gibeault, M.; King, S.; Ingram, Q.; Jimenez, A. M.; Berryman, S.; Lomovtsev, D.; Andrzejewski, L. et al. Solid-state nanopore fabrication by automated controlled breakdown. Nat. Protoc. 2020, 15, 122–143.

[77]

Beamish, E.; Kwok, H.; Tabard-Cossa, V.; Godin, M. Precise control of the size and noise of solid-state nanopores using high electric fields. Nanotechnology 2012, 23, 405301.

[78]

Lin, C. Y.; Acar, E. T.; Polster, J. W.; Lin, K. B.; Hsu, J. P.; Siwy, Z. S. Modulation of charge density and charge polarity of nanopore wall by salt gradient and voltage. ACS Nano 2019, 13, 9868–9879.

[79]

Firnkes, M.; Pedone, D.; Knezevic, J.; Döblinger, M.; Rant, U. Electrically facilitated translocations of proteins through silicon nitride nanopores: Conjoint and competitive action of diffusion, electrophoresis, and electroosmosis. Nano Lett. 2010, 10, 2162–2167.

[80]

Forstater, J. H.; Briggs, K.; Robertson, J. W. F.; Ettedgui, J.; Marie-Rose, O.; Vaz, C.; Kasianowicz, J. J.; Tabard-Cossa, V.; Balijepalli, A. MOSAIC: A modular single-molecule analysis interface for decoding multistate nanopore data. Anal. Chem. 2016, 88, 11900–11907.

Nano Research
Pages 9943-9953
Cite this article:
Charron M, Philipp L, He L, et al. Elucidating the dynamics of polymer transport through nanopores using asymmetric salt concentrations. Nano Research, 2022, 15(11): 9943-9953. https://doi.org/10.1007/s12274-022-4886-3
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Received: 12 January 2022
Revised: 03 August 2022
Accepted: 09 August 2022
Published: 01 September 2022
© Tsinghua University Press 2022
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