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Electric field of DNA in solution: who is in charge?

Published 7 Mar 2024 in cond-mat.soft, physics.bio-ph, and physics.chem-ph | (2403.04949v1)

Abstract: In solution, DNA is a highly charged macromolecule which bears a unit of negative charge on each phosphate of its sugar-phosphate backbone. Although partially compensated by counterions adsorbed at or condensed near it, DNA still produces a substantial electric field in its vicinity, which is screened by buffer electrolyte at longer distances from the DNA. Such field has been explored so far predominantly within the scope of a primitive model of the electrolytic solution, not considering more complicated structural effects of the water solvent. In this paper we investigate the distribution of electric field around DNA using linear response nonlocal electrostatic theory, applied here for helix-specific charge distributions, and compare the predictions of such theory with specially performed fully atomistic large scale molecular dynamics simulations. The main finding of this study is that oscillations in the electrostatic potential distribution are present around DNA, caused by the overscreening effect of structured water. Surprisingly, electrolyte ions at physiological concentrations do not strongly disrupt these oscillations, and rather distribute according to these oscillating patterns, indicating that water structural effects dominate the short-range electrostatics. We also show that (i) structured water adsorbed in the grooves of DNA lead to a positive electrostatic potential core, (ii) the Debye length some 10 {\AA} away from the DNA is reduced, effectively renormalised by the helical pitch of the DNA, and (iii) Lorentzian contributions to the nonlocal dielectric function of water, effectively reducing the dielectric constant close to the DNA, enhances the overall electric field. The impressive agreement between the atomistic simulations and the developed theory substantiates the use of nonlocal electrostatics when considering solvent effects in molecular processes in biology.

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References (56)
  1. G. S. Manning, The molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides, Q. Rev. Biophys. 11, 179 (1978).
  2. M. D. Frank-Kamenetskiǐ, V. V. Anshelevich, and A. V. Lukashin, Polyelectrolyte model of DNA, Sov. Phys. Usp. 30, 317 (1987).
  3. A. Y. Grosberg, T. T. Nguyen, and B. I. Shklovskii, The physics of charge inversion in chemical and biological systems, Rev. Mod. Phys. 74, 329 (2002).
  4. K. A. Sharp and B. Honig, Electrostatic interactions in macromolecules: Theory and applications, Annu. Rev. Biophys. Biophys. Chem. 19, 301 (1990).
  5. D. Soumpasis, Debye-Hückel theory of model polyelectrolytes, J. Chem. Phys. 69, 3190 (1978).
  6. A. A. Kornyshev and S. Leikin, Electrostatic zipper motif for DNA aggregation, Phys. Rev. Lett. 82, 4138 (1999).
  7. A. A. Kornyshev and S. Leikin, Electrostatic interaction between helical molecules in dense aggregates: An impetus for DNA poly- and meso-morphism, Proc. Natl. Acad. Sci. USA 95, 13579 (1998a).
  8. A. A. Kornyshev, S. Leikin, and S. V. Malinin, Chiral interaction and cholesteric liquid crystals of DNA, European Phys. J. E. 7, 83 (2002).
  9. R. Cortini, A. A. Kornyshev, and D. J. Lee, Electrostatic braiding and homologous pairing of DNA double helices, Biophys. J. 101, 875 (2011).
  10. A. A. Kornyshev, Physics of DNA: unravelling hiddden abilities encoded in the structure of ‘the most important molecule’, Phys. Chem. Chem. Phys. 39, 12352 (2010).
  11. A. A. Kornyshev and S. Leikin, Symmetry laws for interaction between helical macromolecules, Biophys. J. 75, 2513 (1998b).
  12. A. A. Kornyshev and A. Wynveen, The homology recognition well as an innate property of DNA structure, Proc. Natl. Acad. Sci. USA 106, 4683 (2009).
  13. B. I. Shklovskii, Wigner crystal model of counterion induced bundle formation of rodlike polyelectrolytes, Phys. Rev. Lett. 82, 3268 (1999).
  14. J. Israelachvili and R. Pashley, Molecular layering of water at surfaces and origin of repulsive hydration forces, Nature 306, 249 (1983).
  15. M. R. Philpott and J. N. Glosli, Screening of charged electrodes in aqueous electrolytes, J. Electrochem. Soc. 142, L25 (1995).
  16. M. R. Philpott, J. N. Glosli, and S. B. Zhu, Molecular dynamics simulation of adsorption in electric double layers, Surf. Sci. 335, 422 (1995).
  17. E. Spohr, Computer simulation of the structure of the electrochemical double layer, J. Electroanal. Chem. 450, 327 (1998).
  18. E. Spohr, Molecular simulation of the electrochemical double layer, Electrochim. Acta 44, 1697 (1999).
  19. D. I. Dimitrov and N. D. Raev, Molecular dynamics simulations of the electrical double layer at the 1M KCl solution Hg electrode interface, J. Electroanal. Chem. 486, 1 (2000).
  20. J. G. Hedley, H. Berthoumieux, and A. A. Kornyshev, The dramatic effect of water structure on hydration forces and the electrical double layer, J. Phys. Chem. C 127, 8429 (2023).
  21. M. Watkins and B. Reischl, A simple approximation for forces exerted on an AFM tip in liquid, J. Chem. Phys. 138, 154703 (2013).
  22. K. Kuchuk and U. Sivan, Hydration structure of a single DNA molecule revealed by frequency-modulation atomic force microscopy, Nano Lett. 18, 2733 (2018).
  23. M. Karplus and J. A. McCammon, Molecular dynamics simulations of biomolecules, Nat. Struct. Biol. 9, 646 (2002).
  24. D. C. Rau, B. Lee, and V. A. Parsegian, Measurement of the repulsive force between polyelectrolyte molecules in ionic solution: hydration forces between parallel DNA double helices, Proc. Natl. Acad. Sci. USA 81, 2621 (1984).
  25. J. Yoo and A. Aksimentiev, The structure and intermolecular forces of DNA condensates, Nucleic Acids Research 44, 2036 (2016).
  26. J. Yoo and A. Aksimentiev, Competitive binding of cations to duplex DNA revealed through molecular dynamics simulations, J. Phys. Chem. B 116, 12895 (2012b).
  27. B. Jayaram and D. L. Beveridge, Modeling DNA in aqueous solutions: Theoretical and computer simulation studies on the ion atmosphere of DNA, Annu. Rev. Biophys. Biomol. Struct. 25, 367 (1996).
  28. A. A. Kornyshev, Nonlocal screening of ions in a structurized polar solvent: new aspects of solvent description in electrolyte theory, Electrochim. Acta 26, 1 (1981).
  29. A. A. Kornyshev and M. A. Vorotyntsev, Nonlocal electrostatic approach to the double layer and adsorption at the electrode/electrolyte interface, Surf. Sci. 101, 23 (1980).
  30. A. Levy, M. Bazant, and A. A. Kornyshev, Ionic activity in concentrated electrolytes: Solvent structure effect revisited, Chem. Phys. Lett. 738, 136915 (2020).
  31. A. A. Kornyshev and G. Sutmann, The shape of nonlocal dielectric function of polar liquids and the implications for thermodynamic properties of electrolytes: A comparative study, J. Chem. Phys. 104, 1524 (1996).
  32. J. E. B. Randles, The real hydration energies of ions, Trans. Faraday Soc. 52, 1573 (1956).
  33. M. V. Fedorov and A. A. Kornyshev, Unravelling the solvent response to neutral and charged solutes, Mol. Phys. 105, 1 (2007).
  34. O. V. Dolgov, D. A. Kirzhnits, and E. G. Maksimov, On an admissible sign of the static dielectric function of matter, Rev. Mod. Phys. 53, 81 (1981).
  35. R. Kjellander, The intimate relationship between the dielectric response and the decay of intermolecular correlations and surface forces in electrolytes, Soft Matter 15, 5866 (2019).
  36. R. Kjellander, Nonlocal electrostatics in ionic liquids: The key to an understanding of the screening decay length and screened interactions, J. Chem. Phys. 145, 124503 (2016).
  37. Y. A. Budkov, Statistical field theory of ion-molecular solutions, Phys. Chem. Chem. Phys. 22, 14756 (2020).
  38. A. A. Kornyshev and S. Leikin, Theory of interaction between helical molecules, J. Chem. Phys. 107, 3656 (1997).
  39. J. Jackson, Classical Electrodynamics, 3rd ed. (Wiley, New York, NY, 1999).
  40. B. Jayaram, K. A. Sharp, and B. Honig, The electrostatic potential of B-DNA, Biopolymers 28, 975 (1989).
  41. E. Harder and B. Roux, On the origin of the electrostatic potential difference at a liquid-vacuum interface, J. Chem. Phys. 129, 234706 (2008).
  42. C. O. Pabo and R. T. Sauer, Protein-dna recognition, Ann. Rev. Biochem. 53, 293 (1984).
  43. W. Humphey, A. Dalke, and K. Schulten, VMD: Visual molecular dynamics, J. Mol. Graphics 14, 33 (1996).
  44. J. Yoo and A. Aksimentiev, New tricks for old dogs: Improving the accuracy of biomolecular force fields by pair-specific corrections to non-bonded interactions, Phys. Chem. Chem. Phys. 20, 8432 (2018).
  45. P. F. Batcho, D. A. Case, and T. Schlick, Optimized particle-mesh Ewald/multiple-time step integration for molecular dynamics simulations, J. Chem. Phys. 115, 4003 (2001).
  46. T. A. Darden, D. York, and L. Pedersen, Particle mesh ewald: An N log(N) method for ewald sums in large systems, J. Chem. Phys. 98, 10089 (1993).
  47. S. Miyamoto and P. A. Kollman, SETTLE: An analytical version of the SHAKE and RATTLE algorithm for rigid water molecules, J. Comput. Chem. 13, 952 (1992).
  48. H. C. Andersen, RATTLE: A “velocity” version of the SHAKE algorithm for molecular dynamics calculations, J. Comput. Phys. 52, 24 (1983).
  49. G. J. Martyna, D. J. Tobias, and M. L. Klein, Constant pressure molecular dynamics algorithms, J. Chem. Phys. 101, 4177 (1994).
  50. A. Aksimentiev and K. Schulten, Imaging α𝛼\alphaitalic_α-hemolysin with molecular dynamics: Ionic conductance, osmotic permeability and the electrostatic potential map, Biophys. J. 88, 3745 (2005).
  51. P. A. Bopp, A. A. Kornyshev, and G. Sutmann, Static nonlocal dielectric function of liquid water, Physical Review Letters 76, 1280 (1996).
  52. P. A. Bopp, A. A. Kornyshev, and G. Sutmann, Frequency and wave-vector dependent dielectric function of water: Collective modes and relaxation spectra, J. Chem. Phys. 109, 1939 (1998).
  53. F. Sciortino, S. Sastry, and P. H. Poole, Molecular dynamics simulations of water, Annual Reviews of Computational Physics II , 47 (1995).
  54. B. Honig and A. Nicholls, Classical electrostatics in biology and chemistry, Science 268, 1144 (1995).
  55. J. Zeman, S. Kondrat, and C. Holm, Bulk ionic screening lengths from extremely large-scale molecular dynamics simulations, Chem. Commun. 56, 15635 (2020).
  56. P. Mereghetti, M. Martinez, and R. C. Wade, Long range Debye-Hückel correction for computation of grid-based electrostatic forces between biomacromolecules, BMC Biophysics 7:4 (2014).
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