Issue

Vol. 13 (2021)

Anomalous Laterally Stressed Kinetically Trapped DNA Surface Conformations

https://doi.org/10.1007/s40820-021-00626-2
Valery V. Prokhorov
Federal Research and Clinical Center of Physical-Chemical Medicine, Malaya Pirogovskaya, 1a, Moscow 119435, Russian Federation
Nikolay A. Barinov
Federal Research and Clinical Center of Physical-Chemical Medicine, Malaya Pirogovskaya, 1a, Moscow 119435, Russian Federation
Kirill A. Prusakov
Federal Research and Clinical Center of Physical-Chemical Medicine, Malaya Pirogovskaya, 1a, Moscow 119435, Russian Federation
Evgeniy V. Dubrovin
Federal Research and Clinical Center of Physical-Chemical Medicine, Malaya Pirogovskaya, 1a, Moscow 119435, Russian Federation
Maxim D. Frank‑Kamenetskii
Department of Biomedical Engineering, Boston University, 44 Cummington Mall, Boston MA02215, USA
Dmitry V. Klinov
Federal Research and Clinical Center of Physical-Chemical Medicine, Malaya Pirogovskaya, 1a, Moscow 119435, Russian Federation

Corresponding Author: Dmitry V. Klinov

dmitry.klinov@niifhm.ru

Nano-Micro Letters, Vol. 13 (2021), Article Number: 130

Abstract

Up to now, the DNA molecule adsorbed on a surface was believed to always preserve its native structure. This belief implies a negligible contribution of lateral surface forces during and after DNA adsorption although their impact has never been elucidated. High-resolution atomic force microscopy was used to observe that stiff DNA molecules kinetically trapped on monomolecular films comprising one-dimensional periodically charged lamellar templates as a single layer or as a sublayer are oversaturated by sharp discontinuous kinks and can also be locally melted and supercoiled. We argue that kink/anti-kink pairs are induced by an overcritical lateral bending stress (> 30 pNnm) inevitable for the highly anisotropic 1D-1D electrostatic interaction of DNA and underlying rows of positive surface charges. In addition, the unexpected kink-inducing mechanical instability in the shape of the template-directed DNA confined between the positively charged lamellar sides is observed indicating the strong impact of helicity. The previously reported anomalously low values of the persistence length of the surface-adsorbed DNA are explained by the impact of the surface-induced low-scale bending. The sites of the local melting and supercoiling are convincingly introduced as other lateral stress-induced structural DNA anomalies by establishing a link with DNA high-force mechanics. The results open up the study in the completely unexplored area of the principally anomalous kinetically trapped DNA surface conformations in which the DNA local mechanical response to the surface-induced spatially modulated lateral electrostatic stress is essentially nonlinear. The underlying rich and complex in-plane nonlinear physics acts at the nanoscale beyond the scope of applicability of the worm-like chain approximation.


Highlights:


1 DNA kinking is inevitable for the highly anisotropic 1D–1D electrostatic interaction with the one-dimensionally periodically charged surface.
2 The double helical structure of the DNA kinetically trapped on positively charged monomolecular films comprising the lamellar templates is strongly laterally stressed and extremely perturbed at the nanometer scale.
3 The DNA kinetic trapping is not a smooth 3D—> 2D conformational flattening but is a complex nonlinear in-plane mechanical response (bending, tensile and unzipping) driven by the physics beyond the scope of the applicability of the linear worm-like chain approximation.

Keywords

DNA surface conformations Kinetic trapping Lateral stress Periodically charged surface DNA kinks
Prokhorov, Valery V., Nikolay A. Barinov, Kirill A. Prusakov, Evgeniy V. Dubrovin, Maxim D. Frank‑Kamenetskii, and Dmitry V. Klinov. 2021. “Anomalous Laterally Stressed Kinetically Trapped DNA Surface Conformations”. Nano-Micro Letters 13 (May):130. https://doi.org/10.1007/s40820-021-00626-2.
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