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Molecular mechanisms of the interaction of chaotropic salts with natural and artificial DNA structures

Subject Area Physical Chemistry of Molecules, Liquids and Interfaces, Biophysical Chemistry
Biophysics
Term from 2019 to 2023
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 428230890
 
Final Report Year 2023

Final Report Abstract

DNA origami provide a unique possibility for the design of nanoscopic DNA superstructures based on predictable shape-generation via base pairing. Whereas shape design has been performed extensively, our project addressed the fundamental questions of macromolecular stability, comparable to in depth studies of protein folding. In fact, we used common ionic protein denaturants but exploited the advantage of quantifying denaturation by evaluation of nanoscopic aberrations visible under the atomic force microscope. By varying the denaturant and its counteranions we were able to thoroughly explore the interplay between DNA superstructural architectures (e.g., lattice type and crossover density), the DNA origami shape, the primary denaturant, and the counteranions. The nanoscopic data were correlated with circular dichroism spectra, i.e., molecular scale information on DNA chirality in temperaturedependent experiments. We discovered a critical role of heat capacity changes during DNA origami denaturation linked to local base pair opening. This was unexpected in the first place but was substantiated by further dedicated experiments. Surprisingly, the heat capacity change is under the control of anions, which – in contrast to the primary cationic denaturant guanidinium – cannot directly interact with the like-charged DNA backbone. We could show by molecular dynamics calculations that the anion-dependent degree of Gdm ion pairing is responsible for the anion-sensitivity of DNA origami stability. Our studies further show that the non-monotonic temperature-sensitivity of nanoscopic features does not correlate with the global melting of DNA origami. One reason is the shape- and architecture-dependent transmission of thermally or chemically generated strain within the superstructure to predisposed sites where damage accumulates in the form of highly “localized melting”. Specific evidence has been obtained for DNA origami triangles, which denature preferably at the vertices in the presence of GdmCl. Remarkably they do so not only upon heating but also upon cooling. The latter effect emphasizes the unexpected similarity to cold denaturation of proteins under similar conditions and is a direct consequence of the heat capacity change upon DNA origami damage. Thus, the project demonstrated that the two classes of biopolymers share fundamental physicochemical properties, but only in DNA origami is an observable available, which provides a link between thermodynamics and predictable localized sub-structure at the nanoscale.

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