Dataset Information

Quantitative Studies of an RNA Duplex Electrostatics by Ion Counting.

ABSTRACT: RNAs are one of the most charged polyelectrolytes in nature, and understanding their electrostatics is fundamental to their structure and biological functions. An effective way to characterize the electrostatic field generated by nucleic acids is to quantify interactions between nucleic acids and ions that surround the molecules. These ions form a loosely associated cloud referred to as an ion atmosphere. Although theoretical and computational studies can describe the ion atmosphere around RNAs, benchmarks are needed to guide the development of these approaches, and experiments to date that read out RNA-ion interactions are limited. Here, we present ion counting studies to quantify the number of ions surrounding well-defined model systems of RNA and DNA duplexes. We observe that the RNA duplex attracts more cations and expels fewer anions compared to the DNA duplex, and the RNA duplex interacts significantly stronger with the divalent cation Mg2+, despite their identical total charge. These experimental results suggest that the RNA duplex generates a stronger electrostatic field than DNA, as is predicted based on the structural differences between their helices. Theoretical calculations using a nonlinear Poisson-Boltzmann equation give excellent agreement with experiments for monovalent ions but underestimate Mg2+-DNA and Mg2+-RNA interactions by 20%. These studies provide needed stringent benchmarks to use against other all-atom theoretical models of RNA-ion interactions, interactions that likely must be accurately accounted for in structural, dynamic, and energetic terms to confidently model RNA structure, interactions, and function.

SUBMITTER: Gebala M

PROVIDER: S-EPMC6818163 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Quantitative Studies of an RNA Duplex Electrostatics by Ion Counting.

Gebala Magdalena M Herschlag Daniel D

Biophysical journal 20190812 6

RNAs are one of the most charged polyelectrolytes in nature, and understanding their electrostatics is fundamental to their structure and biological functions. An effective way to characterize the electrostatic field generated by nucleic acids is to quantify interactions between nucleic acids and ions that surround the molecules. These ions form a loosely associated cloud referred to as an ion atmosphere. Although theoretical and computational studies can describe the ion atmosphere around RNAs, ...[more]

PMID: 31466697

Similar Datasets

Project description:The ion atmosphere is a critical structural, dynamic, and energetic component of nucleic acids that profoundly affects their interactions with proteins and ligands. Experimental methods that "count" the number of ions thermodynamically associated with the ion atmosphere allow dissection of energetic properties of the ion atmosphere, and thus provide direct comparison to theoretical results. Previous experiments have focused primarily on the cations that are attracted to nucleic acid polyanions, but have also showed that anions are excluded from the ion atmosphere. Herein, we have systematically explored the properties of anion exclusion, testing the zeroth-order model that anions of different identity are equally excluded due to electrostatic repulsion. Using a series of monovalent salts, we find, surprisingly, that the extent of anion exclusion and cation inclusion significantly depends on salt identity. The differences are prominent at higher concentrations and mirror trends in mean activity coefficients of the electrolyte solutions. Salts with lower activity coefficients exhibit greater accumulation of both cations and anions within the ion atmosphere, strongly suggesting that cation-anion correlation effects are present in the ion atmosphere and need to be accounted for to understand electrostatic interactions of nucleic acids. To test whether the effects of cation-anion correlations extend to nucleic acid kinetics and thermodynamics, we followed the folding of P4-P6, a domain of the Tetrahymena group I ribozyme, via single-molecule fluorescence resonance energy transfer in solutions with different salts. Solutions of identical concentration but lower activity gave slower and less favorable folding. Our results reveal hitherto unknown properties of the ion atmosphere and suggest possible roles of oriented ion pairs or anion-bridged cations in the ion atmosphere for electrolyte solutions of salts with reduced activity. Consideration of these new results leads to a reevaluation of the strengths and limitations of Poisson-Boltzmann theory and highlights the need for next-generation atomic-level models of the ion atmosphere.

Dataset Information

Quantitative Studies of an RNA Duplex Electrostatics by Ion Counting.

Publications

Quantitative Studies of an RNA Duplex Electrostatics by Ion Counting.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets