RNA as a Complex Polymer with Coupled Dynamics of Ions and Water in the Outer Solvation Sphere.

We unravel the internal and collective modes of a widely studied 58-nucleotide rRNA fragment in solvent using atomically detailed molecular dynamics simulations. The variation of lifetimes for water hydrogen bonds with nucleotide groups indicates heterogeneity of water dynamics on the RNA surface. The time scales of interactions of the discrete water molecules with RNA nucleotides extend from several hundred picoseconds to a few nanoseconds. We determine all of the association sites and the spatial distribution of residence times for Mg2+, K+, and water molecules in those sites. We provide insights into the population of Mg2+ and K+ ions and water molecules in the outer sphere and how their fluctuations are intricately linked with the kinetics of the 58-mer. We find that many of the long-lived Mg2+ sites identified from the simulations agree with the locations of ions in the X-ray structure. We determine the excess ion atmosphere around the rRNA and compare it with experimental data. We investigate the collective behavior of RNA, ions, and water, by performing a joint principle component analysis for the Cartesian coordinates of the RNA phosphorus atoms and for the occupation counts of the association sites. Our results indicate that the 58-mer system is a complex polymer, composed of RNA that is encased by a fluctuating network of associated counterions, co-ions, and water.