Here, we use NMR chemical shifts, spin relaxation, and residual dipolar couplings (RDCs) in conjunction with REMD simulations using the recently updated CHARMM27 nucleic acid force field (31, 32) to explore the conformational properties of the 12 nt ssRNA tail from the queC aptamer domain and the impact of a single A-to-C mutation targeting the polyadenine tract. Our study unmasks a previously unappreciated level of complexity in ssRNA and suggests that these structures can serve as excellent model systems for testing and developing computational force fields.