Amino acid residues of unfolded peptides in water sample only a few basins in the Ramachandran plot, including prominent polyproline II-like (pPII) conformations. Dynamics of guest residues, X, in GXG peptides in water were recently reported to be dominated by pPII and beta-strand-like (beta) conformations, resulting in an enthalpy entropy compensation at similar to 300 K. Using molecular dynamics (MD) in explicit solvent, we here examine pPII and beta conformational ensembles of 15 guest residues in GXG peptides, quantify local orientation of water around their side chains through novel water orientation plots, and study their hydration and hydrogen bonding properties. We show that pPII and beta ensembles are characterized by distinct water orientations: pPII ensembles are associated with an increased population of water oriented in parallel to the side chain surface whereas beta ensembles exhibit more heterogeneous water orientations. The backbone hydration is significantly higher in pPII than in beta ensembles. Importantly, pPII to beta hydration differences and the solvent accessible surface area of C-beta hydrogens both correlate with experimental pPII propensities. We propose that pPII conformations are stabilized by a local, hydrogen-bonded dathrate-like water structure and that residue-specific intrinsic pal propensities reflect distinct abilities of side chains to template this water structure.