Collagen proteins are the main constituents of the extracellular matrix (ECM), and fulfil a number of wide-ranging functions, including contributions to the mechanical and biological behaviour of the ECM. Due to the heterogeneous nature of collagen in tissue samples it is difficult to fully explain the experimental observation, and hence the study of shorter model peptides is common place. Here, the computational energy landscape framework is employed to study Gly to Ala mutations in a GPO model peptide. The results show good agreement with the experimental observations for the GPO reference and a triply mutated peptide, demonstrating the validity of the approach. The modelling predicts that changes in structure are moderate and localised, with an increased dynamic in the backbone and alterations to the hydrogen bonding pattern. Two mechanisms for adjusting to the mutations are observed, with potential consequences regarding protein binding. Finally, in line with a hypothesis that proline puckering allows controlled flexibility (Chow et al., Sci. Rep., 2018, 8, 13809), alterations in the puckering preferences are observed in the strained residues surrounding the mutational sites.