We have performed an extensive set of all-atom molecular dynamics (MD) simulations of a bacterial proton-coupled oligopeptide transporter (POT) in an explicit membrane environment. We have characterized both the local and global conformational dynamics of the transporter upon the proton and/or substrate binding, within a statistical framework. Our results reveal a clearly distinct behavior for local conformational dynamics in the absence and presence of the proton at the putative proton binding residue E310. Particularly, we find that the substrate binding conformation is drastically different in the two conditions, where the substrate binds to the protein in a lateral/vertical manner, in the presence/absence of the proton. We do not observe any statistically significant distinctive behavior in terms of the global conformational changes in different simulation conditions, within the time scales of our simulations. Our extensive simulations and analyses call into question the implicit assumption of many MD studies that local conformational changes observed in short simulations could provide dues to the global conformational changes that occur on much longer time scales. The linear regression analysis of quantities associated with the global conformational fluctuations, however, provides an indication of a mechanism involving the concerted motion of the transmembrane helices, consistent with the rocker-switch mechanism.