The recently reported crystal structures of the membrane-embedded proton-dependent c-ring rotors of a cyanobacterial F(1)F(o) ATP synthase and a chloroplast F(1)F(o) ATP synthase have provided new insights into the mechanism of this essential enzyme. While the overall features of these c-rings are similar, a discrepancy in the structure and hydrogen-bonding interaction network of the H(+) sites suggests two distinct binding modes, potentially reflecting a mechanistic differentiation. Importantly, the conformation of the key glutamate side chain to which the proton binds is also altered. To investigate the nature of these differences, we use molecular dynamics simulations of both c-rings embedded in a phospholipid membrane. We observe that the structure of the c(15) ring from Spirulina platensis is unequivocally stable within the simulation time. By contrast, the proposed structure of the H(+) site in the chloroplast c(14) ring changes rapidly and consistently into that reported for the c(15) ring, indicating that the latter represents a common binding mode. To assess this hypothesis, we have remodeled the c(14) ring by molecular replacement using the published structure factors. The resulting structure provides clear evidence in support of a common binding site conformation and is also considerably improved statistically. These findings, taken together with a sequence analysis of c-subunits in the ATP synthase family, indicate that the so-called proton-locked conformation observed in the c(15) ring may be a common characteristic not only of light-driven systems such as chloroplasts and cyanobacteria but also of a selection of other bacterial species.