The subunit c-ring of H⁺-ATP synthase (F_o c-ring) plays an essential role in the proton translocation across a membrane driven by the electrochemical potential. To understand its structure and function, we have carried out solid-state NMR analysis under magic-angle sample spinning. The uniformly [¹³C, ¹⁵N]-labeled F_o c from E. coli (EF_o c) was reconstituted into lipid membranes as oligomers. Its high resolution two- and three-dimensional spectra were obtained, and the ¹³C and ¹⁵N signals were assigned. The obtained chemical shifts suggested that EF_o c takes on a hairpin-type helix-loop-helix structure in membranes as in an organic solution. The results on the magnetization transfer between the EF_o c and deuterated lipids indicated that Ile55, Ala62, Gly69 and F76 were lined up on the outer surface of the oligomer. This is in good agreement with the cross-linking results previously reported by Fillingame and his colleagues. This agreement reveals that the reconstituted EF_o c oligomer takes on a ring structure similar to the intact one in vivo. On the other hand, analysis of the ¹³C nuclei distance of [3-¹³C]Ala24 and [4-¹³C]Asp61 in the F_o c-ring did not agree with the model structures proposed for the EF_o c-decamer and dodecamer. Interestingly, the carboxyl group of the essential Asp61 in the membrane-embedded EF_o c-ring turned out to be protonated as COOH even at neutral pH. The hydrophobic surface of the EF_o c-ring carries relatively short side chains in its central region, which may allow soft and smooth interactions with the hydrocarbon chains of lipids in the liquid-crystalline state.