The influence of the internal dynamics of two polypeptides comprising transmembrane α-helix A or two α-helices A and B of bacterioopsin on experimentally accessible (15)N NMR relaxation rates was investigated by molecular dynamics (MD) simulations, combined with more simple mechanic considerations. 'Model-free' order parameters and correlation times of internal motions [Lipari, G. and Szabo, A. (1982) J. Am. Chem. Soc., 104, 4546-4559] were calculated for these models. It was found that both peptides exhibit two types of internal motions of the amide bonds, on the pico- and nanosecond time scales, affecting (15)N NMR relaxation. The fast fluctuations are local and correspond to the librational motions of the individual N-H vectors in an effective potential of atoms of the surrounding matrix. In contrast, the motions on the nanosecond time scale imply concerted collective vibrations of a large number of atoms and could be represented as bending oscillation of α-helices, strongly overdamped by the ambient solvent. A few other molecular mechanisms of slow internal motion were found, such as local distortions of the α-helices (e.g., α-aneurysm), delocalized distortions of the α-helical backbone, as well as oscillations of the tilt angle between the axes of the α-helices A and B. The results are compared with (15)N NMR relaxation data measured for the (1-36)bacterioopsin and (1-71)bacterioopsin polypeptides in chloroform-methanol (1:1) and in SDS micelles [Orekhov, V.Yu., Pervushin, K.V. and Arseniev, A.S. (1994) Eur. J. Biochem., 219, 887-896].