Bacteriorhodopsin (bR) is an efficient light-driven proton pump which shows a trans-cis isomerization reaction of its retinal chromophore after light absorption, BR exhibits a large reorganization energy A of 2520 cm(-1) on optical excitation. In this paper, we have studied the nature, origin, and dynamical aspects of this extensive reorganization. We report the results of a femtosecond three-pulse echo peak shift (3PEPS). transient grating (TG) and transient absorption (TA) study, complemented with those of steady-state absorption and fluorescence spectroscopy in wild-type bR and the D85S mutant in its blue and purple, halide-pumping forms. We have simulated the results in the context of the multimode Brownian oscillator (MBO) formalism. A simple model that incorporates retinal's known intramolecular vibrations, which represent 1094 cm(-1) or reorganization energy, and a single Gaussian protein relaxation with a decay of 50 fs representing 1430 cm(-1) of reorganization energy, yielded satisfactory results for all linear and nonlinear experimental results on wild-type bR. For the D85S mutant in its blue form, the same model could be applied with a Gaussian relaxation of 1050 cm(-1) amplitude. It is concluded that the protein environment of the retinal chromophore only exhibits an inertial response, and does not show any diffusive-type motions on a sub-ps to ps time scale, which is probably a consequence of the covalently constrained, polymeric nature of the protein. Our results are in close agreement with earlier molecular dynamics simulations on bR (Xu, D.; Martin, C. H.; Schulten, K. Biophys. J. 1996, 70, 453-460), which indicated that after retinal excitation, which is accompanied by a significant charge relocation along the polyene backbone, the protein exhibits an extensive dielectric relaxation on a 100 fs time scale representing an energy change of similar to1700 cm(-1). We conclude that on the sub-ps to ps timescale, the protein's major influence is electrostatic via a large number of small-amplitude motions of charges and dipoles. Major structural rearrangements of the protein do not occur on the timescale of isomerization. Polarized transient absorption measurements on bR and the D85S mutant indicated a time-independent anisotropy of the stimulated emission of 0.35, indicating that in the excited state, no change of the direction of the transition dipole moment of retinal takes place during the excited-state lifetime.