The photochemistry of the 13-desmethyl (DM) analog of bacteriorhodopsin (BR) is examined by using spectroscopy, molecular orbital theory and chromophore extraction followed by conformational analysis. The removal of the 13-methyl group permits the direct photochemical formation of a thermally stable, photochemically reversible state, P1DM, (λmax = 525 nm) which can be generated efficiently by exciting the resting state, bRDM with yellow or red light (λ > 590 nm). Chromophore extraction analysis reveals that the retinal configuration in P1DM is 9-cis, identical to that of retinal in the native BR P1 state. FTIR and Raman experiments on P1DM indicate an anti configuration around the C15=N bond, as would be expected of an O-state photoproduct. However, low temperature spectroscopy and ambient, time-resolved studies indicate that the P1DM state forms primarily via thermal relaxation from the LDDM state. Theoretical studies on the BR binding site show that 13-dm retinal is capable of isomerizing into a 9-cis configuration with minimal steric hindrance from surrounding residues, in contrast to the native chromophore in which surrounding residues significantly obstruct the corresponding motion. Analysis of the photokinetic experiments indicates that the Arrhenius activation energy of the bRDM → P1DM transition in 13-dm-BR is less than 0.6 kcal/mol (vs. 22 ± 5 kcal/mol measured for the bR → P (P1 and P2) reaction in 85:15 glycerol:water suspensions of WT). Consequently, the P1DM state in 13-dm-BR can form directly from all-trans, 15-anti intermediates (bRDM and ODM) or all-trans, 15-syn (KDDM/LDDM) intermediates. This study demonstrates that the 13-methyl group and its interactions with nearby binding site residues is primarily responsible for channeling one-photon photochemical and thermal reactions and is limited to the all-trans and 13-cis species interconversions in the native protein.