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Lanyi, Janos K; Schobert, Brigitte
Journal of molecular biology, 08/2002, Volume: 321, Issue: 4Journal Article
We illuminated bacteriorhodopsin crystals at 210 K to produce, in a photostationary state with 60% occupancy, the earliest M intermediate (M 1) of the photocycle. The crystal structure of this state was then determined from X-ray diffraction to 1.43 Å resolution. When the refined model is placed after the recently determined structure for the K intermediate but before the reported structures for two later M states, a sequence of structural changes becomes evident in which movements of protein atoms and bound water are coordinated with relaxation of the initially strained photoisomerized 13- cis,15- anti retinal. In the K state only retinal atoms are displaced, but in M 1 water 402 moves also, nearly 1 Å away from the unprotonated retinal Schiff base nitrogen. This breaks the hydrogen bond that bridges them, and initiates rearrangements of the hydrogen-bonded network of the extracellular region that develop more fully in the intermediates that follow. In the M 1 to M 2 transition, relaxation of the C 14–C 15 and C 15NZ torsion angles to near 180° reorients the retinylidene nitrogen atom from the extracellular to the cytoplasmic direction, water 402 becomes undetectable, and the side-chain of Arg82 is displaced strongly toward Glu194 and Glu204. Finally, in the M 2 to M 2′ transition, correlated with release of a proton to the extracellular surface, the retinal assumes a virtually fully relaxed bent shape, and the 13-methyl group thrusts against the indole ring of Trp182 which tilts in the cytoplasmic direction. Comparison of the structures of M 1 and M 2 reveals the principal switch in the photocycle: the change of the angle of the C 15NZ–CE plane breaks the connection of the unprotonated Schiff base to the extracellular side and establishes its connection to the cytoplasmic side.
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