Anabaena Sensory Rhodopsin: A Photochromic Color Sensor at 2.0 Å

Abstract

Microbial sensory rhodopsins are a family of membrane-embedded photoreceptors in prokaryotic and eukaryotic organisms. Structures of archaeal rhodopsins, which function as light-driven ion pumps or photosensors, have been reported. We present the structure of a eubacterial rhodopsin, which differs from those of previously characterized archaeal rhodopsins in its chromophore and cytoplasmic-side portions. Anabaena sensory rhodopsin exhibits light-induced interconversion between stable 13-cis and all-trans states of the retinylidene protein. The ratio of its cis and trans chromophore forms depends on the wavelength of illumination, thus providing a mechanism for a single protein to signal the color of light, for example, to regulate color-sensitive processes such as chromatic adaptation in photosynthesis. Its cytoplasmic half channel, highly hydrophobic in the archaeal rhodopsins, contains numerous hydrophilic residues networked by water molecules, providing a connection from the photoactive site to the cytoplasmic surface believed to interact with the receptor's soluble 14-kilodalton transducer.Over the past 4 years, microbial genomics has revealed a large family of photoactive, seventransmembrane-helix retinylidene proteins called microbial rhodopsins in phylogenetically diverse species, including haloarchaea, proteobacteria, cyanobacteria, fungi, and algae (1-4). *To whom correspondence should be addressed. hudel@uci.edu (H.L.) or john.l.spudich@uth.tmc.edu (J.L.S. Author Manuscript Author ManuscriptAuthor Manuscript Author ManuscriptThe first members of this family were discovered in halophilic archaea: the light-driven ion pumps bacteriorhodopsin and halorhodopsin and the phototaxis receptors sensory rhodopsins I and II. These four related haloarchaeal pigments are among the bestcharacterized membrane proteins in terms of structure and function, and nearly all of our knowledge of the properties of microbial rhodopsins, such as isomeric configuration and conformation of their chromophore, photochemical reactions, light-induced conformational changes in the protein, and function, derives from the study of these four, including atomic resolution structures that have been obtained for three of them (5-9). Studies of nonhaloarchaeal rhodopsins, of which >800 are known to exist (10, 11), are needed to examine the diversity of properties of this widespread family (12). Anabaena sensory rhodopsin, a recently discovered sensory representative outside of archaea (2), is well suited for exploration. It is the only bacterial sensory rhodopsin so far expressed in a photoactive form. Unlike the haloarchaeal sensory rhodopsins, which transmit signals to other integral membrane proteins, its function appears to involve modulation of a soluble cytoplasmic transducer, analogous to animal visual pigments (2).In this study, we report the structure of the retinal-complexed protein at 2.0 Å resolution, obtained by X-ray diffraction of crystals grown in a cubic lipid phase (table S1). The overall membrane-embedded seven-he...

Crystallographic structure of xanthorhodopsin, the light-driven proton pump with a dual chromophore

“…The structure was solved to 1.9-Å resolution ( Table 1). The P1 unit cell contains 2 molecules of xanthorhodopsin with a head-to-tail arrangement somewhat similar to 2-dimensional crystal forms of bacteriorhodopsin (14) and halorhodopsin (15), as well as 3-dimensional crystals of the D85S bacteriorhodopsin mutant (16), sensory rhodopsin II (17,18), and Anabaena sensory rhodopsin (19). Considering its function as an ion transporter in the cell membrane, xanthorhodopsin is unlikely to form such dimers in the original Salinibacter cells.…”

Dynamic Structure of Retinylidene Ligand of Rhodopsin Probed by Molecular Simulations

“…By contrast, the retinal conformation becomes more restricted upon binding to rhodopsin, where it functions as an inverse agonist. It is interesting that in both bacteriorhodopsin 51,53 and sensory rhodopsin, 54 retinal is 6-s-trans; while in dark-adapted rhodopsin it is widely thought to adopt the 6-s-cis conformation 33,40,55 .…”

Cell evolution and Earth history: stasis and revolution

“…Thus, rapid diversification of photosynthetic machineries and antenna pigments followed the glycobacterial revolution. Photoreceptors allowing physiological chromatic adaptation and light-oriented movements probably also stem from the glycobacterial ancestor; sensory rhodopsins occur in cyanobacteria and proteobacteria ( Jung et al 2003;Ruiz-Gonzalez & Marin 2004;Venter et al 2004;Vogeley et al 2004). One green non-S bacterium photosynthesizes using geothermal radiation in deep-sea vents (Beatty et al 2005); like sulphur-oxidizers there, they are glycobacteria and so younger than chlorobacteria.…”