Phototactic and Chemotactic Signal Transduction by Transmembrane Receptors and Transducers in Microorganisms

Journal of Biological Chemistry

Ihara

Kobayashi

et al. 2011

Self Cite

Rhodopsins possess retinal chromophore surrounded by seven transmembrane ␣-helices, are widespread in prokaryotes and in eukaryotes, and can be utilized as optogenetic tools. Although rhodopsins work as distinctly different photoreceptors in various organisms, they can be roughly divided according to their two basic functions, light-energy conversion and light-signal transduction. In microbes, light-driven proton transporters functioning as light-energy converters have been modified by evolution to produce sensory receptors that relay signals to transducer proteins to control motility. In this study, we cloned and characterized two newly identified microbial rhodopsins from Haloquadratum walsbyi. One of them has photochemical properties and a proton pumping activity similar to the well known proton pump bacteriorhodopsin (BR). The other, named middle rhodopsin (MR), is evolutionarily transitional between BR and the phototactic sensory rhodopsin II (SRII), having an SRII-like absorption maximum, a BR-like photocycle, and a unique retinal composition. The wild-type MR does not have a light-induced proton pumping activity. On the other hand, a mutant MR with two key hydrogen-bonding residues located at the interaction surface with the transducer protein HtrII shows robust phototaxis responses similar to SRII, indicating that MR is potentially capable of the signaling. These results demonstrate that color tuning and insertion of the critical threonine residue occurred early in the evolution of sensory rhodopsins. MR may be a missing link in the evolution from type 1 rhodopsins (microorganisms) to type 2 rhodopsins (animals), because it is the first microbial rhodopsin known to have 11-cis-retinal similar to type 2 rhodopsins.Rhodopsin molecules are photochemically active membrane-embedded proteins having seven transmembrane ␣-helices and retinal chromophore (vitamin A aldehyde) (1, 2). Rhodopsins are classified into two groups, microbial (type 1) and animal (type 2) rhodopsins (3). Type 1 rhodopsins are widespread in the microbial world in prokaryotes (bacteria and archaea) and in eukaryotes (fungi and algae) (1, 4 -7), and type 2 rhodopsins, such as visual pigments, are G-proteincoupled receptors, widespread in vertebrates and in invertebrates (3,8). An interesting feature of this photoactive protein family is a wide range of seemingly dissimilar functions performed by its members. Some rhodopsins are light-driven transporters, such as proton pumps bacteriorhodopsin (BR) 2 in haloarchaea, xanthorhodopsin in halophilic bacteria, proteorhodopsin in marine bacteria, and Leptosphaeria rhodopsin in fungi (1, 9 -13). Those proteins generate an electrochemical membrane potential upon light activation, which is utilized by ATP synthase to produce ATP (14). Other rhodopsins are light sensors, such as the phototaxis receptors sensory rhodopsins I (SRI) and II (SRII) in haloarchaea (1, 5) and mammalian rod rhodopsin and color visual pigments both in vertebrates and in invertebrates (3,8). These sensory receptors relay signals...

mentioning

confidence: 97%

Section: Photocycles Of Mr and Hwbr As Revealed By Ftir And Time-resomentioning

confidence: 99%

Section: Two Microbial Rhodopsin Proteins In the Genome Of Hmentioning

confidence: 99%

See 1 more Smart Citation

A Microbial Rhodopsin with a Unique Retinal Composition Shows Both Sensory Rhodopsin II and Bacteriorhodopsin-like Properties

Journal of Biological Chemistry

Ihara

Kobayashi

et al. 2011

Self Cite

“…S1) are called "rhodopsin" (2)(3)(4)(5)(6). Rhodopsins react to light of their corresponding specific wavelengths, although they all share the same basic structure (3,6). They are covalently bound to an 11-cis (mammalian type) or an all-trans (microbial type) retinal chromophore at a conserved lysine residue on the G-helix via a protonated Schiff base bond (supplemental Fig.…”

mentioning

confidence: 99%

“…S1) are called "rhodopsin" (2)(3)(4)(5)(6). Rhodopsins react to light of their corresponding specific wavelengths, although they all share the same basic structure (3,6).…”

mentioning

confidence: 99%

Spectral Tuning in Sensory Rhodopsin I from Salinibacter ruber

Journal of Biological Chemistry

Yuasa

Shibata

et al. 2011

Self Cite

Organisms utilize light as energy sources and as signals. Rhodopsins, which have seven transmembrane ␣-helices with retinal covalently linked to a conserved Lys residue, are found in various organisms as distant in evolution as bacteria, archaea, and eukarya. One of the most notable properties of rhodopsin molecules is the large variation in their absorption spectrum. Sensory rhodopsin I (SRI) and sensory rhodopsin II (SRII) function as photosensors and have similar properties (retinal composition, photocycle, structure, and function) except for their max (SRI, ϳ560 nm; SRII, ϳ500 nm). An expression system utilizing Escherichia coli and the high protein stability of a newly found SRI-like protein, SrSRI, enables studies of mutant proteins. To determine the residue contributing to the spectral shift from SRI to SRII, we constructed various SRI mutants, in which individual residues were substituted with the corresponding residues of SRII. Three such mutants of SrSRI showed a large spectral blue-shift (>14 nm) without a large alteration of their retinal composition. Two of them, A136Y and A200T, are newly discovered color tuning residues. In the triple mutant, the max was 525 nm. The inverse mutation of SRII (F134H/Y139A/ T204A) generated a spectral-shifted SRII toward longer wavelengths, although the effect is smaller than in the case of SRI, which is probably due to the lack of anion binding in the SRII mutant. Thus, half of the spectral shift from SRI to SRII could be explained by only those three residues taking into account the effect of Cl ؊ binding.

Sensory Rhodopsins

Tsukamoto

Encyclopedia of Life Sciences

2014

Motile organisms sense and respond to extracellular stimuli to survive in the various environments in which they live, by changing their movement to migrate towards more favourable habitats or to avoid more harmful habitats. Light is one of the most important signals that provide critical information to biological systems and therefore many organisms utilise light not only as an energy source but also as a signal. Sensory rhodopsin is a photochemically reactive membrane‐embedded protein consisting of seven transmembrane alpha‐helices, which binds the chromophore retinal (vitamin A aldehyde). Sensory rhodopsin is broadly distributed through all three biological kingdoms, eukarya, bacteria and archaea, indicating the biological significance of their light signal conversion. Key Concepts: Many organisms can sense and respond to light stimuli. Photoactive retinal proteins play important roles in light signal transduction in various organisms. The trans – cis photoisomerisation of the retinal chromophore triggers the cyclic photoreaction, leading to structural changes of the protein moiety. Photoactivated sensory rhodopsins regulate the activity of the cognate transducer molecules, which control the motility and morphology of the organisms. Sensory rhodopsins have become a focus of interest in part because of their importance to the general understanding of light signal conversion and because of potential application for the novel technology named ‘optogenetics’, in which retinal proteins are utilised to control biological activity with high temporal and spatial resolutions.