Photo-Induced Proton Transport of Pharaonis Phoborhodopsin (Sensory Rhodopsin II) Is Ceased by Association with the Transducer

Sudo, Yuki; Iwamoto, Masayuki; Shimono, Kazumi; Sumi, Masato; Kamo, Naoki

doi:10.1016/s0006-3495(01)76070-5

Cited by 104 publications

(119 citation statements)

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“…In contrast, sensory rhodopsins SRI and SRII have slow photocycles (20,31,48), which allows the transient accumulation of long lived signaling states of the receptors to catalyze a sustained phosphorylation cascade controlling flagellar motor rotation (49). The fast photocycle of MR is therefore similar to those of ion pumping rhodopsins from other sources.…”

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

confidence: 99%

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

Sudo

Ihara

Kobayashi

et al. 2011

Journal of Biological Chemistry

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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...

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

confidence: 99%

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

Sudo

Ihara

Kobayashi

et al. 2011

Journal of Biological Chemistry

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“…On formation of the NpSRII/NpHtrII complex this function is inhibited 22,23 . This inhibition may originate from kinetics alteration, from structural changes prohibiting the pumping, or from combination of these factors.…”

Section: Implications For Npsrii Proton Pumpingmentioning

confidence: 99%

“…A second observation relates to the inhibition of the proton pump on transducer binding NpHtrII to its cognate receptor NpSRII 22,23 . It has been discussed that in the 2:2 complex the cytoplasmic channel cannot open sufficiently, thereby altering the proton uptake kinetics such that the reprotonation of the Schiff base is faster from the extracellular side.…”

Section: Introductionmentioning

confidence: 99%

Active State of Sensory Rhodopsin II: Structural Determinants for Signal Transfer and Proton Pumping

Gushchin

Reshetnyak

Borshchevskiy

et al. 2011

Journal of Molecular Biology

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The molecular mechanism of transmembrane signal transduction is still a pertinent question in cellular biology. Generally, a receptor can transfer an external signal via its cytoplasmic surface as found for GPCRs like rhodopsin or via the membrane domain like it is utilized by sensory rhodopsin II (SRII) in complex with its transducer HtrII. In the absence of HtrII SRII functions as a proton pump. Here, we report on the crystal structure of the active state of SRII from Natronomonas pharaonis (NpSRII). The problem of a dramatic loss of the diffraction quality upon loading of the active state was overcome by growing better crystals and reducing the occupancy of the state. The determined conformational changes at the region comprising helices F and G are similar to those observed for the NpSRII-transducer complex but they are much more pronounced. Meaning of these differences for proton pumping ability and understanding of the signal transduction by NpSRII is discussed.

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“…Photocycle kinetics in the detergent-solubilized SRII-HtrII complex was measured by Sudo et al (15), who concluded that the decay of the M intermediate is slowed in the presence of transducer. On the other hand, no change in the photocycle rate was observed for the same complex reconstituted in lipids (16,17). Measurements of transient voltage and pH changes in membranes containing transducerfree SRII demonstrated that the receptor (but not the receptortransducer complex) functions as a light-driven proton pump, although with less efficiency than BR (17,18).…”

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confidence: 93%

Conformational Changes Detected in a Sensory Rhodopsin II-Transducer Complex

Bergo

Spudich

et al. 2003

Journal of Biological Chemistry

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Sensory rhodopsins (SRs) are light receptors that belong to the growing family of microbial rhodopsins. SRs have now been found in all three major domains of life including archaea, bacteria, and eukaryotes. One of the most extensively studied sensory rhodopsins is SRII, which controls a blue light avoidance motility response in the halophilic archaeon Natronobacterium pharaonis. This seven-helix integral membrane protein forms a tight intermolecular complex with its cognate transducer protein, HtrII. In this work, the structural changes occurring in a fusion complex consisting of SRII and the two transmembrane helices (TM1 and TM2) of HtrII were investigated by time-resolved Fourier transform infrared difference spectroscopy. Although most of the structural changes observed in SRII are conserved in the fusion complex, several distinct changes are found. A reduction in the intensity of a prominent amide I band observed for SRII indicates that its structural changes are altered in the fusion complex, possibly because of the close interaction of TM2 with the F helix, which interferes with the F helix outward tilt. Deprotonation of at least one Asp/Glu residue is detected in the transducer-free receptor with a pK a near 7 that is abolished or altered in the fusion complex. Changes are also detected in spectral regions characteristic of Asn and Tyr vibrations. At high hydration levels, transducer-fusion interactions lead to a stabilization of an M-like intermediate that most likely corresponds to an active signaling form of the transducer. These findings are discussed in the context of a recently elucidated x-ray structure of the fusion complex. Sensory rhodopsin (SR)1 II is a seven-helix integral membrane protein found in halophilic archaea that functions as a light receptor for negative phototaxis (1). Together with sensory rhodopsin I (SRI), which is a dual photoattractant/photorepellent receptor (2); bacteriorhodopsin (BR), a light-driven proton pump; and halorhodopsin, a light-driven chloride pump, these proteins belong to a widespread family of photoactive retinylidene proteins or microbial rhodopsins (3). Microbial rhodopsins have several common features including an alltrans-retinylidene chromophore covalently attached to the protein via a protonated Schiff base linkage. Light absorption results in an all-trans 3 13-cis-isomerization of the chromophore that triggers subsequent conformational changes associated with a photocycle characteristic of each protein. Members of the microbial rhodopsin family have recently been found in diverse organisms including marine proteobacteria (4), cyanobacteria (5), and lower eukaryotes such as Neurospora crassa (6) and Chlamydomonas reinhardtii (7).Sensory rhodopsin II transmits the photorepellent signal to the cell cytoplasm by activating the transmembrane domain of its cognate transducer HtrII (8), 2 which is tightly bound to the receptor helices F and G (9). The photocycle of SRII comprises several photointermediates (10 -13), including the blue-shifted M and red-shifte...

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Photo-Induced Proton Transport of Pharaonis Phoborhodopsin (Sensory Rhodopsin II) Is Ceased by Association with the Transducer

Cited by 104 publications

References 38 publications

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

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

Active State of Sensory Rhodopsin II: Structural Determinants for Signal Transfer and Proton Pumping

Conformational Changes Detected in a Sensory Rhodopsin II-Transducer Complex

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