Sensory Rhodopsins


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 transcis 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.

Keywords: light; retinal; signal transduction; membrane protein; colour; isomerisation

Figure 1.

Retinal proteins from microorganisms. (a) Chemical structure of the all‐trans retinal protonated Schiff base. (b) Crystal structures of retinal proteins. BR (PDB code: 1C3W) (Luecke et al., ), ASR (PDB code: 1XIO) (Vogeley et al., ), SRII (PDB code: 1H68) (Royant et al., ) and ChR, also called CSR, (PDB code: 3UG9) (Kato et al., ) are coloured by purple, magenta, orange and yellow, respectively. The retinal chromophore covalently binds to a specific Lys residue located at the middle of the membrane via a protonated Schiff base linkage. CP and EC indicate cytoplasmic and extracellular side, respectively. (c) Illustration of absorption spectra of retinal proteins. Retinal proteins show various colours and exhibit two basic functions: the ion pumping and sensing.

Figure 2.

Phylogenetic tree of sensory rhodopsins and BR. They are widespread in archaea, eubacteria and eukarya. Abbreviations: ASR, Anabaena sensory rhodopsin; CSRB, Chlamydomonas sensory rhodopsin B; CSRA, Chlamydomonas sensory rhodopsin A; NpSRII, Natronomonas pharaonis sensory rhodopsin II; HsSRII, Halobacterium salinarum sensory rhodopsin II; HvSRI, Haloarcula vallismortis sensory rhodopsin I; HsSRI, Halobacterium salinarum sensory rhodopsin I; and SrSRI, Salinibacter ruber sensory rhodopsin I.

Figure 3.

Models for signalling by the three types of sensory rhodopsins. (a) SRII forms a tetrameric 2:2 signalling complex with HtrII in the membrane. The SRII–HtrII complex interacts with an adaptor protein CheW and transfers the light signal to CheY via phosphorylation of a kinase CheA. The phosphorylated CheY controls the rotation direction of the flagellar motor apparatus, resulting in negative phototaxis. (b) ASR performs the transcriptional regulation of phycobilisome proteins in collaboration with a putative transducer protein ASRT. (c) CSR mediates the photoinduced membrane depolarisation, leading to a motility change of the cell.



Bogomolni RA , Stoeckenius W , Szundi I et al. (1994) Removal of transducer HtrI allows electrogenic proton translocation by sensory rhodopsin I. Proceedings of the National Academy of Sciences of the USA 91: 10188–10192.

Boyden ES , Zhang F , Bamberg E , Nagel G and Deisseroth K (2005) Millisecond‐timescale, genetically targeted optical control of neural activity. Nature Neuroscience 8: 1263–1268.

Ernst OP , Sánchez Murcia PA , Daldrop P et al. (2008) Photoactivation of channelrhodopsin. Journal of Biological Chemistry 283: 1637–1643.

Falke JJ , Bass RB , Butler SL , Chervitz SA and Danielson MA (1997) The two‐component signaling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes. Annual Review of Cell and Developmental Biology 13: 457–512.

Gordeliy VI , Labahn J , Moukhametzianov R et al. (2002) Molecular basis of transmembrane signalling by sensory rhodopsin II‐transducer complex. Nature 419: 484–487.

Govorunova EG , Sineshchekov OA , Li H , Janz R and Spudich JL (2013) Characterization of a highly efficient blue‐shifted channelrhodopsin from the marine alga Platymonas subcordiformis . Journal of Biological Chemistry. doi: 10.1074/jbc.M113.505495

Hoff WD , Jung KH and Spudich JL (1997) Molecular mechanism of photosignaling by archaeal sensory rhodopsins. Annual Review of Biophysics and Biomolecular Structure 26: 223–258.

Imamoto Y and Shichida Y (2013) Cone visual pigments. Biochimica et Biophysica Acta. doi: 10.1016/j.bbabio.2013.08.009

Inoue K , Tsukamoto T and Sudo Y (2013) Molecular and evolutionary aspects of microbial sensory rhodopsins. Biochimica et Biophysica Acta. doi: 10.1016/j.bbabio.2013.05.005

Irieda H , Morita T , Maki K et al. (2012) Photo‐induced regulation of the chromatic adaptive gene expression by Anabaena sensory rhodopsin. Journal of Biological Chemistry 287: 32485–32493.

Irieda H , Reissig L , Kawanabe A et al. (2011) Structural characteristics around the β‐ionone ring of the retinal chromophore in Salinibacter sensory rhodopsin I. Biochemistry 50: 4912–4922.

Jung K‐H , Trivedi VD and Spudich JL (2003) Demonstration of a sensory rhodopsin in eubacteria. Molecular Microbiology 47: 1513–1522.

Kaneko T , Nakamura Y , Wolk CP et al. (2001) Complete genomic sequence of the filamentous nitrogen‐fixing cyanobacterium Anabaena sp. strain PCC 7120 DNA Research 8: 205–213, 227–253.

Kato HE , Zhang F , Yizhar O et al. (2012) Crystal structure of the channelrhodopsin light‐gated cation channel. Nature 482: 369–374.

Kawanabe A , Furutani Y , Jung K‐H and Kandori H (2007) Photochromism of Anabaena sensory rhodopsin. Journal of the American Chemical Society 129: 8644–8649.

Kehoe DM (2010) Chromatic adaptation and the evolution of light color sensing in cyanobacteria. Proceedings of the National Academy of Sciences of the USA 107: 9029–9030.

Kitajima‐Ihara T , Furutani Y , Suzuki D et al. (2008) Salinibacter sensory rhodopsin: sensory rhodopsin I‐like protein from a eubacterium. Journal of Biological Chemistry 283: 23533–23541.

Luecke H , Schobert B , Richter HT , Cartailler JP and Lanyi JK (1999) Structure of bacteriorhodopsin at 1.55 Å resolution. Journal of Molecular Biology 291: 899–911.

Macinelli RL , Landheim R , Sánchez‐Porro C et al. (2009) Halorubrum chaoviator sp. nov., a haloarchaeon isolated from sea salt in Baja California, Mexico, Western Australia and Naxos, Greece. International Journal of Systematic and Evolutionary Microbiology 59: 1908–1913.

Mongodin EF , Nelson KE , Daugherty S et al. (2005) The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proceedings of the National Academy of Sciences of the USA 102: 18147–18152.

Mori A , Yagasaki J , Homma M , Reissig L and Sudo Y (2013) Investigation of the chromophore binding cavity in the 11‐cis acceptable microbial rhodopsin MR. Chemical Physics 419: 23–29.

Mukohata Y , Ihara K , Tamura T and Sugiyama Y (1999) Halobacterial rhodopsins. Journal of Biochemistry 125: 649–657.

Nagel G , Ollig D , Fuhrmann M et al. (2002) Channelrhodopsin‐1: a light‐gated proton channel in green algae. Science 296: 2395–2398.

Oesterhelt D and Stoeckenius W (1971) Rhodopsin‐like protein from the purple membrane of Halobacterium halobium . Nature New Biology 233: 149–152.

Reissig L , Iwata T , Kikukawa T et al. (2012) Influence of halide binding on the hydrogen bonding network in the active site of Salinibacter sensory rhodopsin I. Biochemistry 51: 8802–8813.

Royant A , Nollert P , Edman K et al. (2001) X‐ray structure of sensory rhodopsin II at 2.1‐Å resolution. Proceedings of the National Academy of Sciences of the USA 98: 10131–10136.

Sharma AK , Spudich JL and Doolittle WF (2006) Microbial rhodopsins: functional versatility and genetic mobility. Trends in Microbiology 14: 463–469.

Shimono K , Iwamoto M , Sumi M and Kamo N (1997) Functional expression of pharaonis phoborhodopsin in Escherichia coli . FEBS Letters 420: 54–56.

Sineshchekov OA , Jung K‐H and Spudich JL (2002) Two rhodopsins mediate phototaxis to low‐ and high‐intensity light in Chlamydomonas reinhardtii . Proceedings of the National Academy of Sciences of the USA 99: 8689–8694.

Sineshchekov OA , Sasaki J , Phillips BJ and Spudich JL (2008) A Schiff base connectivity switch in sensory rhodopsin signaling. Proceedings of the National Academy of Sciences of the USA 105: 16159–16164.

Sineshchekov OA , Sasaki J , Wang J and Spudich JL (2010) Attractant and repellent signaling conformers of sensory rhodopsin‐transducer complexes. Biochemistry 49: 6696–6704.

Spudich JL (1994) Protein–protein interaction converts a proton pump into a sensory receptor. Cell 79: 747–750.

Spudich JL and Bogomolni RA (1984) Mechanism of colour discrimination by a bacterial sensory rhodopsin. Nature 312: 509–513.

Spudich JL , Yang CS , Jung K‐H and Spudich EN (2000) Retinylidene proteins: structures and functions from archaea to humans. Annual Review of Cell and Developmental Biology 16: 365–392.

Sudo Y , Furutani Y , Spudich JL and Kandori H (2007) Early photocycle structural changes in a bacteriorhodopsin mutant engineered to transmit photosensory signals. Journal of Biological Chemistry 282: 15550–15558.

Sudo Y , Iwamoto M , Shimono K , Sumi M and Kamo N (2001) Photo‐induced proton transport of pharaonis phoborhodopsin (sensory rhodopsin II) is ceased by association with the transducer. Biophysical Journal 80: 916–922.

Sudo Y , Okada A , Suzuki D et al. (2009) Characterization of a signaling complex composed of sensory rhodopsin I and its cognate transducer protein from the eubacterium Salinibacter ruber . Biochemistry 48: 10136–10145.

Sudo Y , Okazaki A , Ono H et al. (2013) A blue‐shifted light‐driven proton pump for neural silencing. Journal of Biological Chemistry 288: 20624–20632.

Sudo Y and Spudich JL (2006) Three strategically placed hydrogen‐bonding residues convert a proton pump into a sensory receptor. Proceedings of the National Academy of Sciences of the USA 103: 16129–16134.

Sudo Y , Yamabi M , Iwamoto M , Shimono K and Kamo N (2003) Interaction of Natronobacterium pharaonis phoborhodopsin (sensory rhodopsin II) with its cognate transducer probed by increase in the thermal stability. Photochemistry and Photobiology 78: 511–516.

Sudo Y , Yamabi M , Kato S et al. (2006) Importance of specific hydrogen bonds of archaeal rhodopsins for the binding to the transducer protein. Journal of Molecular Biology 357: 1274–1282.

Sudo Y , Yuasa Y , Shibata J , Suzuki D and Homma M (2011) Spectral tuning in sensory rhodopsin I from Salinibacter ruber . Journal of Biological Chemistry 286: 11328–11336.

Suzuki D , Furutani Y , Inoue K et al. (2009) Effects of chloride ion binding on the photochemical properties of Salinibacter sensory rhodopsin I. Journal of Molecular Biology 392: 48–62.

Suzuki D , Irieda H , Homma M , Kawagishi I and Sudo Y (2010) Phototactic and chemotactic signal transduction by transmembrane receptors and transducers in microorganisms. Sensors 10: 4010–4039.

Suzuki T , Yamasaki K , Fujita S et al. (2003) Archaeal‐type rhodopsins in Chlamydomonas: model structure and intracellular localization. Biochemical and Biophysical Research Communications 301: 711–717.

Takahashi T , Mochizuki Y , Kamo N and Kobatake Y (1985) Evidence that the long‐lifetime photointermediate of s‐rhodopsin is a receptor for negative phototaxis in Halobacterium halobium . Biochemical and Biophysical Research Communications 127: 99–105.

Vogeley L , Sineshchekov OA , Trivedi VD et al. (2004) Anabaena sensory rhodopsin: a photochromic color sensor at 2.0 Å. Science 306: 1390–1393.

Vogeley L , Trivedi VD , Sineshchekov OA et al. (2007) Crystal structure of the Anabaena sensory rhodopsin transducer. Journal of Molecular Biology 367: 741–751.

Yagasaki J , Suzuki D , Ihara K et al. (2010) Spectroscopic studies of a sensory rhodopsin I homologue from the archaeon Haloarcula vallismortis . Biochemistry 49: 1183–1190.

Zhang F , Vierock J , Yizhar O et al. (2011) The microbial opsin family of optogenetic tools. Cell 147: 1446–1457.

Further Reading

Brown LS (2013) Eubacterial rhodopsins – Unique photosensors and diverse ion pumps. Biochimica et Biophysica Acta. doi: 10.1016/j.bbabio.2013.05.006

Brown LS and Jung K‐H (2006) Bacteriorhodopsin‐like proteins of eubacteria and fungi: the extent of conservation of the haloarchaeal proton‐pumping mechanism. Photochemistry and Photobiological Sciences 5: 538–546.

Hegemann P (2008) Algal sensory photoreceptors. Annual Review of Plant Physiology 59: 167–189.

Klare JP , Chizhov I and Engelhard M (2008) Microbial rhodopsins: scaffolds for ion pumps, channels, and sensors. Results and Problems in Cell Differentiation 45: 73–122.

Lanyi JK (2004) Bacteriorhodopsin. Annual Review of Physiology 66: 665–688.

Spudich JL and Jung K‐H (2005) Microbial rhodopsin: phylogenetic and functional diversity. In: Briggs WR and Spudich JL (eds) Handbook of Photosensory Receptors, pp. 1–23. Weinheim, Germany: Wiley‐VCH Verlag.

Spudich JL , Sineshchekov OA and Govorunova EG (2013) Mechanism divergence in microbial rhodopsins. Biochimica et Biophysica Acta. doi: 10.1016/j.bbabio.2013.06.006

Sudo Y (2012) Transport and sensory rhodopsins in microorganisms. In: CRC Handbook of Organic Photochemistry and Photobiology, 3rd edn., pp. 1173–1193. Boca Raton, FL: CRC Press.

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Tsukamoto, Takashi, and Sudo, Yuki(Jan 2014) Sensory Rhodopsins. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0022838]