Abstract
Microbial rhodopsins (MRs) are a large family of photoactive membrane proteins, found in microorganisms belonging to all kingdoms of life, with new members being constantly discovered. Among the MRs are light-driven proton, cation and anion pumps, light-gated cation and anion channels, and various photoreceptors. Due to their abundance and amenability to studies, MRs served as model systems for a great variety of biophysical techniques, and recently found a great application as optogenetic tools. While the basic aspects of microbial rhodopsins functioning have been known for some time, there is still a plenty of unanswered questions. This chapter presents and summarizes the available knowledge, focusing on the functional and structural studies.
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References
Adamantidis A, Arber S, Bains JS et al (2015) Optogenetics: 10 years after ChR2 in neurons – views from the community. Nat Neurosci 18:1202–1212. https://doi.org/10.1038/nn.4106
Altenbach C, Marti T, Khorana HG, Hubbell WL (1990) Transmembrane protein structure: spin labeling of bacteriorhodopsin mutants. Science 248:1088–1092
Anantharaman V, Balaji S, Aravind L (2006) The signaling helix: a common functional theme in diverse signaling proteins. Biol Direct 1:25. https://doi.org/10.1186/1745-6150-1-25
Arenkiel BR, Peca J, Davison IG et al (2007) In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54:205–218. https://doi.org/10.1016/j.neuron.2007.03.005
Avelar GM, Schumacher RI, Zaini PA et al (2014) A rhodopsin-guanylyl cyclase gene fusion functions in visual perception in a fungus. Curr Biol 24:1234–1240. https://doi.org/10.1016/j.cub.2014.04.009
Bagley K, Dollinger G, Eisenstein L et al (1982) Fourier transform infrared difference spectroscopy of bacteriorhodopsin and its photoproducts. Proc Natl Acad Sci U S A 79:4972–4976. PMC346807
Balashov SP, Imasheva ES, Boichenko VA et al (2005) Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna. Science 309:2061–2064. https://doi.org/10.1126/science.1118046
Balashov SP, Imasheva ES, Choi AR et al (2010) Reconstitution of gloeobacter rhodopsin with echinenone: role of the 4-keto group. Biochemistry 49:9792–9799. https://doi.org/10.1021/bi1014166
Balashov SP, Petrovskaya LE, Lukashev EP et al (2012) Aspartate–histidine interaction in the retinal Schiff base counterion of the light-driven proton pump of Exiguobacterium sibiricum. Biochemistry 51:5748–5762. https://doi.org/10.1021/bi300409m
Balashov SP, Petrovskaya LE, Imasheva ES et al (2013) Breaking the carboxyl rule: lysine 96 facilitates reprotonation of the Schiff base in the photocycle of a retinal protein from Exiguobacterium sibiricum. J Biol Chem 288:21254–21265. https://doi.org/10.1074/jbc.M113.465138
Balashov SP, Imasheva ES, Dioumaev AK et al (2014) Light-driven Na+ pump from Gillisia limnaea: a high-affinity Na+ binding site is formed transiently in the photocycle. Biochemistry 53:7549–7561. https://doi.org/10.1021/bi501064n
Bamann C, Kirsch T, Nagel G, Bamberg E (2008) Spectral characteristics of the photocycle of channelrhodopsin-2 and its implication for channel function. J Mol Biol 375:686–694. https://doi.org/10.1016/j.jmb.2007.10.072
Bamann C, Gueta R, Kleinlogel S et al (2010) Structural guidance of the photocycle of channelrhodopsin-2 by an interhelical hydrogen bond. Biochemistry 49:267–278. https://doi.org/10.1021/bi901634p
Bamann C, Bamberg E, Wachtveitl J, Glaubitz C (2014) Proteorhodopsin. Biochim Biophys Acta 1837:614–625. https://doi.org/10.1016/j.bbabio.2013.09.010
Bamberg E, Hegemann P, Oesterhelt D (1984) Reconstitution of the light-driven electrogenic ion pump halorhodopsin in black lipid membranes. Biochim Biophys Acta 773:53–60. https://doi.org/10.1016/0005-2736(84)90549-2
Baudry J, Tajkhorshid E, Molnar F et al (2001) Molecular dynamics study of bacteriorhodopsin and the purple membrane. J Phys Chem B 105:905–918. https://doi.org/10.1021/jp000898e
Béjà O, Aravind L, Koonin EV et al (2000) Bacterial rhodopsin: evidence for a new type of phototrophy in the Sea. Science 289:1902–1906. https://doi.org/10.1126/science.289.5486.1902
Béjà O, Spudich EN, Spudich JL et al (2001) Proteorhodopsin phototrophy in the ocean. Nature 411:786–789. https://doi.org/10.1038/35081051
Bergo VB, Sineshchekov OA, Kralj JM et al (2009) His-75 in proteorhodopsin, a novel component in light-driven proton translocation by primary pumps. J Biol Chem 284:2836–2843. https://doi.org/10.1074/jbc.M803792200
Berndt A, Lee SY, Ramakrishnan C, Deisseroth K (2014) Structure-guided transformation of channelrhodopsin into a light-activated chloride channel. Science 344:420–424. https://doi.org/10.1126/science.1252367
Berndt A, Lee SY, Wietek J et al (2016) Structural foundations of optogenetics: determinants of channelrhodopsin ion selectivity. Proc Natl Acad Sci U S A 113:822–829. https://doi.org/10.1073/pnas.1523341113
Bertsova YV, Bogachev AV, Skulachev VP (2015) Proteorhodopsin from Dokdonia sp. PRO95 is a light-driven Na+-pump. Biochem Mosc 80:449–454. https://doi.org/10.1134/S0006297915040082
Bertsova YV, Arutyunyan AM, Bogachev AV (2016) Na+-translocating rhodopsin from Dokdonia sp. PRO95 does not contain carotenoid antenna. Biochem Mosc 81:414–419. https://doi.org/10.1134/S000629791604012X
Bhate MP, Molnar KS, Goulian M, DeGrado WF (2015) Signal transduction in histidine kinases: insights from new structures. Structure 23:981–994. https://doi.org/10.1016/j.str.2015.04.002
Bivin DB, Stoeckenius W (1986) Photoactive retinal pigments in haloalkaliphilic bacteria. J Gen Microbiol 132:2167–2177
Bogomolni RA, Spudich JL (1982) Identification of a third rhodopsin-like pigment in phototactic Halobacterium halobium. Proc Natl Acad Sci U S A 79:6250–6254
Bogomolni RA, Stoeckenius W, Szundi I et al (1994) Removal of transducer HtrI allows electrogenic proton translocation by sensory rhodopsin I. Proc Natl Acad Sci U S A 91:10188–10192
Bondar A-N, Elstner M, Suhai S et al (2004) Mechanism of primary proton transfer in bacteriorhodopsin. Structure 12:1281–1288. https://doi.org/10.1016/j.str.2004.04.016
Bordignon E, Klare JP, Doebber M et al (2005) Structural analysis of a HAMP domain. J Biol Chem 280:38767–38775. https://doi.org/10.1074/jbc.M509391200
Bordignon E, Klare JP, Holterhues J et al (2007) Analysis of light-induced conformational changes of Natronomonas pharaonis sensory rhodopsin II by time resolved electron paramagnetic resonance spectroscopy. Photochem Photobiol 83:263–272
Borshchevskiy V, Efremov R, Moiseeva E et al (2010) Overcoming merohedral twinning in crystals of bacteriorhodopsin grown in lipidic mesophase. Acta Crystallogr D Biol Crystallogr 66:26–32. https://doi.org/10.1107/S0907444909042838
Borshchevskiy VI, Round ES, Popov AN et al (2011) X-ray-radiation-induced changes in bacteriorhodopsin structure. J Mol Biol 409:813–825. https://doi.org/10.1016/j.jmb.2011.04.038
Borshchevskiy V, Round E, Erofeev I et al (2014) Low-dose X-ray radiation induces structural alterations in proteins. Acta Crystallogr D Biol Crystallogr 70:2675–2685. https://doi.org/10.1107/S1399004714017295
Boyden ES, Zhang F, Bamberg E et al (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8:1263–1268. https://doi.org/10.1038/nn1525
Braiman M, Mathies R (1982) Resonance Raman spectra of bacteriorhodopsin’s primary photoproduct: evidence for a distorted 13-cis retinal chromophore. Proc Natl Acad Sci U S A 79:403–407
Broecker J, Eger BT, Ernst OP (2017) Crystallogenesis of membrane proteins mediated by polymer-bounded lipid nanodiscs. Structure 25:384–392. https://doi.org/10.1016/j.str.2016.12.004
Brown LS (2004) Fungal rhodopsins and opsin-related proteins: eukaryotic homologues of bacteriorhodopsin with unknown functions. Photochem Photobiol Sci 3:555–565. https://doi.org/10.1039/b315527g
Butt HJ, Downing KH, Hansma PK (1990) Imaging the membrane protein bacteriorhodopsin with the atomic force microscope. Biophys J 58:1473–1480. https://doi.org/10.1016/S0006-3495(90)82492-9
Chan SK, Kitajima-Ihara T, Fujii R et al (2014) Crystal structure of cruxrhodopsin-3 from Haloarcula vallismortis. PLoS ONE 9:e108362. https://doi.org/10.1371/journal.pone.0108362
Chan SK, Kawaguchi H, Kubo H et al (2016) Crystal structure of the 11-cis isomer of pharaonis halorhodopsin: structural constraints on interconversions among different isomeric states. Biochemistry 55:4092–4104. https://doi.org/10.1021/acs.biochem.6b00277
Cherezov V, Peddi A, Muthusubramaniam L et al (2004) A robotic system for crystallizing membrane and soluble proteins in lipidic mesophases. Acta Crystallogr D Biol Crystallogr 60:1795–1807. https://doi.org/10.1107/S0907444904019109
Cherezov V, Rosenbaum DM, Hanson MA et al (2007) High-resolution crystal structure of an engineered human β2-adrenergic G protein–coupled receptor. Science 318:1258–1265. https://doi.org/10.1126/science.1150577
Chizhov I, Engelhard M (2001) Temperature and halide dependence of the photocycle of halorhodopsin from natronobacterium pharaonis. Biophys J 81:1600–1612. https://doi.org/10.1016/S0006-3495(01)75814-6
Chizhov I, Chernavskii DS, Engelhard M et al (1996) Spectrally silent transitions in the bacteriorhodopsin photocycle. Biophys J 71:2329–2345. https://doi.org/10.1016/S0006-3495(96)79475-4
Chow BY, Han X, Dobry AS et al (2010) High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463:98–102. https://doi.org/10.1038/nature08652
Cohen AE, Venkatachalam V (2014) Bringing bioelectricity to light. Annu Rev Biophys 43:211–232. https://doi.org/10.1146/annurev-biophys-051013-022717
de la Torre JR, Christianson LM, Béjà O et al (2003) Proteorhodopsin genes are distributed among divergent marine bacterial taxa. Proc Natl Acad Sci U S A 100:12830–12835. https://doi.org/10.1073/pnas.2133554100
Deisenhofer J, Epp O, Miki K et al (1985) Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution. Nature 318:618–624. https://doi.org/10.1038/318618a0
Deisseroth K (2011) Optogenetics. Nat Methods 8:26–29. https://doi.org/10.1038/nmeth.f.324
Deisseroth K (2015) Optogenetics: 10 years of microbial opsins in neuroscience. Nat Neurosci 18:1213–1225. https://doi.org/10.1038/nn.4091
Deisseroth K, Schnitzer MJ (2013) Engineering approaches to illuminating brain structure and dynamics. Neuron 80:568–577. https://doi.org/10.1016/j.neuron.2013.10.032
Dencher N, Wilms M (1975) Flash photometric experiments on the photochemical cycle of bacteriorhodopsin. Biophys Struct Mech 1:259–271. https://doi.org/10.1007/BF00535760
Dencher NA, Dresselhaus D, Zaccai G, Büldt G (1989) Structural changes in bacteriorhodopsin during proton translocation revealed by neutron diffraction. Proc Natl Acad Sci U S A 86:7876–7879
Dioumaev AK, Brown LS, Shih J et al (2002) Proton transfers in the photochemical reaction cycle of proteorhodopsin. Biochemistry 41:5348–5358. https://doi.org/10.1021/bi025563x
Dioumaev AK, Petrovskaya LE, Wang JM et al (2013) Photocycle of Exiguobacterium sibiricum rhodopsin characterized by low-temperature trapping in the IR and time-resolved studies in the visible. J Phys Chem B 117:7235–7253. https://doi.org/10.1021/jp402430w
Doebber M, Bordignon E, Klare JP et al (2008) Salt-driven equilibrium between two conformations in the HAMP domain from Natronomonas pharaonis: the language of signal transfer? J Biol Chem 283:28691–28701. https://doi.org/10.1074/jbc.M801931200
Dong B, Sánchez-Magraner L, Luecke H (2016) Structure of an inward proton-transporting Anabaena sensory rhodopsin mutant: mechanistic insights. Biophys J 111:963–972. https://doi.org/10.1016/j.bpj.2016.04.055
Duschl A, Lanyi JK, Zimányi L (1990) Properties and photochemistry of a halorhodopsin from the haloalkalophile, Natronobacterium pharaonis. J Biol Chem 265:1261–1267
Edman K, Royant A, Nollert P et al (2002) Early structural rearrangements in the photocycle of an integral membrane sensory receptor. Structure 10:473–482. https://doi.org/10.1016/S0969-2126(02)00736-0
Emiliani V, Cohen AE, Deisseroth K, Häusser M (2015) All-optical interrogation of neural circuits. J Neurosci 35:13917–13926. https://doi.org/10.1523/JNEUROSCI.2916-15.2015
Enami N, Yoshimura K, Murakami M et al (2006) Crystal structures of archaerhodopsin-1 and -2: common structural motif in archaeal light-driven proton pumps. J Mol Biol 358:675–685. https://doi.org/10.1016/j.jmb.2006.02.032
Engelhard M, Hess B, Emeis D et al (1989) Magic angle sample spinning carbon-13 nuclear magnetic resonance of isotopically labeled bacteriorhodopsin. Biochemistry 28:3967–3975. https://doi.org/10.1021/bi00435a051
Ernst OP, Murcia PAS, Daldrop P et al (2008) Photoactivation of channelrhodopsin. J Biol Chem 283:1637–1643. https://doi.org/10.1074/jbc.M708039200
Ernst OP, Lodowski DT, Elstner M et al (2014) Microbial and animal rhodopsins: structures, functions, and molecular mechanisms. Chem Rev 114:126–163. https://doi.org/10.1021/cr4003769
Essen L-O (2002) Halorhodopsin: light-driven ion pumping made simple? Curr Opin Struct Biol 12:516–522
Etzkorn M, Martell S, Andronesi OC et al (2007) Secondary structure, dynamics, and topology of a seven-helix receptor in native membranes, studied by solid-state NMR spectroscopy. Angew Chem Int Ed 46:459–462. https://doi.org/10.1002/anie.200602139
Etzkorn M, Seidel K, Li L et al (2010) Complex formation and light activation in membrane-embedded sensory rhodopsin II as seen by solid-state NMR spectroscopy. Structure 18:293–300. https://doi.org/10.1016/j.str.2010.01.011
Faham S, Bowie JU (2002) Bicelle crystallization: a new method for crystallizing membrane proteins yields a monomeric bacteriorhodopsin structure. J Mol Biol 316:1–6. https://doi.org/10.1006/jmbi.2001.5295
Feldbauer K, Zimmermann D, Pintschovius V et al (2009) Channelrhodopsin-2 is a leaky proton pump. Proc Natl Acad Sci U S A 106:12317–12322. https://doi.org/10.1073/pnas.0905852106
Flytzanis NC, Bedbrook CN, Chiu H et al (2014) Archaerhodopsin variants with enhanced voltage sensitive fluorescence in mammalian and caenorhabditis elegans neurons. Nat Commun 5:4894. https://doi.org/10.1038/ncomms5894
Friedrich T, Geibel S, Kalmbach R et al (2002) Proteorhodopsin is a light-driven proton pump with variable vectoriality. J Mol Biol 321:821–838
Frigaard N-U, Martinez A, Mincer TJ, DeLong EF (2006) Proteorhodopsin lateral gene transfer between marine planktonic bacteria and archaea. Nature 439:847–850. https://doi.org/10.1038/nature04435
Fu H-Y, Lin Y-C, Chang Y-N et al (2010) A novel six-rhodopsin system in a single Archaeon. J Bacteriol 192:5866–5873. https://doi.org/10.1128/JB.00642-10
Fu H-Y, Yi H-P, Y-H L, Yang C-S (2013) Insight into a single halobacterium using a dual-bacteriorhodopsin system with different functionally optimized pH ranges to cope with periplasmic pH changes associated with continuous light illumination. Mol Microbiol 88:551–561. https://doi.org/10.1111/mmi.12208
Gao S, Nagpal J, Schneider MW et al (2015) Optogenetic manipulation of cGMP in cells and animals by the tightly light-regulated guanylyl-cyclase opsin CyclOp. Nat Commun https://doi.org/10.1038/ncomms9046
Gautier A, Mott HR, Bostock MJ et al (2010) Structure determination of the seven-helix transmembrane receptor sensory rhodopsin II by solution NMR spectroscopy. Nat Struct Mol Biol 17:768–774. https://doi.org/10.1038/nsmb.1807
Ghai R, Mizuno CM, Picazo A et al (2013) Metagenomics uncovers a new group of low GC and ultra-small marine Actinobacteria. Sci Rep https://doi.org/10.1038/srep02471
Giovannoni SJ, Bibbs L, Cho J-C et al (2005) Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438:82–85. https://doi.org/10.1038/nature04032
Gmelin W, Zeth K, Efremov R et al (2007) The crystal structure of the L1 intermediate of halorhodopsin at 1.9 Å resolution. Photochem Photobiol 83:369–377. https://doi.org/10.1562/2006-06-23-RA-947
Gómez-Consarnau L, González JM, Coll-Lladó M et al (2007) Light stimulates growth of proteorhodopsin-containing marine Flavobacteria. Nature 445:210–213. https://doi.org/10.1038/nature05381
Gómez-Consarnau L, Akram N, Lindell K et al (2010) Proteorhodopsin phototrophy promotes survival of marine bacteria during starvation. PLoS Biol 8:e1000358. https://doi.org/10.1371/journal.pbio.1000358
Gong Y (2015) The evolving capabilities of rhodopsin-based genetically encoded voltage indicators. Curr Opin Chem Biol 27:84–89. https://doi.org/10.1016/j.cbpa.2015.05.006
Gong Y, Wagner MJ, Li JZ, Schnitzer MJ (2014) Imaging neural spiking in brain tissue using FRET-opsin protein voltage sensors. Nat Commun 5:3674. https://doi.org/10.1038/ncomms4674
Gong Y, Huang C, Li JZ et al (2015) High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor. Science 350:1361–1366. https://doi.org/10.1126/science.aab0810
Good DB, Wang S, Ward ME et al (2014) Conformational dynamics of a seven transmembrane helical protein Anabaena sensory rhodopsin probed by solid-state NMR. J Am Chem Soc 136:2833–2842. https://doi.org/10.1021/ja411633w
Gordeliy VI, Labahn J, Moukhametzianov R et al (2002) Molecular basis of transmembrane signalling by sensory rhodopsin II–transducer complex. Nature 419:484–487. https://doi.org/10.1038/nature01109
Govorunova EG, Sineshchekov OA, Janz R et al (2015) Natural light-gated anion channels: a family of microbial rhodopsins for advanced optogenetics. Science 349:647–650. https://doi.org/10.1126/science.aaa7484
Govorunova EG, Sineshchekov OA, Spudich JL (2016) Structurally distinct cation channelrhodopsins from cryptophyte algae. Biophys J 110:2302–2304. https://doi.org/10.1016/j.bpj.2016.05.001
Govorunova EG, Sineshchekov OA, Li H, Spudich JL (2017a) Microbial rhodopsins: diversity, mechanisms, and optogenetic applications. Annu Rev Biochem 86:845–872. https://doi.org/10.1146/annurev-biochem-101910-144233
Govorunova EG, Sineshchekov OA, Rodarte EM et al (2017b) The expanding family of natural anion channelrhodopsins reveals large variations in kinetics, conductance, and spectral sensitivity. Sci Rep 7:43358. https://doi.org/10.1038/srep43358
Gradinaru V, Thompson KR, Deisseroth K (2008) eNpHR: a Natronomonas halorhodopsin enhanced for optogenetic applications. Brain Cell Biol 36:129–139. https://doi.org/10.1007/s11068-008-9027-6
Grigorieff N, Ceska TA, Downing KH et al (1996) Electron-crystallographic refinement of the structure of bacteriorhodopsin. J Mol Biol 259:393–421. https://doi.org/10.1006/jmbi.1996.0328
Grote M, Engelhard M, Hegemann P (2014) Of ion pumps, sensors and channels – perspectives on microbial rhodopsins between science and history. Biochim Biophys Acta 1837:533–545. https://doi.org/10.1016/j.bbabio.2013.08.006
Grudinin S, Büldt G, Gordeliy V, Baumgaertner A (2005) Water molecules and hydrogen-bonded networks in bacteriorhodopsin – molecular dynamics simulations of the ground state and the M-intermediate. Biophys J 88:3252–3261. https://doi.org/10.1529/biophysj.104.047993
Gushchin I, Gordeliy VI, Grudinin S (2011a) Role of the HAMP domain region of sensory rhodopsin transducers in signal transduction. Biochemistry 50:574–580. https://doi.org/10.1021/bi101032a
Gushchin I, Reshetnyak A, Borshchevskiy V et al (2011b) Active state of sensory rhodopsin II: structural determinants for signal transfer and proton pumping. J Mol Biol 412:591–600. https://doi.org/10.1016/j.jmb.2011.07.022
Gushchin I, Chervakov P, Kuzmichev P et al (2013a) Structural insights into the proton pumping by unusual proteorhodopsin from nonmarine bacteria. Proc Natl Acad Sci U S A 110:12631–12636. https://doi.org/10.1073/pnas.1221629110
Gushchin I, Gordeliy V, Grudinin S (2013b) Two distinct states of the HAMP domain from sensory rhodopsin transducer observed in unbiased molecular dynamics simulations. PLoS ONE 8:e66917. https://doi.org/10.1371/journal.pone.0066917
Gushchin I, Gordeliy V (2017) Transmembrane signal transduction in two-component systems: piston, scissoring, or helical rotation? BioEssays 1700197. https://doi.org/10.1002/bies.201700197
Gushchin I, Shevchenko V, Polovinkin V et al (2015) Crystal structure of a light-driven sodium pump. Nat Struct Mol Biol 22:390–395. https://doi.org/10.1038/nsmb.3002
Gushchin I, Shevchenko V, Polovinkin V et al (2016) Structure of the light-driven sodium pump KR2 and its implications for optogenetics. FEBS J 283:1232–1238. https://doi.org/10.1111/febs.13585
Gushchin I, Melnikov I, Polovinkin V et al (2017) Mechanism of transmembrane signaling by sensor histidine kinases. Science https://doi.org/10.1126/science.aah6345
Han X, Boyden ES (2007) Multiple-color optical activation, silencing, and desynchronization of neural activity, with single-spike temporal resolution. PLoS ONE 2:e299. https://doi.org/10.1371/journal.pone.0000299
Han X, Chow BY, Zhou H et al (2011) A high-light sensitivity optical neural silencer: development and application to optogenetic control of non-human primate cortex. Front Syst Neurosci https://doi.org/10.3389/fnsys.2011.00018
Harris A, Ljumovic M, Bondar A-N et al (2015) A new group of eubacterial light-driven retinal-binding proton pumps with an unusual cytoplasmic proton donor. Biochim Biophys Acta 1847:1518–1529. https://doi.org/10.1016/j.bbabio.2015.08.003
Hasemi T, Kikukawa T, Kamo N, Demura M (2016) Characterization of a cyanobacterial chloride-pumping rhodopsin and its conversion into a proton pump. J Biol Chem 291:355–362. https://doi.org/10.1074/jbc.M115.688614
Hayashi S (2014) Silencing neurons with light. Science 344:369–370. https://doi.org/10.1126/science.1253616
Hayashi S, Tajkhorshid E, Pebay-Peyroula E et al (2001) Structural determinants of spectral tuning in retinal ProteinsBacteriorhodopsin vs sensory rhodopsin II. J Phys Chem B 105:10124–10131. https://doi.org/10.1021/jp011362b
Hayashi S, Tajkhorshid E, Schulten K (2002) Structural changes during the formation of early intermediates in the bacteriorhodopsin photocycle. Biophys J 83:1281–1297. https://doi.org/10.1016/S0006-3495(02)73900-3
Hayashi K, Sudo Y, Jee J et al (2007) Structural analysis of the phototactic transducer protein HtrII linker region from Natronomonas pharaonis. Biochemistry 46:14380–14390. https://doi.org/10.1021/bi701837n
Hazelbauer GL, Falke JJ, Parkinson JS (2008) Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends Biochem Sci 33:9–19. https://doi.org/10.1016/j.tibs.2007.09.014
Hegemann P (2008) Algal sensory photoreceptors. Annu Rev Plant Biol 59:167–189. https://doi.org/10.1146/annurev.arplant.59.032607.092847
Hegemann P, Oesterhelt D, Steiner M (1985) The photocycle of the chloride pump halorhodopsin. I: azidecatalyzed deprotonation of the chromophore is a side reaction of photocycle intermediates inactivating the pump. EMBO J 4:2347–2350
Hegemann P, Ehlenbeck S, Gradmann D (2005) Multiple photocycles of channelrhodopsin. Biophys J 89:3911–3918. https://doi.org/10.1529/biophysj.105.069716
Hempelmann F, Hölper S, Verhoefen M-K et al (2011) His75−Asp97 cluster in green proteorhodopsin. J Am Chem Soc 133:4645–4654. https://doi.org/10.1021/ja111116a
Henderson R, Unwin PNT (1975) Three-dimensional model of purple membrane obtained by electron microscopy. Nature 257:28–32. https://doi.org/10.1038/257028a0
Henderson R, Baldwin JM, Ceska TA et al (1990) Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J Mol Biol 213:899–929. https://doi.org/10.1016/S0022-2836(05)80271-2
Henrich E, Sörmann J, Eberhardt P et al (2017) From gene to function: cell-free electrophysiological and optical analysis of ion pumps in nanodiscs. Biophys J https://doi.org/10.1016/j.bpj.2017.03.026
Hildebrand E, Dencher N (1975) Two photosystems controlling behavioural responses of Halobacterium halobium. Nature 257:46–48. https://doi.org/10.1038/257046a0
Hirai T, Subramaniam S (2009) Protein conformational changes in the bacteriorhodopsin photocycle: comparison of findings from electron and X-ray crystallographic analyses. PLoS ONE 4:e5769. https://doi.org/10.1371/journal.pone.0005769
Hirai T, Subramaniam S, Lanyi JK (2009) Structural snapshots of conformational changes in a seven-helix membrane protein: lessons from bacteriorhodopsin. Curr Opin Struct Biol 19:433–439. https://doi.org/10.1016/j.sbi.2009.07.009
Hochbaum DR, Zhao Y, Farhi SL et al (2014) All-optical electrophysiology in mammalian neurons using engineered microbial rhodopsins. Nat Methods 11:825–833. https://doi.org/10.1038/nmeth.3000
Hoffmann M, Wanko M, Strodel P et al (2006) Color tuning in rhodopsins: the mechanism for the spectral shift between bacteriorhodopsin and sensory rhodopsin II. J Am Chem Soc 128:10808–10818. https://doi.org/10.1021/ja062082i
Hofrichter J, Henry ER, Lozier RH (1989) Photocycles of bacteriorhodopsin in light- and dark-adapted purple membrane studied by time-resolved absorption spectroscopy. Biophys J 56:693–706. PMC1280525
Holterhues J, Bordignon E, Klose D et al (2011) The signal transfer from the receptor NpSRII to the transducer NpHtrII is not hampered by the D75N mutation. Biophys J 100:2275–2282. https://doi.org/10.1016/j.bpj.2011.03.017
Hosaka T, Yoshizawa S, Nakajima Y et al (2016) Structural mechanism for light-driven transport by a new type of chloride ion pump, nonlabens marinus rhodopsin-3. J Biol Chem 291:17488–17495. https://doi.org/10.1074/jbc.M116.728220
Hou JH, Venkatachalam V, Cohen AE (2014) Temporal dynamics of microbial rhodopsin fluorescence reports absolute membrane voltage. Biophys J 106:639–648. https://doi.org/10.1016/j.bpj.2013.11.4493
Hsu M-F, T-F Y, Chou C-C et al (2013) Using Haloarcula marismortui bacteriorhodopsin as a fusion tag for enhancing and visible expression of integral membrane proteins in Escherichia coli. PLoS ONE 8:e56363. https://doi.org/10.1371/journal.pone.0056363
Hsu M-F, H-Y F, Cai C-J et al (2015) Structural and functional studies of a newly grouped haloquadratum walsbyi bacteriorhodopsin reveal the acid-resistant light-driven proton pumping activity. J Biol Chem 290:29567–29577. https://doi.org/10.1074/jbc.M115.685065
Inoue K, Ono H, Abe-Yoshizumi R et al (2013) A light-driven sodium ion pump in marine bacteria. Nat Commun 4:1678. https://doi.org/10.1038/ncomms2689
Inoue K, Koua FHM, Kato Y et al (2014) Spectroscopic study of a light-driven chloride ion pump from marine bacteria. J Phys Chem B 118:11190–11199. https://doi.org/10.1021/jp507219q
Inoue K, Tsukamoto T, Shimono K et al (2015) Converting a light-driven proton pump into a light-gated proton channel. J Am Chem Soc 137:3291–3299. https://doi.org/10.1021/ja511788f
Inoue K, Ito S, Kato Y et al (2016) A natural light-driven inward proton pump. Nat Commun https://doi.org/10.1038/ncomms13415
Irieda H, Morita T, Maki K et al (2012) Photo-induced regulation of the chromatic adaptive gene expression by Anabaena sensory rhodopsin. J Biol Chem 287:32485–32493. https://doi.org/10.1074/jbc.M112.390864
Ishchenko A, Round E, Borshchevskiy V et al (2013) Ground state structure of D75N mutant of sensory rhodopsin II in complex with its cognate transducer. J Photochem Photobiol B Biol 123:55–58. https://doi.org/10.1016/j.jphotobiol.2013.03.008
Ishchenko A, Round E, Borshchevskiy V et al (2017) New insights on signal propagation by sensory rhodopsin II/transducer complex. Sci Rep 7:41811. https://doi.org/10.1038/srep41811
Iverson V, Morris RM, Frazar CD et al (2012) Untangling genomes from metagenomes: revealing an uncultured class of marine Euryarchaeota. Science 335:587–590. https://doi.org/10.1126/science.1212665
Iwamoto M, Shimono K, Sumi M et al (1999) Light-induced proton uptake and release of pharaonis phoborhodopsin detected by a photoelectrochemical cell. J Phys Chem B 103:10311–10315. https://doi.org/10.1021/jp992168g
Jung K-H, Trivedi VD, Spudich JL (2003) Demonstration of a sensory rhodopsin in eubacteria. Mol Microbiol 47:1513–1522. https://doi.org/10.1046/j.1365-2958.2003.03395.x
Kanada S, Takeguchi Y, Murakami M et al (2011) Crystal structures of an O-like blue form and an anion-free yellow form of pharaonis halorhodopsin. J Mol Biol 413:162–176. https://doi.org/10.1016/j.jmb.2011.08.021
Kanehara K, Yoshizawa S, Tsukamoto T, Sudo Y (2017) A phylogenetically distinctive and extremely heat stable light-driven proton pump from the eubacterium Rubrobacter xylanophilus DSM 9941T. Sci Rep https://doi.org/10.1038/srep44427
Kateriya S, Nagel G, Bamberg E, Hegemann P (2004) “Vision” in single-celled algae. Physiology 19:133–137. https://doi.org/10.1152/nips.01517.2004
Kato HE, Zhang F, Yizhar O et al (2012) Crystal structure of the channelrhodopsin light-gated cation channel. Nature 482:369–374. https://doi.org/10.1038/nature10870
Kato HE, Inoue K, Abe-Yoshizumi R et al (2015a) Structural basis for Na+ transport mechanism by a light-driven Na+ pump. Nature 521:48–53. https://doi.org/10.1038/nature14322
Kato Y, Inoue K, Kandori H (2015b) Kinetic analysis of H+–Na+ selectivity in a light-driven Na+-pumping rhodopsin. J Phys Chem Lett 6:5111–5115. https://doi.org/10.1021/acs.jpclett.5b02371
Kato HE, Inoue K, Kandori H, Nureki O (2016) The light-driven sodium ion pump: a new player in rhodopsin research. BioEssays 38:1274–1282. https://doi.org/10.1002/bies.201600065
Kawanabe A, Kandori H (2009) Photoreactions and structural changes of Anabaena sensory rhodopsin. Sensors 9:9741–9804. https://doi.org/10.3390/s91209741
Kawanabe A, Furutani Y, Jung K-H, Kandori H (2007) Photochromism of Anabaena sensory rhodopsin. J Am Chem Soc 129:8644–8649. https://doi.org/10.1021/ja072085a
Kawanabe A, Furutani Y, Jung K-H, Kandori H (2009) Engineering an inward proton transport from a bacterial sensor rhodopsin. J Am Chem Soc 131:16439–16444. https://doi.org/10.1021/ja904855g
Kikukawa T, Shimono K, Tamogami J et al (2011) Photochemistry of Acetabularia rhodopsin II from a marine plant, Acetabularia acetabulum. Biochemistry 50:8888–8898. https://doi.org/10.1021/bi2009932
Kim SY, Yoon SR, Han S et al (2014) A role of Anabaena sensory rhodopsin transducer (ASRT) in photosensory transduction. Mol Microbiol 93:403–414. https://doi.org/10.1111/mmi.12635
Kim K, Kwon S-K, Jun S-H et al (2016) Crystal structure and functional characterization of a light-driven chloride pump having an NTQ motif. Nat Commun 7:12677. https://doi.org/10.1038/ncomms12677
Kitajima-Ihara T, Furutani Y, Suzuki D et al (2008) Salinibacter sensory rhodopsin. Sensory rhodopsin I-like protein from a eubacterium. J Biol Chem 283:23533–23541. https://doi.org/10.1074/jbc.M802990200
Klapoetke NC, Murata Y, Kim SS et al (2014) Independent optical excitation of distinct neural populations. Nat Methods 11:338–346. https://doi.org/10.1038/nmeth.2836
Klare JP, Schmies G, Chizhov I et al (2002) Probing the proton channel and the retinal binding site of Natronobacterium pharaonis sensory rhodopsin II. Biophys J 82:2156–2164
Klare JP, Gordeliy VI, Labahn J et al (2004) The archaeal sensory rhodopsin II/transducer complex: a model for transmembrane signal transfer. FEBS Lett 564:219–224. https://doi.org/10.1016/S0014-5793(04)00193-0
Klare JP, Bordignon E, Engelhard M, Steinhoff H-J (2011) Transmembrane signal transduction in archaeal phototaxis: the sensory rhodopsin II-transducer complex studied by electron paramagnetic resonance spectroscopy. Eur J Cell Biol 90:731–739. https://doi.org/10.1016/j.ejcb.2011.04.013
Kleinlogel S, Feldbauer K, Dempski RE et al (2011) Ultra light-sensitive and fast neuronal activation with the Ca2+-permeable channelrhodopsin CatCh. Nat Neurosci 14:513–518. https://doi.org/10.1038/nn.2776
Klose D, Voskoboynikova N, Orban-Glass I et al (2014) Light-induced switching of HAMP domain conformation and dynamics revealed by time-resolved EPR spectroscopy. FEBS Lett 588:3970–3976. https://doi.org/10.1016/j.febslet.2014.09.012
Klyszejko AL, Shastri S, Mari SA et al (2008) Folding and assembly of proteorhodopsin. J Mol Biol 376:35–41. https://doi.org/10.1016/j.jmb.2007.11.030
Koh EY, Atamna-Ismaeel N, Martin A et al (2010) Proteorhodopsin-bearing bacteria in Antarctic Sea ice. Appl Environ Microbiol 76:5918–5925. https://doi.org/10.1128/AEM.00562-10
Kolbe M, Besir H, Essen L-O, Oesterhelt D (2000) Structure of the light-driven chloride pump halorhodopsin at 1.8 Å resolution. Science 288:1390–1396. https://doi.org/10.1126/science.288.5470.1390
Kondoh M, Inoue K, Sasaki J et al (2011) Transient dissociation of the transducer protein from Anabaena sensory rhodopsin concomitant with formation of the M state produced upon photoactivation. J Am Chem Soc 133:13406–13412. https://doi.org/10.1021/ja202329u
Konno M, Kato Y, Kato HE et al (2015) Mutant of a light-driven sodium ion pump can transport cesium ions. J Phys Chem Lett 7:51–55. https://doi.org/10.1021/acs.jpclett.5b02385
Koua FHM, Kandori H (2015) Light-induced structural changes during early photo-intermediates of the eubacterial Cl− pump Fulvimarina rhodopsin observed by FTIR difference spectroscopy. RSC Adv 6:383–392. https://doi.org/10.1039/C5RA19363J
Kouyama T, Kanada S, Takeguchi Y et al (2010) Crystal structure of the light-driven chloride pump halorhodopsin from Natronomonas pharaonis. J Mol Biol 396:564–579. https://doi.org/10.1016/j.jmb.2009.11.061
Kouyama T, Kawaguchi H, Nakanishi T et al (2015) Crystal structures of the L1, L2, N, and O states of pharaonis halorhodopsin. Biophys J 108:2680–2690. https://doi.org/10.1016/j.bpj.2015.04.027
Kralj JM, Hochbaum DR, Douglass AD, Cohen AE (2011) Electrical spiking in Escherichia coli probed with a fluorescent voltage-indicating protein. Science 333:345–348. https://doi.org/10.1126/science.1204763
Kralj JM, Douglass AD, Hochbaum DR et al (2012) Optical recording of action potentials in mammalian neurons using a microbial rhodopsin. Nat Methods 9:90–95. https://doi.org/10.1038/nmeth.1782
Kwon S-K, Kim BK, Song JY et al (2013) Genomic makeup of the marine flavobacterium nonlabens (Donghaeana) dokdonensis and identification of a novel class of rhodopsins. Genome Biol Evol 5:187–199. https://doi.org/10.1093/gbe/evs134
Landau EM, Rosenbusch JP (1996) Lipidic cubic phases: a novel concept for the crystallization of membrane proteins. Proc Natl Acad Sci U S A 93:14532–14535
Lanyi JK (2004) Bacteriorhodopsin. Annu Rev Physiol 66:665–688. https://doi.org/10.1146/annurev.physiol.66.032102.150049
Lanyi JK (2006) Proton transfers in the bacteriorhodopsin photocycle. Biochim Biophys Acta 1757:1012–1018. https://doi.org/10.1016/j.bbabio.2005.11.003
Lee SC, Bennett BC, Hong W-X et al (2013) Steroid-based facial amphiphiles for stabilization and crystallization of membrane proteins. Proc Natl Acad Sci U S A 110:E1203–E1211. https://doi.org/10.1073/pnas.1221442110
Li X, Gutierrez DV, Hanson MG et al (2005) Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin. Proc Natl Acad Sci U S A 102:17816–17821. https://doi.org/10.1073/pnas.0509030102
Li H, Sineshchekov OA, da Silva GFZ, Spudich JL (2015) In vitro demonstration of dual light-driven Na+/H+ pumping by a microbial rhodopsin. Biophys J 109:1446–1453. https://doi.org/10.1016/j.bpj.2015.08.018
Lin MZ, Schnitzer MJ (2016) Genetically encoded indicators of neuronal activity. Nat Neurosci 19:1142–1153. https://doi.org/10.1038/nn.4359
Lin JY, Lin MZ, Steinbach P, Tsien RY (2009) Characterization of engineered channelrhodopsin variants with improved properties and kinetics. Biophys J 96:1803–1814. https://doi.org/10.1016/j.bpj.2008.11.034
Lin JY, Knutsen PM, Muller A et al (2013) ReaChR: a red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation. Nat Neurosci 16:1499–1508. https://doi.org/10.1038/nn.3502
Lórenz-Fonfría VA, Heberle J (2014) Channelrhodopsin unchained: structure and mechanism of a light-gated cation channel. Biochim Biophys Acta 1837:626–642. https://doi.org/10.1016/j.bbabio.2013.10.014
Lörinczi É, Verhoefen M-K, Wachtveitl J et al (2009) Voltage- and pH-dependent changes in vectoriality of photocurrents mediated by wild-type and mutant proteorhodopsins upon expression in Xenopus oocytes. J Mol Biol 393:320–341. https://doi.org/10.1016/j.jmb.2009.07.055
Lozier RH, Bogomolni RA, Stoeckenius W (1975) Bacteriorhodopsin: a light-driven proton pump in Halobacterium halobium. Biophys J 15:955–962. https://doi.org/10.1016/S0006-3495(75)85875-9
Luck M, Mathes T, Bruun S et al (2012) A photochromic Histidine Kinase Rhodopsin (HKR1) that is bimodally switched by ultraviolet and blue light. J Biol Chem 287:40083–40090. https://doi.org/10.1074/jbc.M112.401604
Luck M, Bruun S, Keidel A et al (2015) Photochemical chromophore isomerization in histidine kinase rhodopsin HKR1. FEBS Lett 589:1067–1071. https://doi.org/10.1016/j.febslet.2015.03.024
Luecke H, Schobert B, Richter H-T et al (1999) Structure of bacteriorhodopsin at 1.55 Å resolution. J Mol Biol 291:899–911. https://doi.org/10.1006/jmbi.1999.3027
Luecke H, Schobert B, Lanyi JK et al (2001) Crystal structure of sensory rhodopsin II at 2.4 Angstroms: insights into color tuning and transducer interaction. Science 293:1499–1503. https://doi.org/10.1126/science.1062977
Luecke H, Schobert B, Stagno J et al (2008) Crystallographic structure of xanthorhodopsin, the light-driven proton pump with a dual chromophore. Proc Natl Acad Sci U S A 105:16561–16565. https://doi.org/10.1073/pnas.0807162105
Maclaurin D, Venkatachalam V, Lee H, Cohen AE (2013) Mechanism of voltage-sensitive fluorescence in a microbial rhodopsin. Proc Natl Acad Sci U S A 110:5939–5944. https://doi.org/10.1073/pnas.1215595110
Man D, Wang W, Sabehi G et al (2003) Diversification and spectral tuning in marine proteorhodopsins. EMBO J 22:1725–1731. https://doi.org/10.1093/emboj/cdg183
Martinez A, Bradley AS, Waldbauer JR et al (2007) Proteorhodopsin photosystem gene expression enables photophosphorylation in a heterologous host. Proc Natl Acad Sci U S A 104:5590–5595. https://doi.org/10.1073/pnas.0611470104
Marwan W, Oesterhelt D (1987) Signal formation in the halobacterial photophobic response mediated by a fourth retinal protein (P480). J Mol Biol 195:333–342
Matsui Y, Sakai K, Murakami M et al (2002) Specific damage induced by X-ray radiation and structural changes in the primary photoreaction of bacteriorhodopsin. J Mol Biol 324:469–481
Matsuno-Yagi A, Mukohata Y (1977) Two possible roles of bacteriorhodopsin; a comparative study of strains of Halobacterium halobium differing in pigmentation. Biochem Biophys Res Commun 78:237–243. https://doi.org/10.1016/0006-291X(77)91245-1
McIsaac RS, Engqvist MKM, Wannier T et al (2014) Directed evolution of a far-red fluorescent rhodopsin. Proc Natl Acad Sci U S A 111:13034–13039. https://doi.org/10.1073/pnas.1413987111
McIsaac RS, Bedbrook CN, Arnold FH (2015) Recent advances in engineering microbial rhodopsins for optogenetics. Curr Opin Struct Biol 33:8–15. https://doi.org/10.1016/j.sbi.2015.05.001
Mohrmann H, Kube I, Lórenz-Fonfría VA et al (2016) Transient conformational changes of sensory rhodopsin II investigated by vibrational stark effect probes. J Phys Chem B 120:4383–4387. https://doi.org/10.1021/acs.jpcb.6b01900
Molnar KS, Bonomi M, Pellarin R et al (2014) Cys-scanning disulfide crosslinking and Bayesian modeling probe the transmembrane signaling mechanism of the histidine kinase, PhoQ. Structure 22:1239–1251. https://doi.org/10.1016/j.str.2014.04.019
Mongodin EF, Nelson KE, Daugherty S et al (2005) The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proc Natl Acad Sci U S A 102:18147–18152. https://doi.org/10.1073/pnas.0509073102
Moukhametzianov R, Klare JP, Efremov R et al (2006) Development of the signal in sensory rhodopsin and its transfer to the cognate transducer. Nature 440:115–119. https://doi.org/10.1038/nature04520
Müller M, Bamann C, Bamberg E, Kühlbrandt W (2011) Projection structure of channelrhodopsin-2 at 6 Å resolution by electron crystallography. J Mol Biol 414:86–95. https://doi.org/10.1016/j.jmb.2011.09.049
Müller M, Bamann C, Bamberg E, Kühlbrandt W (2015) Light-induced helix movements in channelrhodopsin-2. J Mol Biol 427:341–349. https://doi.org/10.1016/j.jmb.2014.11.004
Nagel G, Ollig D, Fuhrmann M et al (2002) Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296:2395–2398. https://doi.org/10.1126/science.1072068
Nagel G, Szellas T, Huhn W et al (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci U S A 100:13940–13945. https://doi.org/10.1073/pnas.1936192100
Nagel G, Brauner M, Liewald JF et al (2005) Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr Biol 15:2279–2284. https://doi.org/10.1016/j.cub.2005.11.032
Nakanishi T, Kanada S, Murakami M et al (2013) Large deformation of helix F during the photoreaction cycle of pharaonis halorhodopsin in complex with azide. Biophys J 104:377–385. https://doi.org/10.1016/j.bpj.2012.12.018
Nango E, Royant A, Kubo M et al (2016) A three-dimensional movie of structural changes in bacteriorhodopsin. Science 354:1552–1557. https://doi.org/10.1126/science.aah3497
Niho A, Yoshizawa S, Tsukamoto T et al (2017) Demonstration of a light-driven SO42–transporter and its spectroscopic characteristics. J Am Chem Soc 139:4376–4389. https://doi.org/10.1021/jacs.6b12139
Nikolaev M, Round E, Gushchin I et al (2017) Integral membrane proteins can be crystallized directly from nanodiscs. Cryst Growth Des 17:945–948. https://doi.org/10.1021/acs.cgd.6b01631
Nikolic K, Grossman N, Grubb MS et al (2009) Photocycles of channelrhodopsin-2. Photochem Photobiol 85:400–411. https://doi.org/10.1111/j.1751-1097.2008.00460.x
Nishikata K, Fuchigami S, Ikeguchi M, Kidera A (2010) Molecular modeling of the HAMP domain of sensory rhodopsin II transducer from Natronomonas pharaonis. Biophysics 6:27–36
Nishikata K, Ikeguchi M, Kidera A (2012) Comparative simulations of the ground state and the M-intermediate state of the sensory rhodopsin II–transducer complex with a HAMP domain model. Biochemistry 51:5958–5966. https://doi.org/10.1021/bi300696b
Nogly P, James D, Wang D et al (2015) Lipidic cubic phase serial millisecond crystallography using synchrotron radiation. IUCrJ 2:168–176. https://doi.org/10.1107/S2052252514026487
Oesterhelt D (1995) Structure and function of halorhodopsin. Isr J Chem 35:475–494. https://doi.org/10.1002/ijch.199500044
Oesterhelt D, Stoeckenius W (1971) Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nature 233:149–152. https://doi.org/10.1038/10.1038/newbio233149a0
Oesterhelt D, Hegemann P, Tittor J (1985) The photocycle of the chloride pump halorhodopsin. II: quantum yields and a kinetic model. EMBO J 4:2351–2356
Oesterhelt F, Oesterhelt D, Pfeiffer M et al (2000) Unfolding pathways of individual bacteriorhodopsins. Science 288:143–146. https://doi.org/10.1126/science.288.5463.143
Orban-Glaß I, Voskoboynikova N, Busch KB et al (2015) Clustering and dynamics of phototransducer signaling domains revealed by site-directed spin labeling electron paramagnetic resonance on SRII/HtrII in membranes and nanodiscs. Biochemistry 54:349–362. https://doi.org/10.1021/bi501160q
Orekhov PS, Klose D, Mulkidjanian AY et al (2015) Signaling and adaptation modulate the dynamics of the photosensoric complex of Natronomonas pharaonis. PLoS Comput Biol 11:e1004561. https://doi.org/10.1371/journal.pcbi.1004561
Orekhov P, Bothe A, Steinhoff H-J et al (2017) Sensory rhodopsin I and sensory rhodopsin II form trimers of dimers in complex with their cognate transducers. Photochem Photobiol 93:796–804. https://doi.org/10.1111/php.12763
Ozaki Y, Kawashima T, Abe-Yoshizumi R, Kandori H (2014) A color-determining amino acid residue of proteorhodopsin. Biochemistry 53:6032–6040. https://doi.org/10.1021/bi500842w
Parkinson JS (2010) Signaling mechanisms of HAMP domains in chemoreceptors and sensor kinases. Annu Rev Microbiol 64:101–122. https://doi.org/10.1146/annurev.micro.112408.134215
Parkinson JS, Hazelbauer GL, Falke JJ (2015) Signaling and sensory adaptation in Escherichia coli chemoreceptors: 2015 update. Trends Microbiol 23:257–266. https://doi.org/10.1016/j.tim.2015.03.003
Pebay-Peyroula E, Rummel G, Rosenbusch JP, Landau EM (1997) X-ray structure of bacteriorhodopsin at 2.5 angstroms from microcrystals grown in lipidic cubic phases. Science 277:1676–1681. https://doi.org/10.1126/science.277.5332.1676
Penzkofer A, Luck M, Mathes T, Hegemann P (2014) Bistable retinal Schiff base photodynamics of Histidine Kinase Rhodopsin HKR1 from Chlamydomonas reinhardtii. Photochem Photobiol 90:773–785. https://doi.org/10.1111/php.12246
Petreanu L, Huber D, Sobczyk A, Svoboda K (2007) Channelrhodopsin-2–assisted circuit mapping of long-range callosal projections. Nat Neurosci 10:663–668. https://doi.org/10.1038/nn1891
Petrovskaya LE, Lukashev EP, Chupin VV et al (2010) Predicted bacteriorhodopsin from Exiguobacterium sibiricum is a functional proton pump. FEBS Lett 584:4193–4196. https://doi.org/10.1016/j.febslet.2010.09.005
Petrovskaya LE, Balashov SP, Lukashev EP et al (2015) ESR – a retinal protein with unusual properties from Exiguobacterium sibiricum. Biochem Mosc 80:688–700
Pinhassi J, DeLong EF, Béjà O et al (2016) Marine bacterial and archaeal ion-pumping rhodopsins: genetic diversity, physiology, and ecology. Microbiol Mol Biol Rev 80:929–954. https://doi.org/10.1128/MMBR.00003-16
Polovinkin V, Gushchin I, Sintsov M et al (2014) High-resolution structure of a membrane protein transferred from amphipol to a lipidic mesophase. J Membr Biol 247:997–1004. https://doi.org/10.1007/s00232-014-9700-x
Racker E, Stoeckenius W (1974) Reconstitution of purple membrane vesicles catalyzing light-driven proton uptake and adenosine triphosphate formation. J Biol Chem 249:662–663
Radu I, Bamann C, Nack M et al (2009) Conformational changes of channelrhodopsin-2. J Am Chem Soc 131:7313–7319. https://doi.org/10.1021/ja8084274
Ran T, Ozorowski G, Gao Y et al (2013) Cross-protomer interaction with the photoactive site in oligomeric proteorhodopsin complexes. Acta Crystallogr D Biol Crystallogr 69:1965–1980. https://doi.org/10.1107/S0907444913017575
Reckel S, Gottstein D, Stehle J et al (2011) Solution NMR structure of proteorhodopsin. Angew Chem Int Ed 50:11942–11946. https://doi.org/10.1002/anie.201105648
Ritter E, Stehfest K, Berndt A et al (2008) Monitoring light-induced structural changes of channelrhodopsin-2 by UV-visible and fourier transform infrared spectroscopy. J Biol Chem 283:35033–35041. https://doi.org/10.1074/jbc.M806353200
Rodrigues DF, Goris J, Vishnivetskaya T et al (2006) Characterization of Exiguobacterium isolates from the Siberian permafrost. Description of Exiguobacterium sibiricum sp. nov. Extremophiles 10:285–294. https://doi.org/10.1007/s00792-005-0497-5
Rodrigues DF, Ivanova N, He Z et al (2008) Architecture of thermal adaptation in an Exiguobacterium sibiricum strain isolated from 3 million year old permafrost: a genome and transcriptome approach. BMC Genomics 9:547. https://doi.org/10.1186/1471-2164-9-547
Royant A, Nollert P, Edman K et al (2001) X-ray structure of sensory rhodopsin II at 2.1-Å resolution. Proc Natl Acad Sci U S A 98:10131–10136. https://doi.org/10.1073/pnas.181203898
Sasaki J, Spudich JL (1999) Proton circulation during the photocycle of sensory rhodopsin II. Biophys J 77:2145–2152. https://doi.org/10.1016/S0006-3495(99)77055-4
Sasaki J, Spudich JL (2000) Proton transport by sensory rhodopsins and its modulation by transducer-binding. Biochim Biophys Acta 1460:230–239. https://doi.org/10.1016/S0005-2728(00)00142-0
Sasaki J, Spudich JL (2008) Signal transfer in Haloarchaeal sensory rhodopsin – transducer complexes. Photochem Photobiol 84:863–868. https://doi.org/10.1111/j.1751-1097.2008.00314.x
Schapiro I, Ruhman S (2014) Ultrafast photochemistry of Anabaena sensory rhodopsin: experiment and theory. Biochim Biophys Acta 1837:589–597. https://doi.org/10.1016/j.bbabio.2013.09.014
Scharf B, Engelhard M (1994) Blue halorhodopsin from Natronobacterium pharaonis: wavelength regulation by anions. Biochemistry 33:6387–6393. https://doi.org/10.1021/bi00187a002
Scheib U, Stehfest K, Gee CE et al (2015) The rhodopsin–guanylyl cyclase of the aquatic fungus Blastocladiella emersonii enables fast optical control of cGMP signaling. Sci Signal 8:rs8. https://doi.org/10.1126/scisignal.aab0611
Schmies G, Lüttenberg B, Chizhov I et al (2000) Sensory rhodopsin II from the haloalkaliphilic natronobacterium pharaonis: light-activated proton transfer reactions. Biophys J 78:967–976. https://doi.org/10.1016/S0006-3495(00)76654-9
Schmies G, Engelhard M, Wood PG et al (2001) Electrophysiological characterization of specific interactions between bacterial sensory rhodopsins and their transducers. Proc Natl Acad Sci U S A 98:1555–1559. https://doi.org/10.1073/pnas.031562298
Schneider F, Grimm C, Hegemann P (2015) Biophysics of channelrhodopsin. Annu Rev Biophys 44:167–186. https://doi.org/10.1146/annurev-biophys-060414-034014
Schobert B, Lanyi JK (1982) Halorhodopsin is a light-driven chloride pump. J Biol Chem 257:10306–10313
Schreiner M, Schlesinger R, Heberle J, Niemann HH (2015) Structure of halorhodopsin from Halobacterium salinarum in a new crystal form that imposes little restraint on the E–F loop. J Struct Biol 190:373–378. https://doi.org/10.1016/j.jsb.2015.04.010
Sharma AK, Zhaxybayeva O, Papke RT, Doolittle WF (2008) Actinorhodopsins: proteorhodopsin-like gene sequences found predominantly in non-marine environments. Environ Microbiol 10:1039–1056. https://doi.org/10.1111/j.1462-2920.2007.01525.x
Shevchenko V, Gushchin I, Polovinkin V et al (2014) Crystal structure of Escherichia coli-expressed Haloarcula marismortui bacteriorhodopsin I in the trimeric form. PLoS ONE 9:e112873. https://doi.org/10.1371/journal.pone.0112873
Shevchenko V, Mager T, Kovalev K et al (2017) Inward H+ pump xenorhodopsin: mechanism and alternative optogenetic approach. Sci Adv 3:e1603187. https://doi.org/10.1126/sciadv.1603187
Shi L, Lake EMR, Ahmed MAM et al (2009) Solid-state NMR study of proteorhodopsin in the lipid environment: secondary structure and dynamics. Biochim Biophys Acta 1788:2563–2574. https://doi.org/10.1016/j.bbamem.2009.09.011
Shibata M, Yamashita H, Uchihashi T et al (2010) High-speed atomic force microscopy shows dynamic molecular processes in photoactivated bacteriorhodopsin. Nat Nanotechnol 5:208–212. https://doi.org/10.1038/nnano.2010.7
Sineshchekov OA, Trivedi VD, Sasaki J, Spudich JL (2005) Photochromicity of Anabaena sensory rhodopsin, an atypical microbial receptor with a cis-retinal light-adapted form. J Biol Chem 280:14663–14668. https://doi.org/10.1074/jbc.M501416200
Slamovits CH, Okamoto N, Burri L et al (2011) A bacterial proteorhodopsin proton pump in marine eukaryotes. Nat Commun 2:183. https://doi.org/10.1038/ncomms1188
Spudich JL, Bogomolni RA (1984) Mechanism of colour discrimination by a bacterial sensory rhodopsin. Nature 312:509–513. https://doi.org/10.1038/312509a0
Spudich EN, Spudich JL (1982) Control of transmembrane ion fluxes to select halorhodopsin-deficient and other energy-transduction mutants of Halobacterium halobium. Proc Natl Acad Sci U S A 79:4308–4312
Spudich EN, Zhang W, Alam M, Spudich JL (1997) Constitutive signaling by the phototaxis receptor sensory rhodopsin II from disruption of its protonated Schiff base–Asp-73 interhelical salt bridge. Proc Natl Acad Sci U S A 94:4960–4965
Strambi A, Durbeej B, Ferré N, Olivucci M (2010) Anabaena sensory rhodopsin is a light-driven unidirectional rotor. Proc Natl Acad Sci U S A 107:21322–21326. https://doi.org/10.1073/pnas.1015085107
Sudo Y, Spudich JL (2006) Three strategically placed hydrogen-bonding residues convert a proton pump into a sensory receptor. Proc Natl Acad Sci U S A 103:16129–16134. https://doi.org/10.1073/pnas.0607467103
Sudo Y, Yoshizawa S (2016) Functional and photochemical characterization of a light-driven proton pump from the Gammaproteobacterium Pantoea vagans. Photochem Photobiol 92:420–427. https://doi.org/10.1111/php.12585
Sudo Y, Iwamoto M, Shimono K et al (2001) Photo-induced proton transport of pharaonis phoborhodopsin (sensory rhodopsin II) is ceased by association with the transducer. Biophys J 80:916–922. https://doi.org/10.1016/S0006-3495(01)76070-5
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. https://doi.org/10.1021/bi901338d
Sudo Y, Ihara K, Kobayashi S et al (2011) A microbial rhodopsin with a unique retinal composition shows both sensory rhodopsin II and bacteriorhodopsin-like properties. J Biol Chem 286:5967–5976. https://doi.org/10.1074/jbc.M110.190058
Takahashi T, Tomioka H, Kamo N, Kobatake Y (1985) A photosystem other than PS370 also mediates the negative phototaxis of<i> Halobacterium halobium</i>. FEMS Microbiol Lett 28:161–164
Takeda K, Sato H, Hino T et al (1998) A novel three-dimensional crystal of bacteriorhodopsin obtained by successive fusion of the vesicular assemblies. J Mol Biol 283:463–474. https://doi.org/10.1006/jmbi.1998.2103
Tomioka H, Takahashi T, Kamo N, Kobatake Y (1986) Flash spectrophotometric identification of a fourth rhodopsin-like pigment in Halobacterium halobium. Biochem Biophys Res Commun 139:389–395. https://doi.org/10.1016/S0006-291X(86)80003-1
Tsukamoto T, Inoue K, Kandori H, Sudo Y (2013) Thermal and spectroscopic characterization of a proton pumping rhodopsin from an extreme thermophile. J Biol Chem 288:21581–21592. https://doi.org/10.1074/jbc.M113.479394
Tsukamoto T, Mizutani K, Hasegawa T et al (2016) X-ray crystallographic structure of thermophilic rhodopsin implications for high thermal stability and optogenetic function. J Biol Chem 291:12223–12232. https://doi.org/10.1074/jbc.M116.719815
Tsukamoto T, Yoshizawa S, Kikukawa T et al (2017) Implications for the light-driven chloride ion transport mechanism of nonlabens marinus rhodopsin 3 by its photochemical characteristics. J Phys Chem B 121:2027–2038. https://doi.org/10.1021/acs.jpcb.6b11101
Tsunoda SP, Ewers D, Gazzarrini S et al (2006) H+-pumping rhodopsin from the marine alga Acetabularia. Biophys J 91:1471–1479. https://doi.org/10.1529/biophysj.106.086421
Ugalde JA, Podell S, Narasingarao P, Allen EE (2011) Xenorhodopsins, an enigmatic new class of microbial rhodopsins horizontally transferred between archaea and bacteria. Biol Direct 6:52. https://doi.org/10.1186/1745-6150-6-52
Váró G, Brown LS, Lakatos M, Lanyi JK (2003) Characterization of the photochemical reaction cycle of proteorhodopsin. Biophys J 84:1202–1207. https://doi.org/10.1016/S0006-3495(03)74934-0
Venkatachalam V, Brinks D, Maclaurin D et al (2014) Flash memory: photochemical imprinting of neuronal action potentials onto a microbial rhodopsin. J Am Chem Soc 136:2529–2537. https://doi.org/10.1021/ja411338t
Vogeley L, Sineshchekov OA, Trivedi VD et al (2004) Anabaena sensory rhodopsin: a photochromic color sensor at 2.0 Å. Science 306:1390–1393. https://doi.org/10.1126/science.1103943
Vogeley L, Trivedi VD, Sineshchekov OA et al (2007) Crystal structure of the Anabaena sensory rhodopsin transducer. J Mol Biol 367:741–751. https://doi.org/10.1016/j.jmb.2006.11.074
Wada T, Shimono K, Kikukawa T et al (2011) Crystal structure of the eukaryotic light-driven proton-pumping rhodopsin, Acetabularia rhodopsin II, from marine alga. J Mol Biol 411:986–998. https://doi.org/10.1016/j.jmb.2011.06.028
Walter JM, Greenfield D, Bustamante C, Liphardt J (2007) Light-powering Escherichia coli with proteorhodopsin. Proc Natl Acad Sci U S A 104:2408–2412. https://doi.org/10.1073/pnas.0611035104
Wang W-W, Sineshchekov OA, Spudich EN, Spudich JL (2003) Spectroscopic and photochemical characterization of a deep ocean proteorhodopsin. J Biol Chem 278:33985–33991. https://doi.org/10.1074/jbc.M305716200
Wang S, Kim SY, Jung K-H et al (2011) A eukaryotic-like interaction of soluble Cyanobacterial sensory rhodopsin transducer with DNA. J Mol Biol 411:449–462. https://doi.org/10.1016/j.jmb.2011.06.002
Wang J, Sasaki J, Tsai A, Spudich JL (2012) HAMP domain signal relay mechanism in a sensory rhodopsin-transducer complex. J Biol Chem 287:21316–21325. https://doi.org/10.1074/jbc.M112.344622
Wang S, Munro RA, Shi L et al (2013a) Solid-state NMR spectroscopy structure determination of a lipid-embedded heptahelical membrane protein. Nat Methods 10:1007–1012. https://doi.org/10.1038/nmeth.2635
Wang T, Sessions AO, Lunde CS et al (2013b) Deprotonation of D96 in bacteriorhodopsin opens the proton uptake pathway. Structure 21:290–297. https://doi.org/10.1016/j.str.2012.12.018
Ward ME, Wang S, Munro R et al (2015) In situ structural studies of Anabaena sensory rhodopsin in the E. coli membrane. Biophys J 108:1683–1696. https://doi.org/10.1016/j.bpj.2015.02.018
Waschuk SA, Bezerra AG, Shi L, Brown LS (2005) Leptosphaeria rhodopsin: bacteriorhodopsin-like proton pump from a eukaryote. Proc Natl Acad Sci U S A 102:6879–6883. https://doi.org/10.1073/pnas.0409659102
Wegener A-A, Chizhov I, Engelhard M, Steinhoff H-J (2000) Time-resolved detection of transient movement of helix F in spin-labelled pharaonis sensory rhodopsin II. J Mol Biol 301:881–891. https://doi.org/10.1006/jmbi.2000.4008
Wegener AA, Klare JP, Engelhard M, Steinhoff HJ (2001) Structural insights into the early steps of receptor-transducer signal transfer in archaeal phototaxis. EMBO J 20:5312–5319. https://doi.org/10.1093/emboj/20.19.5312
Wickstrand C, Dods R, Royant A, Neutze R (2015) Bacteriorhodopsin: would the real structural intermediates please stand up? Biochim Biophys Acta 1850:536–553. https://doi.org/10.1016/j.bbagen.2014.05.021
Wietek J, Prigge M (2016) Enhancing channelrhodopsins: an overview. In: Kianianmomeni A (ed) Optogenetics. Springer, New York, pp 141–165
Wietek J, Wiegert JS, Adeishvili N et al (2014) Conversion of channelrhodopsin into a light-gated chloride channel. Science 344:409–412. https://doi.org/10.1126/science.1249375
Wolff EK, Bogomolni RA, Scherrer P et al (1986) Color discrimination in halobacteria: spectroscopic characterization of a second sensory receptor covering the blue-green region of the spectrum. Proc Natl Acad Sci U S A 83:7272–7276
Wood K, Tobias DJ, Kessler B et al (2010) The low-temperature inflection observed in neutron scattering measurements of proteins is due to methyl rotation: direct evidence using isotope labeling and molecular dynamics simulations. J Am Chem Soc 132:4990–4991. https://doi.org/10.1021/ja910502g
Yang HH, St-Pierre F (2016) Genetically encoded voltage indicators: opportunities and challenges. J Neurosci 36:9977–9989
Yang J, Aslimovska L, Glaubitz C (2011) Molecular dynamics of proteorhodopsin in lipid bilayers by solid-state NMR. J Am Chem Soc 133:4874–4881. https://doi.org/10.1021/ja109766n
Yoshida K, Tsunoda SP, Brown LS, Kandori H (2017) A unique choanoflagellate enzyme rhodopsin exhibits light-dependent cyclic nucleotide phosphodiesterase activity. J Biol Chem 292:7531–7541. https://doi.org/10.1074/jbc.M117.775569
Yoshimura K, Kouyama T (2008) Structural role of bacterioruberin in the trimeric structure of archaerhodopsin-2. J Mol Biol 375:1267–1281. https://doi.org/10.1016/j.jmb.2007.11.039
Yoshizawa S, Kumagai Y, Kim H et al (2014) Functional characterization of flavobacteria rhodopsins reveals a unique class of light-driven chloride pump in bacteria. Proc Natl Acad Sci U S A 111:6732–6737. https://doi.org/10.1073/pnas.1403051111
Yutin N, Koonin EV (2012) Proteorhodopsin genes in giant viruses. Biol Direct 7:34. https://doi.org/10.1186/1745-6150-7-34
Zander U, Bourenkov G, Popov AN et al (2015) MeshAndCollect: an automated multi-crystal data-collection workflow for synchrotron macromolecular crystallography beamlines. Acta Crystallogr D Biol Crystallogr 71:2328–2343
Zhang F, Vierock J, Yizhar O et al (2011) The microbial opsin family of optogenetic tools. Cell 147:1446–1457. https://doi.org/10.1016/j.cell.2011.12.004
Zhang J, Mizuno K, Murata Y et al (2013) Crystal structure of deltarhodopsin-3 from Haloterrigena thermotolerans. Proteins Struct Funct Bioinf 81:1585–1592. https://doi.org/10.1002/prot.24316
Zhao H, Ma B, Ji L et al (2017) Coexistence of light-driven Na+ and H+ transport in a microbial rhodopsin from Nonlabens dokdonensis. J Photochem Photobiol B Biol 172:70–76. https://doi.org/10.1016/j.jphotobiol.2017.05.004
Zou P, Zhao Y, Douglass AD et al (2014) Bright and fast multicoloured voltage reporters via electrochromic FRET. Nat Commun 5:4625. https://doi.org/10.1038/ncomms5625
Zschiedrich CP, Keidel V, Szurmant H (2016) Molecular mechanisms of two-component signal transduction. J Mol Biol 428:3752–3775. https://doi.org/10.1016/j.jmb.2016.08.003
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The work was supported by the Russian Science Foundation research project 16-15-00242.
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Gushchin, I., Gordeliy, V. (2018). Microbial Rhodopsins. In: Harris, J., Boekema, E. (eds) Membrane Protein Complexes: Structure and Function. Subcellular Biochemistry, vol 87. Springer, Singapore. https://doi.org/10.1007/978-981-10-7757-9_2
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