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Advances in Solid-state NMR Studies of Microbial Rhodopsins

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Modern Magnetic Resonance

Abstract

Microbial rhodopsins are membrane-embedded heptahelical proteins which are responsible for ion transport or signal transduction in cells. Whereas initial research focused on the four microbial rhodopsins found in Halobacterium Salinarium and related haloarchaea, many additional members have been recently discovered in eubacteria and eukarya, and their structures and functions have been extensively studied. Solid-state nuclear magnetic resonance (NMR) spectroscopy is unique among structural and biophysical methods in that it reports on a structure of a membrane protein in its native-like lipid-embedded state. Here we review the developments in solid-state NMR and highlight its recent contributions to the structural studies of microbial rhodopsins.

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References

  1. Oesterhelt D, Stoeckenius W. Functions of a new photoreceptor membrane. Proc Natl Acad Sci U S A. 1973;70:2853–7.

    Article  Google Scholar 

  2. Matsuno-Yagi A, Mukohata Y. Two possible roles of bacteriorhodopsin; a comparative study of strains of Halobacterium halobium differing in pigmentation. Biochem Biophys Res Commun. 1977;78:237–43.

    Article  Google Scholar 

  3. Bogomolni RA, Spudich JL. Identification of a third rhodopsin-like pigment in phototactic Halobacterium halobium. Proc Natl Acad Sci U S A. 1982;79:6250–4.

    Article  Google Scholar 

  4. Takahashi T, Tomioka H, Kamo N, Kobatake Y. A photosystem other than PS370 also mediates the negative phototaxis of Halobacterium-halobium. FEMS Microbiol Lett. 1985;28:161–4.

    Article  Google Scholar 

  5. Beja O, Aravind L, Koonin EV, Suzuki MT, Hadd A, Nguyen LP, Jovanovich S, Gates CM, Feldman RA, Spudich JL, Spudich EN, DeLong EF. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science. 2000;289:1902–6.

    Article  Google Scholar 

  6. Beja O, Spudich EN, Spudich JL, Leclerc M, DeLong EF. Proteorhodopsin phototrophy in the ocean. Nature. 2001;411:786–9.

    Article  Google Scholar 

  7. Ernst OP, Lodowski DT, Elstner M, Hegemann P, Brown LS, Kandori H. Microbial and animal rhodopsins: structures, functions, and molecular mechanisms. Chem Rev. 2014;114:126–63.

    Article  Google Scholar 

  8. Brown LS. Eubacterial rhodopsins – unique photosensors and diverse ion pumps. Biochim Biophys Acta. 2014;1837:553–61.

    Article  Google Scholar 

  9. Inoue K, Tsukamoto T, Sudo Y. Molecular and evolutionary aspects of microbial sensory rhodopsins. Biochim Biophys Acta. 1837;2014:562–77.

    Google Scholar 

  10. Herzfeld J, Lansing JC. Magnetic resonance studies of the bacteriorhodopsin pump cycle. Annu Rev Biophys Biomol Struct. 2002;31:73–95.

    Article  Google Scholar 

  11. Saito H, Naito A. NMR studies on fully hydrated membrane proteins, with emphasis on bacteriorhodopsin as a typical and prototype membrane protein. Biochim Biophys Acta. 1768;2007:3145–61.

    Google Scholar 

  12. Zhou HX, Cross TA. Influences of membrane mimetic environments on membrane protein structures. Annu Rev Biophys. 2013;42:361–92.

    Article  Google Scholar 

  13. Andrew ER, Bradbury A, Eades RG. Nuclear magnetic resonance spectra from a crystal rotated at high speed. Nature. 1958;182:1659.

    Article  Google Scholar 

  14. Lowe IJ. Free induction decay of rotating solids. Phys Rev Lett. 1959;2:285.

    Article  Google Scholar 

  15. Griffin RG. Dipolar recoupling in MAS spectra of biological solids. Nat Struct Biol. 1998;5:508–12.

    Article  Google Scholar 

  16. Colombo MG, Meier BH, Ernst RR. Rotor-driven spin diffusion in natural-abundance C-13 spin systems. Chem Phys Lett. 1988;146:189–96.

    Article  Google Scholar 

  17. Raleigh DP, Levitt MH, Griffin RG. Rotational resonance in solid-state NMR. Chem Phys Lett. 1988;146:71–6.

    Article  Google Scholar 

  18. Bennett AE, Griffin RG, Vega S. Recoupling of homo- and heteronuclear dipolar interactions in rotating solids. In: Blumich B, editor. Solid state NMR IV: methods and applications of solid-state NMR. Berlin: Springer; 1994. p. 1–77.

    Chapter  Google Scholar 

  19. Dusold S, Sebald A. Dipolar recoupling under magic-angle spinning conditions. Annu Rep NMR Spectrosc. 2000;41:185–264.

    Article  Google Scholar 

  20. Ladizhansky V. Homonuclear dipolar recoupling techniques for structure determination in uniformly 13C-labeled proteins. Solid State Nucl Magn Reson. 2009;36:119–28.

    Article  Google Scholar 

  21. Nielsen NC, Strasso LA, Nielsen AB. Dipolar recoupling. Top Curr Chem. 2012;306:1–45.

    Article  Google Scholar 

  22. De Paepe G. Dipolar recoupling in magic angle spinning solid-state nuclear magnetic resonance. Annu Rev Phys Chem. 2012;63:661–84.

    Article  Google Scholar 

  23. Tuzi S, Naito A, Saito H. C-13 NMR-study on conformation and dynamics of the transmembrane alpha-helices, loops, and C-terminus of [3-C-13]ala-labeled bacteriorhodopsin. Biochemistry. 1994;33:15046–52.

    Article  Google Scholar 

  24. Griffiths JM, Bennett AE, Engelhard M, Siebert F, Raap J, Lugtenburg J, Herzfeld J, Griffin RG. Structural investigation of the active site in bacteriorhodopsin: geometric constraints on the roles of Asp-85 and Asp-212 in the proton-pumping mechanism from solid state NMR. Biochemistry. 2000;39:362–71.

    Article  Google Scholar 

  25. Creuzet F, McDermott A, Gebhard R, van der Hoef K, Spijker-Assink MB, Herzfeld J, Lugtenburg J, Levitt MH, Griffin RG. Determination of membrane protein structure by rotational resonance NMR: bacteriorhodopsin. Science. 1991;251:783–6.

    Article  Google Scholar 

  26. Feng X, Lee YK, Sandstrom D, Eden M, Maisel H, Sebald A, Levitt MH. Direct determination of a molecular torsional angle by solid-state NMR. Chem Phys Lett. 1996;257:314–20.

    Article  Google Scholar 

  27. Feng X, Verdegem PJ, Eden M, Sandstrom D, Lee YK, Bovee-Geurts PH, de Grip WJ, Lugtenburg J, de Groot HJ, Levitt MH. Determination of a molecular torsional angle in the metarhodopsin-I photointermediate of rhodopsin by double-quantum solid-state NMR. J Biomol NMR. 2000;16:1–8.

    Article  Google Scholar 

  28. Feng X, Verdegem PJE, Lee YK, Sandstrom D, Eden M, BoveeGeurts P, deGrip WJ, Lugtenburg J, deGroot HJM, Levitt MH. Direct determination of a molecular torsional angle in the membrane protein rhodopsin by solid-state NMR. J Am Chem Soc. 1997;119:6853–7.

    Article  Google Scholar 

  29. Lansing JC, Hohwy M, Jaroniec CP, Creemers AF, Lugtenburg J, Herzfeld J, Griffin RG. Chromophore distortions in the bacteriorhodopsin photocycle: evolution of the H-C14-C15-H dihedral angle measured by solid-state NMR. Biochemistry. 2002;41:431–8.

    Article  Google Scholar 

  30. Becker-Baldus J, Bamann C, Saxena K, Gustmann H, Brown LJ, Brown RC, Reiter C, Bamberg E, Wachtveitl J, Schwalbe H, Glaubitz C. Enlightening the photoactive site of channelrhodopsin-2 by DNP-enhanced solid-state NMR spectroscopy. Proc Natl Acad Sci U S A. 2015;112:9896–901.

    Article  Google Scholar 

  31. Tuzi S, Hasegawa J, Kawaminami R, Naito A, Saito H. Regio-selective detection of dynamic structure of transmembrane alpha-helices as revealed from C-13 NMR spectra of [3-C-13]Ala-labeled bacteriorhodopsin in the presence of Mn2+ ion. Biophys J. 2001;81:425–34.

    Article  Google Scholar 

  32. Tian C, Gao PF, Pinto LH, Lamb RA, Cross TA. Initial structural and dynamic characterization of the M2 protein transmembrane and amphipathic helices in lipid bilayers. Protein Sci. 2003;12:2597–605.

    Article  Google Scholar 

  33. Shi L, Kawamura I, Jung KH, Brown LS, Ladizhansky V. Conformation of a seven-helical transmembrane photosensor in the lipid environment. Angew Chem Int Ed Eng. 2011;50:1302–5.

    Article  Google Scholar 

  34. Harbison GS, Roberts JE, Herzfeld J, Griffin RG. Solid-state NMR detection of proton-exchange between the bacteriorhodopsin schiff-base and bulk water. J Am Chem Soc. 1988;110:7221–3.

    Article  Google Scholar 

  35. Reif B. Ultra-high resolution in MAS solid-state NMR of perdeuterated proteins: implications for structure and dynamics. J Magn Reson. 2012;216:1–12.

    Article  Google Scholar 

  36. Linser R, Dasari M, Hiller M, Higman V, Fink U, Lopez del Amo JM, Markovic S, Handel L, Kessler B, Schmieder P, Oesterhelt D, Oschkinat H, Reif B. Proton-detected solid-state NMR spectroscopy of fibrillar and membrane proteins. Angew Chem Int Ed Eng. 2011;50:4508–12.

    Article  Google Scholar 

  37. Stanek J, Andreas LB, Jaudzems K, Cala D, Lalli D, Bertarello A, Schubeis T, Akopjana I, Kotelovica S, Tars K, Pica A, Leone S, Picone D, Xu ZQ, Dixon NE, Martinez D, Berbon M, El Mammeri N, Noubhani A, Saupe S, Habenstein B, Loquet A, Pintacuda G. NMR spectroscopic assignment of backbone and side-chain protons in fully protonated proteins: microcrystals, sedimented assemblies, and amyloid fibrils. Angew Chem Int Ed Eng. 2016;55:15504–9.

    Article  Google Scholar 

  38. Hall DA, Maus DC, Gerfen GJ, Inati SJ, Becerra LR, Dahlquist FW, Griffin RG. Polarization-enhanced NMR spectroscopy of biomolecules in frozen solution. Science. 1997;276:930–2.

    Article  Google Scholar 

  39. Song CS, Hu KN, Joo CG, Swager TM, Griffin RG. TOTAPOL: a biradical polarizing agent for dynamic nuclear polarization experiments in aqueous media. J Am Chem Soc. 2006;128:11385–90.

    Article  Google Scholar 

  40. Sauvee C, Rosay M, Casano G, Aussenac F, Weber RT, Ouari O, Tordo P. Highly efficient, water-soluble polarizing agents for dynamic nuclear polarization at high frequency. Angew Chem Int Ed Eng. 2013;52:10858–61.

    Article  Google Scholar 

  41. Mak-Jurkauskas ML, Bajaj VS, Hornstein MK, Belenky M, Griffin RG, Herzfeld J. Energy transformations early in the bacteriorhodopsin photocycle revealed by DNP-enhanced solid-state NMR. Proc Natl Acad Sci U S A. 2008;105:883–8.

    Article  Google Scholar 

  42. Bajaj VS, Mak-Jurkauskas ML, Belenky M, Herzfeld J, Griffin RG. Functional and shunt states of bacteriorhodopsin resolved by 250 GHz dynamic nuclear polarization-enhanced solid-state NMR. Proc Natl Acad Sci U S A. 2009;106:9244–9.

    Article  Google Scholar 

  43. Bruun S, Stoeppler D, Keidel A, Kuhlmann U, Luck M, Diehl A, Geiger MA, Woodmansee D, Trauner D, Hegemann P, Oschkinat H, Hildebrandt P, Stehfest K. Light-dark adaptation of channelrhodopsin involves photoconversion between the all-trans and 13-cis retinal isomers. Biochemistry. 2015;54:5389–400.

    Article  Google Scholar 

  44. Maciejko J, Mehler M, Kaur J, Lieblein T, Morgner N, Ouari O, Tordo P, Becker-Baldus J, Glaubitz C. Visualizing specific cross-protomer interactions in the homo-oligomeric membrane protein proteorhodopsin by dynamic-nuclear-polarization-enhanced solid-state NMR. J Am Chem Soc. 2015;137:9032–43.

    Article  Google Scholar 

  45. Engelhard M, Hess B, Emeis D, Metz G, Kreutz W, Siebert F. Magic angle sample spinning 13C nuclear magnetic resonance of isotopically labeled bacteriorhodopsin. Biochemistry. 1989;28:3967–75.

    Article  Google Scholar 

  46. Metz G, Siebert F, Engelhard M. Asp85 is the only internal aspartic acid that gets protonated in the M intermediate and the purple-to-blue transition of bacteriorhodopsin. A solid-state 13C CP-MAS NMR investigation. FEBS Lett. 1992;303:237–41.

    Article  Google Scholar 

  47. Lakshmi KV, Farrar MR, Raap J, Lugtenburg J, Griffin RG, Herzfeld J. Solid-state C-13-NMR and N-15-NMR investigations of the N intermediate of bacteriorhodopsin. Biochemistry. 1994;33:8853–7.

    Article  Google Scholar 

  48. Hu JG, Sun BQ, Bizounok M, Hatcher ME, Lansing JC, Raap J, Verdegem PJ, Lugtenburg J, Griffin RG, Herzfeld J. Early and late M intermediates in the bacteriorhodopsin photocycle: a solid-state NMR study. Biochemistry. 1998;37:8088–96.

    Article  Google Scholar 

  49. Lanyi JK, Schobert B. Structural changes in the L photointermediate of bacteriorhodopsin. J Mol Biol. 2007;365:1379–92.

    Article  Google Scholar 

  50. Beja O, Suzuki MT, Heidelberg JF, Nelson WC, Preston CM, Hamada T, Eisen JA, Fraser CM, DeLong EF. Unsuspected diversity among marine aerobic anoxygenic phototrophs. Nature. 2002;415:630–3.

    Article  Google Scholar 

  51. Sabehi G, Massana R, Bielawski JP, Rosenberg M, Delong EF, Beja O. Novel proteorhodopsin variants from the Mediterranean and Red Seas. Environ Microbiol. 2003;5:842–9.

    Article  Google Scholar 

  52. Sabehi G, Loy A, Jung KH, Partha R, Spudich JL, Isaacson T, Hirschberg J, Wagner M, Beja O. New insights into metabolic properties of marine bacteria encoding proteorhodopsins. PLoS Biol. 2005;3:1409–17.

    Article  Google Scholar 

  53. de la Torre JR, Christianson LM, Beja O, Suzuki MT, Karl DM, Heidelberg J, DeLong EF. Proteorhodopsin genes are distributed among divergent marine bacterial taxa. P Natl Acad Sci USA. 2003;100:12830–5.

    Article  Google Scholar 

  54. Dioumaev AK, Brown LS, Shih J, Spudich EN, Spudich JL, Lanyi JK. Proton transfers in the photochemical reaction cycle of proteorhodopsin. Biochemistry. 2002;41:5348–58.

    Article  Google Scholar 

  55. Bergo VB, Sineshchekov OA, Kralj JM, Partha R, Spudich EN, Rothschild KJ, Spudich JL. His-75 in proteorhodopsin, a novel component in light-driven proton translocation by primary pumps. J Biol Chem. 2009;284:2836–43.

    Article  Google Scholar 

  56. Hempelmann F, Holper S, Verhoefen MK, Woerner AC, Kohler T, Fiedler SA, Pfleger N, Wachtveitl J, Glaubitz C. His75-Asp97 cluster in green proteorhodopsin. J Am Chem Soc. 2011;133:4645–54.

    Article  Google Scholar 

  57. Garczarek F, Brown LS, Lanyi JK, Gerwert K. Proton binding within a membrane protein by a protonated water cluster. P Natl Acad Sci USA. 2005;102:3633–8.

    Article  Google Scholar 

  58. Pfleger N, Worner AC, Yang J, Shastri S, Hellmich UA, Aslimovska L, Maier MS, Glaubitz C. Solid-state NMR and functional studies on proteorhodopsin. Biochim Biophys Acta. 2009;1787:697–705.

    Article  Google Scholar 

  59. Shi L, Ahmed MA, Zhang W, Whited G, Brown LS, Ladizhansky V. Three-dimensional solid-state NMR study of a seven-helical integral membrane proton pump-structural insights. J Mol Biol. 2009;386:1078–93.

    Article  Google Scholar 

  60. Shi L, Lake EM, Ahmed MA, Brown LS, Ladizhansky V. Solid-state NMR study of proteorhodopsin in the lipid environment: secondary structure and dynamics. Biochim Biophys Acta. 2009;1788:2563–74.

    Article  Google Scholar 

  61. Ward ME, Shi L, Lake E, Krishnamurthy S, Hutchins H, Brown LS, Ladizhansky V. Proton-detected solid-state NMR reveals intramembrane polar networks in a seven-helical transmembrane protein proteorhodopsin. J Am Chem Soc. 2011;133:17434–43.

    Article  Google Scholar 

  62. Heyn MP, Cherry RJ, Dencher NA. Lipid-protein interactions in bacteriorhodopsin – dimyristoylphosphatidylcholine vesicles. Biochemistry. 1981;20:840–9.

    Article  Google Scholar 

  63. Hoffmann J, Aslimovska L, Bamann C, Glaubitz C, Bamberg E, Brutschy B. Studying the stoichiometries of membrane proteins by mass spectrometry: microbial rhodopsins and a potassium ion channel. Phys Chem Chem Phys. 2010;12:3480–5.

    Article  Google Scholar 

  64. Stone KM, Voska J, Kinnebrew M, Pavlova A, Junk MJ, Han S. Structural insight into proteorhodopsin oligomers. Biophys J. 2013;104:472–81.

    Article  Google Scholar 

  65. Edwards DT, Huber T, Hussain S, Stone KM, Kinnebrew M, Kaminker I, Matalon E, Sherwin MS, Goldfarb D, Han S. Determining the oligomeric structure of proteorhodopsin by Gd3+−based pulsed dipolar spectroscopy of multiple distances. Structure. 2014;22:1–10.

    Article  Google Scholar 

  66. Klyszejko AL, Shastri S, Mari SA, Grubmuller H, Muller DJ, Glaubitz C. Folding and assembly of proteorhodopsin. J Mol Biol. 2008;376:35–41.

    Article  Google Scholar 

  67. Wang N, Wang M, Gao Y, Ran T, Lan Y, Wang J, Xu L, Wang W. Crystallization and preliminary X-ray crystallographic analysis of a blue-light-absorbing proteorhodopsin. Acta Crystallogr Sect F Struct Biol Cryst Commun. 2012;68:281–3.

    Article  Google Scholar 

  68. Ran T, Ozorowski G, Gao Y, Sineshchekov OA, Wang W, Spudich JL, Luecke H. Cross-protomer interaction with the photoactive site in oligomeric proteorhodopsin complexes. Acta Crystallogr D Biol Crystallogr. 2013;69:1965–80.

    Article  Google Scholar 

  69. Hing AW, Vega S, Schaefer J. Transferred-echo double-resonance NMR. J Magn Reson. 1992;96:205–9.

    Google Scholar 

  70. Jaroniec CP, Filip C, Griffin RG. 3D TEDOR NMR experiments for the simultaneous measurement of multiple carbon-nitrogen distances in uniformly C-13, N-15-labeled solids. J Am Chem Soc. 2002;124:10728–42.

    Article  Google Scholar 

  71. Yomoda H, Makino Y, Tomonaga Y, Hidaka T, Kawamura I, Okitsu T, Wada A, Sudo Y, Naito A. Color-discriminating retinal configurations of sensory rhodopsin I by photo-irradiation solid-state NMR spectroscopy. Angew Chem Int Ed Eng. 2014;53:6960–4.

    Article  Google Scholar 

  72. Tomonaga Y, Hidaka T, Kawamura I, Nishio T, Ohsawa K, Okitsu T, Wada A, Sudo Y, Kamo N, Ramamoorthy A, Naito A. An active photoreceptor intermediate revealed by in situ photoirradiated solid-state NMR spectroscopy. Biophys J. 2011;101:L50–2.

    Article  Google Scholar 

  73. Gordeliy VI, Labahn J, Moukhametzianov R, Efremov R, Granzin J, Schlesinger R, Buldt G, Savopol T, Scheidig AJ, Klare JP, Engelhard M. Molecular basis of transmembrane signalling by sensory rhodopsin II-transducer complex. Nature. 2002;419:484–7.

    Article  Google Scholar 

  74. Jung KH, Trivedi VD, Spudich JL. Demonstration of a sensory rhodopsin in eubacteria. Mol Microbiol. 2003;47:1513–22.

    Article  Google Scholar 

  75. Vogeley L, Trivedi VD, Sineshchekov OA, Spudich EN, Spudich JL, Luecke H. Crystal structure of the Anabaena sensory rhodopsin transducer. J Mol Biol. 2007;367:741–51.

    Article  Google Scholar 

  76. Kondoh M, Inoue K, Sasaki J, Spudich JL, Terazima M. Transient dissociation of the transducer protein from anabaena sensory rhodopsin concomitant with formation of the M state produced upon photoactivation. J Am Chem Soc. 2011;133:13406–12.

    Article  Google Scholar 

  77. Jung KH. The distinct signaling mechanisms of microbial sensory rhodopsins in Archaea Eubacteria and Eukarya. Photochem Photobiol. 2007;83:63–9.

    Article  Google Scholar 

  78. Wang S, Kim SY, Jung KH, Ladizhansky V, Brown LS. A eukaryotic-like interaction of soluble cyanobacterial sensory rhodopsin transducer with DNA. J Mol Biol. 2011;411:449–62.

    Article  Google Scholar 

  79. Vogeley L, Sineshchekov OA, Trivedi VD, Sasaki J, Spudich JL, Luecke H. Anabaena sensory rhodopsin: a photochromic color sensor at 2.0 A. Science. 2004;306:1390–3.

    Article  Google Scholar 

  80. Wang S, Munro RA, Shi L, Kawamura I, Okitsu T, Wada A, Kim SY, Jung KH, Brown LS, Ladizhansky V. Solid-state NMR spectroscopy structure determination of a lipid-embedded heptahelical membrane protein. Nat Methods. 2013;10:1007–12.

    Article  Google Scholar 

  81. Wang S, Shi L, Kawamura I, Brown LS, Ladizhansky V. Site-specific solid-state NMR detection of hydrogen-deuterium exchange reveals conformational changes in a 7-helical transmembrane protein. Biophys J. 2011;101:L23–5.

    Article  Google Scholar 

  82. Ward ME, Wang S, Munro RA, Ritz E, Hung I, Gor'kov PL, Jiang Y, Liang H, Brown LS, Ladizhansky V. In situ structural studies of Anabaena sensory rhodopsin in the E. coli membrane. Biophys J. 2015;108:1683–96.

    Article  Google Scholar 

  83. Kato HE, Zhang F, Yizhar O, Ramakrishnan C, Nishizawa T, Hirata K, Ito J, Aita Y, Tsukazaki T, Hayashi S, Hegemann P, Maturana AD, Ishitani R, Deisseroth K, Nureki O. Crystal structure of the channelrhodopsin light-gated cation channel. Nature. 2012;482:369–74.

    Article  Google Scholar 

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Acknowledgments

This work was supported by NSERC Discovery grant to V.L. We thank Dr. M. Baldus for providing us with high-resolution figures for this review.

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Correspondence to Vladimir Ladizhansky .

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Glossary

ASR

Anabaena Sensory Rhodopsin

ASRT

Anabaena Sensory Rhodopsin Transducer

BR

Bacteriorhodopsin

ChR1

Channelrhodopsin 1

ChR2

Channelrhodopsin 2

DMPA

1,2-dimyristoyl-sn-glycero-3-phosphate

DMPC

1,2-dimyristoyl-sn-glycero-3-phosphocholine

DOPC

1,2-dioleoyl-sn-glycero-3-phosphocholine

GPR

Green Proteorhodopsin

MAS

Magic Angle Spinning

NMR

Nuclear Magnetic Resonance

PRE

Paramagnetic Relaxation Enhancement

SRI

Sensory Rhodopsin I

SRII

Sensory Rhodopsin II

7TM

Seven-Helical

SSNMR

Solid-state NMR

TEDOR

Transferred Echo Double Resonance

TM

Transmembrane

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Ladizhansky, V. (2017). Advances in Solid-state NMR Studies of Microbial Rhodopsins. In: Webb, G. (eds) Modern Magnetic Resonance. Springer, Cham. https://doi.org/10.1007/978-3-319-28275-6_65-1

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