Crystallographic structure of xanthorhodopsin, the light-driven proton pump with a dual chromophore

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 43, 2008, Pages 16561-16565

  Luecke, Hartmut ^a,b   Schobert, Brigitte ^b   Stagno, Jason ^a   Imasheva, Eleonora S ^b   Wang, Jennifer M ^b   Balashov, Sergei P ^b   Lanyi, Janos K ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Carotenoid antenna; Energy transfer; Retinal protein; Salinixanthin; X ray structure

Indexed keywords

ARCHAERHODOPSIN; ASPARTIC ACID; BACTERIAL PROTEIN; BACTERIORHODOPSIN; CAROTENOID; HISTIDINE; MEMBRANE PROTEIN; PROTON PUMP; RETINAL; RHODOPSIN; UNCLASSIFIED DRUG; XANTHORHODOPSIN;

ARCHAEBACTERIUM; ARTICLE; BACTERIUM; CHROMATOPHORE; CRYSTALLOGRAPHY; ENERGY TRANSFER; GEOMETRY; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN MOTIF; PROTON TRANSPORT; REGULATORY MECHANISM; RETINA; STRUCTURE ANALYSIS; X RAY DIFFRACTION;

BACTERIAL PROTEINS; CAROTENOIDS; CRYSTALLOGRAPHY, X-RAY; ENERGY TRANSFER; EUBACTERIUM; LIGHT; PROTEIN CONFORMATION; PROTONS; RETINALDEHYDE; RHODOPSINS, MICROBIAL;

ARCHAEA; BACTERIA (MICROORGANISMS);

EID: 55949126022     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0807162105     Document Type: Article

References (46)

1. Balashov SP, et al. (2005) Xanthorhodopsin: A proton pump with a light-harvesting carotenoid antenna. Science 309:2061-2064.
2. Antón J, et al. (2002) Salinibacter ruber gen nov, sp nov, a novel, extremely halophilic member of the Bacteria from saltern crystallizer ponds. Int J Syst Evol Microbiol 52:485-491.
3. Lutnaes BF, Oren A, Liaaen-Jensen S (2002) New C40-carotenoid acylglycoside as principal carotenoid in Salinibacter ruber, an extremely halophilic eubacterium. J Nat Prod 65:1340-1343.
4. Balashov SP, Imasheva ES, Wang JM, Lanyi JK (2008) Excitation energy-transfer and the relative orientation of retinal and carotenoid in xanthorhodopsin. Biophys J 95:2402-2414.
5. Balashov SP, Imasheva ES, Lanyi JK (2006) Induced chirality of light-harvesting carotenoid salinixanthin and its interaction with the retinal of xanthorhodopsin. Biochemistry 45:10998-11004.
6. Imasheva ES, et al. (2008) Chromophore interaction in xanthorhodopsin: Retinal dependence of salinixanthin binding. Photochem Photobiol 84:977-984.
7. Lanyi JK, Balashov SP (2008) Xanthorhodopsin: A bacteriorhodopsin-like proton pump with a carotenoid antenna. Biochim Biophys Acta 1777:684-688.
8. Imasheva ES, Balashov SP, Wang JM, Lanyi JK (2006) pH-dependent transitions in xanthorhodopsin. Photochem Photobiol 82:1406-1413.
9. Béjà O, et al. (2000) Bacterial rhodopsin: Evidence for a new type of phototrophy in the sea. Science 289:1902-1906.
10. Fuhrman JA, Schwalbach MS, Stingl U (2008) Proteorhodopsins: An array of physiological roles? Nat Rev Microbiol 6:488-494.
11. Giovannoni SJ, et al. (2008) The small genome of an abundant coastal ocean methylotroph. Environ Microbiol 10:1771-1782.
12. Mongodin EF, et al. (2005) The genome of Salinibacter ruber: Convergence and gene exchange among hyperhalophilic bacteria and archaea. Proc Natl Acad Sci USA 102:18147-18152.
13. 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.
14. Michel H, Oesterhelt D, Henderson R (1980) Orthorhombic 2-dimensional crystal form of purple membrane. Proc Natl Acad Sci USA 77:338-342.
15. Kunji ERS, von Gronau S, Oesterhelt D, Henderson R (2000) The 3-dimensional structure of halorhodopsin to 5 Å by electron crystallography: A new unbending procedure for 2-dimensional crystals by using a global reference structure. Proc Natl Acad Sci USA 97:4637-4642.
16. Rouhani S, et al. (2001) Crystal structure of the D85S mutant of bacteriorhodopsin: Model of an O-like photocycle intermediate. J Mol Biol 313:615-628.
17. Luecke H, Schobert B, Lanyi JK, Spudich EN, Spudich JL (2001) Crystal structure of sensory rhodopsin II at 2.4 Ångströms: Insights into color tuning and transducer interaction. Science 293:1499-1503.
18. Royant A, et al. (2001) X-ray structure of sensory rhodopsin II at 2.1-Å resolution. Proc Natl Acad Sci USA 98:10131-10136.
19. Vogeley L, et al. (2004) Anabaena sensory rhodopsin: A photochromic color sensor at 2.0 Å. Science 306:1390-1393.
20. Kralj JM, et al. (2008) Protonation state of Glu-142 differs in the green- and blue-absorbing variants of proteorhodopsin. Biochemistry 47:3447-3453.
21. Takaichi S, Mochimaru M (2007) Carotenoids and carotenogenesis in cyanobacteria: Unique ketocarotenoids and carotenoid glycosides. Cell Mol Life Sci 64:2607-2619.
22. Yoshimura K, Kouyama T (2008) Structural role of bacterioruberin in the trimeric structure of archaerhodopsin-2. J Mol Biol 375:1267-1281.
23. Boichenko VA, Wang JM, Antón J, Lanyi JK, Balashov SP (2006) Functions of carotenoids in xanthorhodopsin and archaerhodopsin, from action spectra of photoinhibition of cell respiration. Biochim Biophys Acta 1757:1649-1656.
24. Georgakopoulou S, Cogdell RJ, van Grondelle R, van Amerongen H (2003) Linear-dichroism measurements on the LH2 antenna complex of Rhodopseudomonas acidophila strain 10050 show that the transition dipole moment of the carotenoid rhodopsin glucoside is not collinear with the long molecular axis. J Phys Chem B 107:655-658.
25. Green BR, Parson WW, eds (2003) Light-Harvesting Antennas in Photosynthesis (Kluwer, Dordrecht).
26. Polivka T, Sundström V (2004) Ultrafast dynamics of carotenoid excited states: From solution to natural and artificial systems. Chem Rev 104:2021-2071.
27. Spudich JL, Jung K-H (2005) Handbook of Photosensory Receptors, eds Briggs WR, Spudich JL (Wiley, Darmstadt), pp 1-23.
28. Luecke H, Schobert B, Richter H-T, Cartailler J-P, Lanyi JK (1999) Structure of bacteriorhodopsin at 1.55-Å resolution. J Mol Biol 291:899-911.
29. Belrhali H, et al. (1999) Protein, lipid, and water organization in bacteriorhodopsin crystals: A molecular view of the purple membrane at 1.9-Å resolution. Structure 7:909-917.
30. Luecke H, Schobert B, Richter H-T, Cartailler J-P, Lanyi JK (1999) Structural changes in bacteriorhodopsin during ion transport at 2-Å resolution. Science 286:255-260.
31. Garczarek F, Gerwert K (2006) Functional waters in intraprotein proton transfer monitored by FTIR difference spectroscopy. Nature 439:109-112.
32. Dioumaev AK, et al. (2002) Proton transfers in the photochemical reaction cycle of proteorhodopsin. Biochemistry 41:5348-5358.
33. Imasheva ES, Balashov SP, Wang JM, Dioumaev AK, Lanyi JK (2004) Selectivity of retinal photoisomerization in proteorhodopsin is controlled by aspartic acid-227. Biochemistry 43:1648-1655.
34. Dioumaev AK, Wang JM, Balint Z, Váró G, Lanyi JK (2003) Proton transport by proteorhodopsin requires that the retinal Schiff base counterion Asp-97 be anionic. Biochemistry 42:6582-6587.
35. Cleland WW, Frey PA, Gerlt JA (1998) The low-barrier hydrogen bond in enzymatic catalysis. J Biol Chem 273:25529-25532.
36. Rangarajan R, Galan JF, Whited G, Birge RR (2007) Mechanism of spectral tuning in green-absorbing proteorhodopsin. Biochemistry 46:12679-12686.
37. Man-Aharonovich D, et al. (2004) Characterization of RS29, a blue-green proteorhodopsin variant from the Red Sea. Photochem Photobiol Sci 3:459-462.
38. Balashov SP, et al. (1997) Glutamate-194 to cysteine mutation inhibits fast light-induced proton release in bacteriorhodopsin. Biochemistry 36:8671-8676.
39. Brown LS, et al. (1995) Glutamic acid-204 is the terminal proton release group at the extracellular surface of bacteriorhodopsin. J Biol Chem 270:27122-27126.
40. Balashov SP, Imasheva ES, Govindjee R, Ebrey TG (1996) Titration of aspartate-85 in bacteriorhodopsin: What it says about chromophore isomerization and proton release. Biophys J 70:473-481.
41. Schobert B, Brown LS, Lanyi JK (2003) Crystallographic structures of the M and N intermediates of bacteriorhodopsin: Assembly of a hydrogen-bonded chain of water molecules between Asp-96 and the retinal Schiff base. J Mol Biol 330:553-570.
42. McCoy AJ, Grosse-Kunstleve RW, Storoni LC, Read RJ (2005) Likelihood-enhanced fast translation functions. Acta Crystallogr D 61:458-464.
43. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D 53:240-255.
44. Cowtan KD, Zhang KYJ (1999) Density modification for macromolecular phase improvement. Prog Biophys Mol Biol 72:245-270.
45. Emsley P, Cowtan K (2004) COOT: Model-building tools for molecular graphics. Acta Crystallogr D 60:2126-2132.
46. Brünger AT, et al. (1998) Crystallography and NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D 54:905-921.