Advertisement

Proton-Pumping Microbial Rhodopsins – Ubiquitous Structurally Simple Helpers of Respiration and Photosynthesis

  • Leonid S. BrownEmail author
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 39)

Summary

For almost four decades, bacteriorhodopsin has served as a classic example of the simplest standalone proton gradient generator. Bacteriorhodopsin-based bioenergetics was viewed as the most basic type of photosynthesis, becoming useful under limiting oxygen conditions only in a small group of extremophilic haloarchaea. With the advent of genomic and metagenomic high-throughput sequencing, the taxonomic and ecological diversity of bacteriorhodopsin-related proteins (microbial rhodopsins) appeared to be large. In this chapter, we survey structural and taxonomic diversity of proton-pumping microbial rhodopsins, describing haloarchaeal, fungal, algal, and eubacterial representatives, including those in photosynthetic organisms. Comparison of both primary and 3-D structures is made, and common structural trends are pointed out. Finally, we outline the main structural blocks involved in light-driven proton-transport mechanism, and discuss its conserved and variable parts.

Keywords

Schiff Base Proton Donor Proton Transport Cytoplasmic Side Extracellular Side 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations:

ACR-2

Acetabularia rhodopsin-2;

AR

– Archaerhodopsin;

BR

– Bacteriorhodopsin;

GPR

– Green-absorbing proteorhodopsin;

GR

Gloeobacter rhodopsin;

PR

– Proteorhodopsin;

RD

– Rhodopsin;

TM

– Transmembrane;

XR

– Xanthorhodopsin

Notes

Acknowledgements

This work is supported by Natural Sciences and Engineering Research Council of Canada and the University of Guelph.

References

  1. Adamian L, Ouyang Z, Tseng YY, Liang J (2006) Evolutionary patterns of retinal-binding pockets of type I rhodopsins and their functions. Photochem Photobiol 82:1426–1435PubMedGoogle Scholar
  2. Andersson M, Malmerberg E, Westenhoff S, Katona G, Cammarata M, Wohri AB, Johansson LC, Ewald F, Eklund M, Wulff M, Davidsson J, Neutze R (2009) Structural dynamics of light-driven proton pumps. Structure 17:1265–1275PubMedGoogle Scholar
  3. Atamna-Ismaeel N, Sabehi G, Sharon I, Witzel KP, Labrenz M, Jurgens K, Barkay T, Stomp M, Huisman J, Beja O (2008) Widespread distribution of proteorhodopsins in freshwater and brackish ecosystems. ISME J 2:656–662PubMedGoogle Scholar
  4. Atamna-Ismaeel N, Finkel OM, Glaser F, Sharon I, Schneider R, Post AF, Spudich JL, von Mering C, Vorholt JA, Iluz D, Beja O and Belkin S (2011) Microbial rhodopsins on leaf surfaces of terrestrial plants. Environ Microbiol 14:40–46Google Scholar
  5. Balashov SP (2000) Protonation reactions and their coupling in bacteriorhodopsin. Biochim Biophys Acta 1460:75–94PubMedGoogle Scholar
  6. Balashov SP, Govindjee R, Imasheva ES, Misra S, Ebrey TG, Feng Y, Crouch RK, Menick DR (1995) The two pKa’s of aspartate-85 and control of thermal isomerization and proton release in the arginine-82 to lysine mutant of bacteriorhodopsin. Biochemistry 34:8820–8834PubMedGoogle Scholar
  7. Balashov SP, Imasheva ES, Ebrey TG, Chen N, Menick DR, Crouch RK (1997) Glutamate-194 to cysteine mutation inhibits fast light-induced proton release in bacteriorhodopsin. Biochemistry 36:8671–8676PubMedGoogle Scholar
  8. Balashov SP, Lu M, Imasheva ES, Govindjee R, Ebrey TG, Othersen B 3rd, Chen Y, Crouch RK, Menick DR (1999) The proton release group of bacteriorhodopsin controls the rate of the final step of its photocycle at low pH. Biochemistry 38:2026–2039PubMedGoogle Scholar
  9. Balashov SP, Imasheva ES, Boichenko VA, Anton J, Wang JM, Lanyi JK (2005) Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna. Science 309:2061–2064PubMedCentralPubMedGoogle Scholar
  10. Balashov SP, Imasheva ES, Choi AR, Jung KH, Liaaen-Jensen S, Lanyi JK (2010) Reconstitution of Gloeobacter rhodopsin with echinenone: role of the 4-keto group. Biochemistry 49:9792–9799PubMedCentralPubMedGoogle Scholar
  11. Baliga NS, Bonneau R, Facciotti MT, Pan M, Glusman G, Deutsch EW, Shannon P, Chiu Y, Weng RS, Gan RR, Hung P, Date SV, Marcotte E, Hood L, Ng WV (2004) Genome sequence of Haloarcula marismortui: a halophilic archaeon from the Dead Sea. Genome Res 14:2221–2234PubMedCentralPubMedGoogle Scholar
  12. Beja O, Aravind L, Koonin EV, Suzuki MT, Hadd A, Nguyen LP, Jovanovich S, Gates CM, Feldman RA, Spudich JL, Spudich EN, DeLong EF (2000) Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289:1902–1906PubMedGoogle Scholar
  13. Beja O, Spudich EN, Spudich JL, Leclerc M, DeLong EF (2001) Proteorhodopsin phototrophy in the ocean. Nature 411:786–789PubMedGoogle Scholar
  14. Bergo V, Amsden JJ, Spudich EN, Spudich JL, Rothschild KJ (2004) Structural changes in the photoactive site of proteorhodopsin during the primary photoreaction. Biochemistry 43:9075–9083PubMedGoogle Scholar
  15. Bergo VB, Sineshchekov OA, Kralj JM, Partha R, Spudich EN, Rothschild KJ, Spudich JL (2009) His-75 in proteorhodopsin, a novel component in light-driven proton translocation by primary pumps. J Biol Chem 284:2836–2843PubMedCentralPubMedGoogle Scholar
  16. Bieszke JA, Spudich EN, Scott KL, Borkovich KA, Spudich JL (1999) A eukaryotic protein, NOP-1, binds retinal to form an archaeal rhodopsin-like photochemically reactive pigment. Biochemistry 38:14138–14145PubMedGoogle Scholar
  17. Bolhuis H, Palm P, Wende A, Falb M, Rampp M, Rodriguez-Valera F, Pfeiffer F, Oesterhelt D (2006) The genome of the square archaeon Haloquadratum walsbyi: life at the limits of water activity. BMC Genom 7:169Google Scholar
  18. Boyden ES, Chow BY, Han X, Qian X, Klapoetke NC, Kwon AH (2011) Light-activated proton pumps, particular microbial rhodopsins, for use in adjusting cell pH or voltage, or in proton release. USA Patent US 2,011,016,568,1Google Scholar
  19. Brown LS (2004) Fungal rhodopsins and opsin-related proteins: eukaryotic homologues of bacteriorhodopsin with unknown functions. Photochem Photobiol Sci 3:555–565PubMedGoogle Scholar
  20. Brown LS, Jung KH (2006) Bacteriorhodopsin-like proteins of eubacteria and fungi: the extent of conservation of the haloarchaeal proton-pumping mechanism. Photochem Photobiol Sci 5:538–546PubMedGoogle Scholar
  21. Brown LS, Yamazaki Y, Maeda A, Sun L, Needleman R, Lanyi JK (1994) The proton transfers in the cytoplasmic domain of bacteriorhodopsin are facilitated by a cluster of interacting residues. J Mol Biol 239:401–414PubMedGoogle Scholar
  22. Brown LS, Sasaki J, Kandori H, Maeda A, Needleman R, Lanyi JK (1995) Glutamic-acid-204 is the terminal proton release group at the surface of bacteriorhodopsin. J Biol Chem 270:27122–27126PubMedGoogle Scholar
  23. Brown LS, Dioumaev AK, Needleman R, Lanyi JK (1998) Local-access model for proton transfer in bacteriorhodopsin. Biochemistry 37:3982–3993PubMedGoogle Scholar
  24. Brown LS, Needleman R, Lanyi JK (1999) Functional roles of aspartic acid residues at the cytoplasmic surface of bacteriorhodopsin. Biochemistry 38:6855–6861PubMedGoogle Scholar
  25. Brown LS, Dioumaev AK, Lanyi JK, Spudich EN, Spudich JL (2001) Photochemical reaction cycle and proton transfers in Neurospora rhodopsin. J Biol Chem 276:32495–32505PubMedGoogle Scholar
  26. Butt HJ, Fendler K, Bamberg E, Tittor J, Oesterhelt D (1989) Aspartic acids 96 and 85 play a central role in the function of bacteriorhodopsin as a proton pump. EMBO J 8:1657–1663PubMedCentralPubMedGoogle Scholar
  27. Checover S, Marantz Y, Nachliel E, Gutman M, Pfeiffer M, Tittor J, Oesterhelt D, Dencher NA (2001) Dynamics of the proton transfer reaction on the cytoplasmic surface of bacteriorhodopsin. Biochemistry 40:4281–4292PubMedGoogle Scholar
  28. Chow BY, Han X, Dobry AS, Qian X, Chuong AS, Li M, Henninger MA, Belfort GM, Lin Y, Monahan PE, Boyden ES (2010) High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463:98–102PubMedCentralPubMedGoogle Scholar
  29. Danon A, Stoeckenius W (1974) Photophosphorylation in Halobacterium halobium. Proc Natl Acad Sci U S A 71:1234–1238PubMedCentralPubMedGoogle Scholar
  30. Decoursey TE (2003) Voltage-gated proton channels and other proton transfer pathways. Physiol Rev 83:475–579PubMedGoogle Scholar
  31. DeLong EF, Beja O (2010) The light-driven proton pump proteorhodopsin enhances bacterial survival during tough times. PLoS Biol 8:e1000359PubMedCentralPubMedGoogle Scholar
  32. Desiderio RA, Laney SR, Letelier RM, Giovannoni SJ (2007) Using lasers to probe the transient light absorption by proteorhodopsin in marine bacterioplankton. Appl Opt 46:7329–7336PubMedGoogle Scholar
  33. Dioumaev AK, Brown LS, Needleman R, Lanyi JK (1999) Fourier transform infrared spectra of a late intermediate of the bacteriorhodopsin photocycle suggest transient protonation of Asp-212. Biochemistry 38:10070–10078PubMedGoogle Scholar
  34. Dioumaev AK, Brown LS, Shih J, Spudich EN, Spudich JL, Lanyi JK (2002) Proton transfers in the photochemical reaction cycle of proteorhodopsin. Biochemistry 41:5348–5358PubMedGoogle Scholar
  35. Dioumaev AK, Wang JM, Balint Z, Varo G, Lanyi JK (2003) Proton transport by proteorhodopsin requires that the retinal Schiff base counterion Asp-97 be anionic. Biochemistry 42:6582–6587PubMedGoogle Scholar
  36. Enami N, Yoshimura K, Murakami M, Okumura H, Ihara K, Kouyama T (2006) Crystal structures of archaerhodopsin-1 and -2: common structural motif in archaeal light-driven proton pumps. J Mol Biol 358:675–685PubMedGoogle Scholar
  37. Fan Y, Shi L, Brown LS (2007) Structural basis of diversification of fungal retinal proteins probed by site-directed mutagenesis of Leptosphaeria rhodopsin. FEBS Lett 581:2557–2561PubMedGoogle Scholar
  38. Fan Y, Solomon P, Oliver RP, Brown LS (2011) Photochemical characterization of a novel fungal rhodopsin from Phaeosphaeria nodorum. Biochim Biophys Acta 1807:1457–1466PubMedGoogle Scholar
  39. Feldbauer K, Zimmermann D, Pintschovius V, Spitz J, Bamann C, Bamberg E (2009) Channelrhodopsin-2 is a leaky proton pump. Proc Natl Acad Sci U S A 106:12317–12322PubMedCentralPubMedGoogle Scholar
  40. Freier E, Wolf S, Gerwert K (2011) Proton transfer via a transient linear water-molecule chain in a membrane protein. Proc Natl Acad Sci U S A 108:11435–11439PubMedCentralPubMedGoogle Scholar
  41. Friedrich T, Geibel S, Kalmbach R, Chizhov I, Ataka K, Heberle J, Engelhard M, Bamberg E (2002) Proteorhodopsin is a light-driven proton pump with variable vectoriality. J Mol Biol 321:821–838PubMedGoogle Scholar
  42. Frigaard NU, Martinez A, Mincer TJ, DeLong EF (2006) Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea. Nature 439:847–850PubMedGoogle Scholar
  43. Fu HY, Lin YC, Chang YN, Tseng H, Huang CC, Liu KC, Huang CS, Su CW, Weng RR, Lee YY, Ng WV, Yang CS (2010) A novel six-rhodopsin system in a single archaeon. J Bacteriol 192:5866–5873PubMedCentralPubMedGoogle Scholar
  44. Fuhrman JA, Schwalbach MS, Stingl U (2008) Proteorhodopsins: an array of physiological roles? Nat Rev Microbiol 6:488–494PubMedGoogle Scholar
  45. Furutani Y, Ikeda D, Shibata M, Kandori H (2006a) Strongly hydrogen-bonded water molecule is observed only in the alkaline form of proteorhodopsin. Chem Phys 324:705–708Google Scholar
  46. Furutani Y, Sumii M, Fan Y, Shi LC, Waschuk SA, Brown LS, Kandori H (2006b) Conformational coupling between the cytoplasmic carboxylic acid and the retinal in a fungal light-driven proton pump. Biochemistry 45:15349–15358PubMedGoogle Scholar
  47. Ganea C, Gergely C, Ludmann K, Varo G (1997) The role of water in the extracellular half channel of bacteriorhodopsin. Biophys J 73:2718–2725PubMedCentralPubMedGoogle Scholar
  48. Garczarek F, Gerwert K (2006) Functional waters in intraprotein proton transfer monitored by FTIR difference spectroscopy. Nature 439:109–112PubMedGoogle Scholar
  49. Gomez-Consarnau L, Akram N, Lindell K, Pedersen A, Neutze R, Milton DL, Gonzalez JM, Pinhassi J (2010) Proteorhodopsin phototrophy promotes survival of marine bacteria during starvation. PLoS Biol 8:e1000358PubMedCentralPubMedGoogle Scholar
  50. Gonzalez JM, Fernandez-Gomez B, Fernandez-Guerra A, Gomez-Consarnau L, Sanchez O, Coll-Llado M, Del Campo J, Escudero L, Rodriguez-Martinez R, Alonso-Saez L, Latasa M, Paulsen I, Nedashkovskaya O, Lekunberri I, Pinhassi J, Pedros-Alio C (2008) Genome analysis of the proteorhodopsin-containing marine bacterium Polaribacter sp. MED152 (Flavobacteria). Proc Natl Acad Sci U S A 105:8724–8729PubMedCentralPubMedGoogle Scholar
  51. Gourdon P, Alfredsson A, Pedersen A, Malmerberg E, Nyblom M, Widell M, Berntsson R, Pinhassi J, Braiman M, Hansson O, Bonander N, KarlssonG, Neutze R (2008) Optimized in vitro and in vivo expression of proteorhodopsin: a seven-transmembrane proton pump. Protein Expr Purif 58:103–113PubMedGoogle Scholar
  52. Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PDB viewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723PubMedGoogle Scholar
  53. Hashimoto K, Choi AR, Furutani Y, Jung KH, Kandori H (2010) Low-temperature FTIR study of Gloeobacter rhodopsin: presence of strongly hydrogen-bonded water and long-range structural protein perturbation upon retinal photoisomerization. Biochemistry 49:3343–3350PubMedGoogle Scholar
  54. Haupts U, Tittor J, Bamberg E, Oesterhelt D (1997) General concept for ion translocation by halobacterial retinal proteins: the isomerization/switch/transfer (IST) model. Biochemistry 36:2–7PubMedGoogle Scholar
  55. Haupts U, Tittor J, Oesterhelt D (1999) Closing in on bacteriorhodopsin: progress in understanding the molecule. Annu Rev Biophys Biomol Struct 28:367–399PubMedGoogle Scholar
  56. Hegemann P (2008) Algal sensory photoreceptors. Annu Rev Plant Biol 59:167–189PubMedGoogle Scholar
  57. Hempelmann F, Holper S, Verhoefen MK, Woerner AC, Kohler T, Fiedler SA, Pfleger N, Wachtveitl J, Glaubitz C (2011) His75-Asp97 cluster in green proteorhodopsin. J Am Chem Soc 133:4645–4654PubMedGoogle Scholar
  58. Herzfeld J, Lansing JC (2002) Magnetic resonance studies of the bacteriorhodopsin pump cycle. Annu Rev Biophys Biomol Struct 31:73–95PubMedGoogle Scholar
  59. Herzfeld J, Tounge B (2000) NMR probes of vectoriality in the proton-motive photocycle of bacteriorhodopsin: evidence for an ‘electrostatic steering’ mechanism. Biochim Biophys Acta 1460:95–105PubMedGoogle Scholar
  60. Hessling B, Herbst J, Rammelsberg R, Gerwert K (1997) Fourier transform infrared double-flash experiments resolve bacteriorhodopsin’s M1 to M2 transition. Biophys J 73:2071–2080PubMedCentralPubMedGoogle Scholar
  61. 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:e5769PubMedCentralPubMedGoogle Scholar
  62. 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 19:433–439PubMedCentralPubMedGoogle Scholar
  63. Idnurm A, Verma S, Corrochano LM (2010) A glimpse into the basis of vision in the kingdom Mycota. Fungal Genet Biol 47:881–892PubMedCentralPubMedGoogle Scholar
  64. Ihara K, Amemiya T, Miyashita Y, Mukohata Y (1994) Met-145 is a key residue in the dark adaptation of bacteriorhodopsin homologs. Biophys J 67:1187–1191PubMedCentralPubMedGoogle Scholar
  65. Ihara K, Umemura T, Katagiri I, Kitajima-Ihara T, Sugiyama Y, Kimura Y, Mukohata Y (1999) Evolution of the archaeal rhodopsins: evolution rate changes by gene duplication and functional differentiation. J Mol Biol 285:163–174PubMedGoogle Scholar
  66. Imasheva ES, Balashov SP, Wang JM, Lanyi JK (2006) pH-Dependent transitions in xanthorhodopsin. Photochem Photobiol 82:1406–1413PubMedCentralPubMedGoogle Scholar
  67. Imasheva ES, Balashov SP, Choi AR, Jung KH, Lanyi JK (2009) Reconstitution of Gloeobacter violaceus rhodopsin with a light-harvesting carotenoid antenna. Biochemistry 48:10948–10955PubMedCentralPubMedGoogle Scholar
  68. Johnson ET, Baron DB, Naranjo B, Bond DR, Schmidt-Dannert C, Gralnick JA (2010) Enhancement of survival and electricity production in an engineered bacterium by light-driven proton pumping. Appl Environ Microbiol 76:4123–4129PubMedCentralPubMedGoogle Scholar
  69. Jung KH, Trivedi VD, Spudich JL (2003) Demonstration of a sensory rhodopsin in eubacteria. Mol Microbiol 47:1513–1522PubMedGoogle Scholar
  70. Jung JY, Choi AR, Lee YK, Lee HK, Jung KH (2008) Spectroscopic and photochemical analysis of proteorhodopsin variants from the surface of the Arctic Ocean. FEBS Lett 582:1679–1684PubMedGoogle Scholar
  71. Kandori H (2000) Role of internal water molecules in bacteriorhodopsin. Biochim Biophys Acta 1460:177–191PubMedGoogle Scholar
  72. Kandori H (2004) Hydration switch model for the proton transfer in the Schiff base region of bacteriorhodopsin. Biochim Biophys Acta 1658:72–79PubMedGoogle Scholar
  73. Kandori H (2011) Protein–controlled ultrafast photoisomerization in rhodopsin and bacteriorhodopsin. In: Ramamurthy V, Inoue Y (eds) Supramolecular photochemistry: controlling photochemical processes. Wiley, Hoboken, pp 571–595Google Scholar
  74. Kataoka M, Kamikubo H (2000) Structures of photointermediates and their implications for the proton pump mechanism. Biochim Biophys Acta 1460:166–176PubMedGoogle Scholar
  75. Kawanabe A, Furutani Y, Jung KH, Kandori H (2009) Engineering an inward proton transport from a bacterial sensor rhodopsin. J Am Chem Soc 131:16439–16444PubMedGoogle Scholar
  76. Kikukawa T, Shimono K, Tamogami J, Miyauchi S, Kim SY, Kimura-Someya T, Shirouzu M, Jung KH, Yokoyama S, Kamo N (2011) Photochemistry of Acetabularia rhodopsin II from a marine plant, Acetabularia acetabulum. Biochemistry 50:8888–8898PubMedGoogle Scholar
  77. Kimura H, Young CR, Martinez A, Delong EF (2011) Light-induced transcriptional responses associated with proteorhodopsin-enhanced growth in a marine flavobacterium. ISME J 5:1641–1651Google Scholar
  78. Klare JP, Bordignon E, Engelhard M, Steinhoff HJ (2004) Sensory rhodopsin II and bacteriorhodopsin: light activated helix F movement. Photochem Photobiol Sci 3:543–547PubMedGoogle Scholar
  79. Klare JP, Chizhov I, Engelhard M (2008) Microbial rhodopsins: scaffolds for ion pumps, channels, and sensors. Results Probl Cell Differ 45:73–122PubMedGoogle Scholar
  80. Koh EY, Atamna-Ismaeel N, Martin A, Cowie RO, Beja O, Davy SK, Maas EW, Ryan KG (2010) Proteorhodopsin-bearing bacteria in Antarctic sea ice. Appl Environ Microbiol 76:5918–5925PubMedCentralPubMedGoogle Scholar
  81. Kouyama T, Murakami M (2010) Structural divergence and functional versatility of the rhodopsin superfamily. Photochem Photobiol Sci 9:1458–1465PubMedGoogle Scholar
  82. Kralj JM, Bergo VB, Amsden JJ, Spudich EN, Spudich JL, Rothschild KJ (2008) Protonation state of Glu142 differs in the green- and blue-absorbing variants of proteorhodopsin. Biochemistry 47:3447–3453PubMedGoogle Scholar
  83. Krebs MP, Khorana HG (1993) Mechanism of light-dependent proton translocation by bacteriorhodopsin. J Bacteriol 175:1555–1560PubMedCentralPubMedGoogle Scholar
  84. Lanyi JK (2004) Bacteriorhodopsin. Annu Rev Physiol 66:665–688PubMedGoogle Scholar
  85. Lanyi JK, Balashov SP (2011) Xanthorhodopsin. In: Ventosa A (ed) Halophiles and hypersaline environments. Springer, Dordrecht, pp 319–340Google Scholar
  86. Lanyi JK, Schobert B (2004) Local-global conformational coupling in a heptahelical membrane protein: transport mechanism from crystal structures of the nine states in the bacteriorhodopsin photocycle. Biochemistry 43:3–8PubMedGoogle Scholar
  87. Lanyi JK, Schobert B (2006) Propagating structural perturbation inside bacteriorhodopsin: crystal structures of the M state and the D96A and T46V mutants. Biochemistry 45:12003–12010PubMedCentralPubMedGoogle Scholar
  88. Lorenz-Fonfria VA, Kandori H (2009) Spectroscopic and kinetic evidence on how bacteriorhodopsin accomplishes vectorial proton transport under functional conditions. J Am Chem Soc 131:5891–5901PubMedGoogle Scholar
  89. Lorinczi E, Verhoefen MK, Wachtveitl J, Woerner AC, Glaubitz C, Engelhard M, Bamberg E, Friedrich T (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 393:320–341PubMedGoogle Scholar
  90. Luecke H, Schobert B, Richter HT, Cartailler JP, Lanyi JK (1999a) Structural changes in bacteriorhodopsin during ion transport at 2 Angstrom resolution. Science 286:255–260PubMedGoogle Scholar
  91. Luecke H, Schobert B, Richter HT, Cartailler JP, Lanyi JK (1999b) Structure of bacteriorhodopsin at 1.55 angstrom resolution. J Mol Biol 291:899–911PubMedGoogle Scholar
  92. Luecke H, Schobert B, Cartailler JP, Richter HT, Rosengarth A, Needleman R, Lanyi JK (2000) Coupling photoisomerization of retinal to directional transport in bacteriorhodopsin. J Mol Biol 300:1237–1255PubMedGoogle Scholar
  93. Luecke H, Schobert B, Stagno J, Imasheva ES, Wang JM, Balashov SP, Lanyi JK (2008) Crystallographic structure of xanthorhodopsin, the light-driven proton pump with a dual chromophore. Proc Natl Acad Sci U S A 105:16561–16565PubMedCentralPubMedGoogle Scholar
  94. Lukashev EP, Govindjee R, Kono M, Ebrey TG, Sugiyama Y, Mukohata Y (1994) pH dependence of the absorption spectra and photochemical transformations of the archaerhodopsins. Photochem Photobiol 60:69–75PubMedGoogle Scholar
  95. Maeda A, Gennis RB, Balashov SP, Ebrey TG (2005) Relocation of water molecules between the Schiff base and the Thr46-Asp96 region during light-driven unidirectional proton transport by bacteriorhodopsin: an FTIR study of the N intermediate. Biochemistry 44:5960–5968PubMedGoogle Scholar
  96. Man-Aharonovich D, Sabehi G, Sineshchekov OA, Spudich EN, Spudich JL, Beja O (2004) Characterization of RS29, a blue-green proteorhodopsin variant from the Red Sea. Photochem Photobiol Sci 3:459–462PubMedGoogle Scholar
  97. Martinez A, Bradley AS, Waldbauer JR, Summons RE, DeLong EF (2007) Proteorhodopsin photosystem gene expression enables photophosphorylation in a heterologous host. Proc Natl Acad Sci U S A 104:5590–5595PubMedCentralPubMedGoogle Scholar
  98. Martinez-Garcia M, Swan BK, Poulton NJ, Gomez ML, Masland D, Sieracki ME, Stepanauskas R (2012) High-throughput single-cell sequencing identifies photoheterotrophs and chemoautotrophs in freshwater bacterioplankton. ISME J 6:113–123PubMedCentralPubMedGoogle Scholar
  99. McCarren J, DeLong EF (2007) Proteorhodopsin photosystem gene clusters exhibit co-evolutionary trends and shared ancestry among diverse marine microbial phyla. Environ Microbiol 9:846–858PubMedGoogle Scholar
  100. Mills DA, Ferguson-Miller S (2003) Understanding the mechanism of proton movement linked to oxygen reduction in cytochrome c oxidase: lessons from other proteins. FEBS Lett 545:47–51PubMedGoogle Scholar
  101. Mimuro M, Tsuchiya T, Koyama K, Peschek GA (2011) Bioenergetics in a primordial cyanobacterium Gloeobacter violaceus PCC 7421. In: Peschek GA (ed) Bioenergetic processes of cyanobacteria. Springer, The Netherlands, pp 211–238Google Scholar
  102. Miranda MR, Choi AR, Shi L, Bezerra AG Jr, Jung KH, Brown LS (2009) The photocycle and proton translocation pathway in a cyanobacterial ion-pumping rhodopsin. Biophys J 96:1471–1481PubMedCentralPubMedGoogle Scholar
  103. Mongodin EF, Nelson KE, Daugherty S, Deboy RT, Wister J, Khouri H, Weidman J, Walsh DA, Papke RT, Sanchez Perez G, Sharma AK, Nesbo CL, MacLeod D, Bapteste E, Doolittle WF, Charlebois RL, Legault B, Rodriguez-Valera F (2005) The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proc Natl Acad Sci U S A 102:18147–18152PubMedCentralPubMedGoogle Scholar
  104. Mulkidjanian AY, Cherepanov DA, Heberle J, Junge W (2005) Proton transfer dynamics at membrane/water interface and mechanism of biological energy conversion. Biochemistry (Mosc) 70:251–256Google Scholar
  105. Neutze R, Pebay-Peyroula E, Edman K, Royant A, Navarro J, Landau EM (2002) Bacteriorhodopsin: a high-resolution structural view of vectorial proton transport. Biochim Biophys Acta 1565:144–167PubMedGoogle Scholar
  106. Oesterhelt D, Stoeckenius W (1973) Functions of a new photoreceptor membrane. Proc Natl Acad Sci U S A 70:2853–2857PubMedCentralPubMedGoogle Scholar
  107. Okamoto OK, Hastings JW (2003) Novel dinoflagellate clock-related genes identified through microarray analysis. J Phycol 39:519–526Google Scholar
  108. Oren A (1999) Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev 63:334–348PubMedCentralPubMedGoogle Scholar
  109. Ormos P (1991) Infrared spectroscopic demonstration of a conformational change in bacteriorhodopsin involved in proton pumping. Proc Natl Acad Sci U S A 88:473–477PubMedCentralPubMedGoogle Scholar
  110. Page RD (2002) Visualizing phylogenetic trees using TreeView. Current Protocols in Bioinformatics, Chapter 6: Unit 6.2Google Scholar
  111. Partha R, Krebs R, Caterino TL, Braiman MS (2005) Weakened coupling of conserved arginine to the proteorhodopsin chromophore and its counterion implies structural differences from bacteriorhodopsin. Biochim Biophys Acta 1708:6–12PubMedGoogle Scholar
  112. Petrovskaya LE, Lukashev EP, Chupin VV, Sychev SV, Lyukmanova EN, Kryukova EA, Ziganshin RH, Spirina EV, Rivkina EM, Khatypov RA, Erokhina LG, Gilichinsky DA, Shuvalov VA, Kirpichnikov MP (2010) Predicted bacteriorhodopsin from Exiguobacterium sibiricum is a functional proton pump. FEBS Lett 584:4193–4196PubMedGoogle Scholar
  113. Pfleger N, Worner AC, Yang J, Shastri S, Hellmich UA, Aslimovska L, Maier MS, Glaubitz C (2009) Solid-state NMR and functional studies on proteorhodopsin. Biochim Biophys Acta 1787:697–705PubMedGoogle Scholar
  114. Racker E, Stoeckenius W (1974) Reconstitution of purple membrane vesicles catalyzing light-driven proton uptake and adenosine triphosphate formation. J Biol Chem 249:662–663PubMedGoogle Scholar
  115. Raven JA (2009) Functional evolution of photochemical energy transformations in oxygen-producing organisms. Funct Plant Biol 36:505–515Google Scholar
  116. Reckel S, Gottstein D, Stehle J, Lohr F, Verhoefen MK, Takeda M, Silvers R, Kainosho M, Glaubitz C, Wachtveitl J, Bernhard F, Schwalbe H, Guntert P, Dotsch V (2011) Solution NMR structure of proteorhodopsin. Angew Chem Int Ed Engl 50:11942–11946PubMedGoogle Scholar
  117. Richter HT, Brown LS, Needleman R, Lanyi JK (1996) A linkage of the pK(a)’s of asp-85 and glu-204 forms part of the reprotonation switch of bacteriorhodopsin. Biochemistry 35:4054–4062PubMedGoogle Scholar
  118. Riesle J, Oesterhelt D, Dencher NA, Heberle J (1996) D38 is an essential part of the proton translocation pathway in bacteriorhodopsin. Biochemistry 35:6635–6643PubMedGoogle Scholar
  119. Rothschild KJ (1992) FTIR difference spectroscopy of bacteriorhodopsin: toward a molecular model. J Bioenerg Biomembr 24:147–167PubMedGoogle Scholar
  120. Rothschild KJ, He YW, Sonar S, Marti T, Khorana HG (1992) Vibrational spectroscopy of bacteriorhodopsin mutants. Evidence that Thr-46 and Thr-89 form part of a transient network of hydrogen bonds. J Biol Chem 267:1615–1622PubMedGoogle Scholar
  121. Ruiz-Gonzalez MX, Marin I (2004) New insights into the evolutionary history of type 1 rhodopsins. J Mol Evol 58:348–358PubMedGoogle Scholar
  122. Sabehi G, Loy A, Jung KH, Partha R, Spudich JL, Isaacson T, Hirschberg J, Wagner M, Beja O (2005) New insights into metabolic properties of marine bacteria encoding proteorhodopsins. PLoS Biol 3:1409–1417Google Scholar
  123. Sasaki J, Spudich JL (2000) Proton transport by sensory rhodopsins and its modulation by transducer-binding. Biochim Biophys Acta 1460:230–239PubMedGoogle Scholar
  124. Schafer G, Engelhard M, Muller V (1999) Bioenergetics of the archaea. Microbiol Mol Biol Rev 63:570–620PubMedCentralPubMedGoogle Scholar
  125. Schobert B, Brown LS, Lanyi JK (2003) Crystallographic intermediates of structures of the M and N bacteriorhodopsin: assembly of a hydrogen-bonded chain of water molecules between Asp-96 and the retinal Schiff base. J Mol Biol 330:553–570PubMedGoogle Scholar
  126. Sharma AK, Spudich JL, Doolittle WF (2006) Microbial rhodopsins: functional versatility and genetic mobility. Trends Microbiol 14:463–469PubMedGoogle Scholar
  127. Sharma AK, Walsh DA, Bapteste E, Rodriguez-Valera F, Ford Doolittle W, Papke RT (2007) Evolution of rhodopsin ion pumps in haloarchaea. BMC Evol Biol 7:79PubMedCentralPubMedGoogle Scholar
  128. Sharma AK, Zhaxybayeva O, Papke RT, Doolittle WF (2008) Actinorhodopsins: proteorhodopsin-like gene sequences found predominantly in non-marine environments. Environ Microbiol 10:1039–1056PubMedGoogle Scholar
  129. Sharma AK, Sommerfeld K, Bullerjahn GS, Matteson AR, Wilhelm SW, Jezbera J, Brandt U, Doolittle WF, Hahn MW (2009) Actinorhodopsin genes discovered in diverse freshwater habitats and among cultivated freshwater Actinobacteria. ISME J 3:726–737PubMedGoogle Scholar
  130. Shi L, Lake EM, Ahmed MA, Brown LS, Ladizhansky V (2009a) Solid-state NMR study of proteorhodopsin in the lipid environment: secondary structure and dynamics. Biochim Biophys Acta 1788:2563–2574PubMedGoogle Scholar
  131. Shi L, Ahmed MA, Zhang W, Whited G, Brown LS, Ladizhansky V (2009b) Three-dimensional solid-state NMR study of a seven-helical integral membrane proton pump–structural insights. J Mol Biol 386:1078–1093PubMedGoogle Scholar
  132. Shibata M, Tanimoto T, Kandori H (2003) Water molecules in the Schiff base region of bacteriorhodopsin. J Am Chem Soc 125:13312–13313PubMedGoogle Scholar
  133. Shimono K, Hayashi T, Ikeura Y, Sudo Y, Iwamoto M, Kamo N (2003) Importance of the broad regional interaction for spectral tuning in Natronobacterium pharaonis phoborhodopsin (sensory rhodopsin II). J Biol Chem 278:23882–23889PubMedGoogle Scholar
  134. Sineshchekov OA, Spudich JL (2004) Light-induced intramolecular charge movements in microbial rhodopsins in intact E. coli cells. Photochem Photobiol Sci 3:548–554PubMedGoogle Scholar
  135. Sineshchekov OA, Govorunova EG, Jung KH, Zauner S, Maier UG, Spudich JL (2005) Rhodopsin-mediated photoreception in cryptophyte flagellates. Biophys J 89:4310–4319PubMedCentralPubMedGoogle Scholar
  136. Slamovits CH, Okamoto N, Burri L, James ER, Keeling PJ (2011) A bacterial proteorhodopsin proton pump in marine eukaryotes. Nat Commun 2:183PubMedGoogle Scholar
  137. Spudich JL (2006) The multitalented microbial sensory rhodopsins. Trends Microbiol 14:480–487PubMedGoogle Scholar
  138. Spudich JL, Yang CS, Jung KH, Spudich EN (2000) Retinylidene proteins: structures and functions from archaea to humans. Annu Rev Cell Dev Biol 16:365–392PubMedGoogle Scholar
  139. Steindler L, Schwalbach MS, Smith DP, Chan F, Giovannoni SJ (2011) Energy starved candidatus pelagibacter ubique substitutes light-mediated ATP production for endogenous carbon respiration. PLoS One 6:e19725PubMedCentralPubMedGoogle Scholar
  140. Stingl U, Desiderio RA, Cho JC, Vergin KL, Giovannoni SJ (2007) The SAR92 clade: an abundant coastal clade of culturable marine bacteria possessing proteorhodopsin. Appl Environ Microbiol 73:2290–2296PubMedCentralPubMedGoogle Scholar
  141. Subramaniam S, Henderson R (2000) Molecular mechanism of vectorial proton translocation by bacteriorhodopsin. Nature 406:653–657PubMedGoogle Scholar
  142. Subramaniam S, Lindahl I, Bullough P, Faruqi AR, Tittor J, Oesterhelt D, Brown L, Lanyi J, Henderson R (1999) Protein conformational changes in the bacteriorhodopsin photocycle. J Mol Biol 287:145–161PubMedGoogle Scholar
  143. Subramaniam S, Hirai T, Henderson R (2002) From structure to mechanism: electron crystallographic studies of bacteriorhodopsin. Philos Trans A Math Phys Eng Sci 360:859–874PubMedGoogle Scholar
  144. Sudo Y, Ihara K, Kobayashi S, Suzuki D, Irieda H, Kikukawa T, Kandori H, Homma M (2011) A microbial rhodopsin with a unique retinal composition shows both sensory rhodopsin II and bacteriorhodopsin-like properties. J Biol Chem 286:5967–5976PubMedCentralPubMedGoogle Scholar
  145. Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Current Protocols in Bioinformatics, Chapter 2: Unit 2 3Google Scholar
  146. Tsunoda SP, Ewers D, Gazzarrini S, Moroni A, Gradmann D, Hegemann P (2006) H+-pumping rhodopsin from the marine alga Acetabularia. Biophys J 91:1471–1479PubMedCentralPubMedGoogle Scholar
  147. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu D, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers YH, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74PubMedGoogle Scholar
  148. Wada T, Shimono K, Kikukawa T, Hato M, Shinya N, Kim SY, Kimura-Someya T, Shirouzu M, Tamogami J, Miyauchi S, Jung KH, Kamo N, Yokoyama S (2011) Crystal structure of the eukaryotic light-driven proton-pumping rhodopsin, Acetabularia rhodopsin II, from marine alga. J Mol Biol 411:986–998PubMedGoogle Scholar
  149. Walter JM, Greenfield D, Bustamante C, Liphardt J (2007) Light-powering Escherichia coli with proteorhodopsin. Proc Natl Acad Sci U S A 104:2408–2412PubMedCentralPubMedGoogle Scholar
  150. 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 102:6879–6883PubMedCentralPubMedGoogle Scholar
  151. Wikstrom M (1998) Proton translocation by bacteriorhodopsin and heme-copper oxidases. Curr Opin Struct Biol 8:480–488PubMedGoogle Scholar
  152. Xiao YW, Hutson MS, Belenky M, Herzfeld J, Braiman MS (2004) Role of arginine-82 in fast proton release during the bacteriorhodopsin photocycle: a time-resolved FT-IR study of purple membranes containing N-15-labeled arginine. Biochemistry 43:12809–12818PubMedGoogle Scholar
  153. Yoshimura K, Kouyama T (2008) Structural role of bacterioruberin in the trimeric structure of archaerhodopsin-2. J Mol Biol 375:1267–1281PubMedGoogle Scholar
  154. Zhang F, Vierock J, Yizhar O, Fenno LE, Tsunoda S, Kianianmomeni A, Prigge M, Berndt A, Cushman J, Polle J, Magnuson J, Hegemann P, Deisseroth K (2011) The microbial opsin family of optogenetic tools. Cell 147:1446–1457PubMedGoogle Scholar
  155. Zubkov MV (2009) Photoheterotrophy in marine prokaryotes. J Plankton Res 31:933–938Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2014

Authors and Affiliations

  1. 1.Department of PhysicsUniversity of GuelphGuelphCanada

Personalised recommendations