Abstract
Phoborhodopsin (pR; also sensory rhodopsin II, sRII) is a retinoid protein in Halobacterium salinarum and works as a receptor of negative phototaxis. Pharaonis phoborhodopsin (ppR; also pharaonis sensory rhodopsin II, psRII) is a corresponding protein of Natronobacterium pharaonis. In bacterial membrane, ppR forms a complex with its transducer pHtrII, and this complex transmits the light signal to the sensory system in the cytoplasm. We expressed pHtrII-free ppR or ppR-pHtrII complex in H. salinarum Pho81/wr(-) cells. Flash-photolysis experiments showed no essential changes between pHtrII-free ppR and the complex. Using SnO2 electrode, which works as a sensitive pH electrode, and envelope membrane vesicles, we showed the photo-induced outward proton transport. This membranous proton transport was also shown using membrane vesicles from Escherichia coli in which ppR was functionally expressed. On the other hand, the proton transport was ceased when ppR formed a complex with pHtrII. Using membrane sheet, it was shown that the complex undergoes first proton uptake and then release during the photocycle, the same as pHtrII-free ppR, although the net proton transport ceases. Taking into consideration that the complex of sRII (pR) and its transducer undergoes extracellular proton circulation (J. Sasaki and J. L., Biophys. J. 77:2145-2152), we inferred that association with pHtrII closes a cytoplasmic channel of ppR, which lead to the extracellular proton circulation.
Full Text
The Full Text of this article is available as a PDF (85.7 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Blaseio U., Pfeifer F. Transformation of Halobacterium halobium: development of vectors and investigation of gas vesicle synthesis. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6772–6776. doi: 10.1073/pnas.87.17.6772. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bogomolni R. A., Spudich J. L. Identification of a third rhodopsin-like pigment in phototactic Halobacterium halobium. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6250–6254. doi: 10.1073/pnas.79.20.6250. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bogomolni R. A., Stoeckenius W., Szundi I., Perozo E., Olson K. D., Spudich J. L. Removal of transducer HtrI allows electrogenic proton translocation by sensory rhodopsin I. Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):10188–10192. doi: 10.1073/pnas.91.21.10188. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chizhov I., Schmies G., Seidel R., Sydor J. R., Lüttenberg B., Engelhard M. The photophobic receptor from Natronobacterium pharaonis: temperature and pH dependencies of the photocycle of sensory rhodopsin II. Biophys J. 1998 Aug;75(2):999–1009. doi: 10.1016/S0006-3495(98)77588-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Haupts U., Bamberg E., Oesterhelt D. Different modes of proton translocation by sensory rhodopsin I. EMBO J. 1996 Apr 15;15(8):1834–1841. [PMC free article] [PubMed] [Google Scholar]
- Haupts U., Tittor J., Oesterhelt D. Closing in on bacteriorhodopsin: progress in understanding the molecule. Annu Rev Biophys Biomol Struct. 1999;28:367–399. doi: 10.1146/annurev.biophys.28.1.367. [DOI] [PubMed] [Google Scholar]
- Hirayama J., Imamoto Y., Shichida Y., Kamo N., Tomioka H., Yoshizawa T. Photocycle of phoborhodopsin from haloalkaliphilic bacterium (Natronobacterium pharaonis) studied by low-temperature spectrophotometry. Biochemistry. 1992 Feb 25;31(7):2093–2098. doi: 10.1021/bi00122a029. [DOI] [PubMed] [Google Scholar]
- Hoff W. D., Jung K. H., Spudich J. L. Molecular mechanism of photosignaling by archaeal sensory rhodopsins. Annu Rev Biophys Biomol Struct. 1997;26:223–258. doi: 10.1146/annurev.biophys.26.1.223. [DOI] [PubMed] [Google Scholar]
- Iwamoto M., Shimono K., Sumi M., Kamo N. Positioning proton-donating residues to the Schiff-base accelerates the M-decay of pharaonis phoborhodopsin expressed in Escherichia coli. Biophys Chem. 1999 Jun 28;79(3):187–192. doi: 10.1016/s0301-4622(99)00054-x. [DOI] [PubMed] [Google Scholar]
- Lanyi J. K. Halorhodopsin, a light-driven electrogenic chloride-transport system. Physiol Rev. 1990 Apr;70(2):319–330. doi: 10.1152/physrev.1990.70.2.319. [DOI] [PubMed] [Google Scholar]
- Lanyi J. K., MacDonald R. E. Light-induced transport in Halobacterium halobium. Methods Enzymol. 1979;56:398–407. doi: 10.1016/0076-6879(79)56038-8. [DOI] [PubMed] [Google Scholar]
- Lanyi J. K. Mechanism of ion transport across membranes. Bacteriorhodopsin as a prototype for proton pumps. J Biol Chem. 1997 Dec 12;272(50):31209–31212. doi: 10.1074/jbc.272.50.31209. [DOI] [PubMed] [Google Scholar]
- Lüttenberg B., Wolff E. K., Engelhard M. Heterologous coexpression of the blue light receptor psRII and its transducer pHtrII from Natronobacterium pharaonis in the Halobacterium salinarium strain Pho81/w restores negative phototaxis. FEBS Lett. 1998 Apr 10;426(1):117–120. doi: 10.1016/s0014-5793(98)00322-6. [DOI] [PubMed] [Google Scholar]
- 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 Sep 9;78(1):237–243. doi: 10.1016/0006-291x(77)91245-1. [DOI] [PubMed] [Google Scholar]
- Olson K. D., Spudich J. L. Removal of the transducer protein from sensory rhodopsin I exposes sites of proton release and uptake during the receptor photocycle. Biophys J. 1993 Dec;65(6):2578–2585. doi: 10.1016/S0006-3495(93)81295-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Perazzona B., Spudich E. N., Spudich J. L. Deletion mapping of the sites on the HtrI transducer for sensory rhodopsin I interaction. J Bacteriol. 1996 Nov;178(22):6475–6478. doi: 10.1128/jb.178.22.6475-6478.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Robertson B., Lukashev E. P. Rapid pH change due to bacteriorhodopsin measured with a tin-oxide electrode. Biophys J. 1995 Apr;68(4):1507–1517. doi: 10.1016/S0006-3495(95)80323-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rosen B. P., Tsuchiya T. Preparation of everted membrane vesicles from Escherichia coli for the measurement of calcium transport. Methods Enzymol. 1979;56:233–241. doi: 10.1016/0076-6879(79)56026-1. [DOI] [PubMed] [Google Scholar]
- Sasaki J., Spudich J. L. Proton circulation during the photocycle of sensory rhodopsin II. Biophys J. 1999 Oct;77(4):2145–2152. doi: 10.1016/S0006-3495(99)77055-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sasaki J., Spudich J. L. Proton transport by sensory rhodopsins and its modulation by transducer-binding. Biochim Biophys Acta. 2000 Aug 30;1460(1):230–239. doi: 10.1016/s0005-2728(00)00142-0. [DOI] [PubMed] [Google Scholar]
- Sasaki J., Spudich J. L. The transducer protein HtrII modulates the lifetimes of sensory rhodopsin II photointermediates. Biophys J. 1998 Nov;75(5):2435–2440. doi: 10.1016/S0006-3495(98)77687-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scharf B., Pevec B., Hess B., Engelhard M. Biochemical and photochemical properties of the photophobic receptors from Halobacterium halobium and Natronobacterium pharaonis. Eur J Biochem. 1992 Jun 1;206(2):359–366. doi: 10.1111/j.1432-1033.1992.tb16935.x. [DOI] [PubMed] [Google Scholar]
- Schmies G., Lüttenberg B., Chizhov I., Engelhard M., Becker A., Bamberg E. Sensory rhodopsin II from the haloalkaliphilic natronobacterium pharaonis: light-activated proton transfer reactions. Biophys J. 2000 Feb;78(2):967–976. doi: 10.1016/S0006-3495(00)76654-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Seidel R., Scharf B., Gautel M., Kleine K., Oesterhelt D., Engelhard M. The primary structure of sensory rhodopsin II: a member of an additional retinal protein subgroup is coexpressed with its transducer, the halobacterial transducer of rhodopsin II. Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):3036–3040. doi: 10.1073/pnas.92.7.3036. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shimono K., Iwamoto M., Sumi M., Kamo N. Functional expression of pharaonis phoborhodopsin in Escherichia coli. FEBS Lett. 1997 Dec 22;420(1):54–56. doi: 10.1016/s0014-5793(97)01487-7. [DOI] [PubMed] [Google Scholar]
- Spudich E. N., Spudich J. L. The photochemical reactions of sensory rhodopsin I are altered by its transducer. J Biol Chem. 1993 Aug 5;268(22):16095–16097. [PubMed] [Google Scholar]
- Spudich J. L. Variations on a molecular switch: transport and sensory signalling by archaeal rhodopsins. Mol Microbiol. 1998 Jun;28(6):1051–1058. doi: 10.1046/j.1365-2958.1998.00859.x. [DOI] [PubMed] [Google Scholar]
- Takahashi T., Yan B., Mazur P., Derguini F., Nakanishi K., Spudich J. L. Color regulation in the archaebacterial phototaxis receptor phoborhodopsin (sensory rhodopsin II). Biochemistry. 1990 Sep 11;29(36):8467–8474. doi: 10.1021/bi00488a038. [DOI] [PubMed] [Google Scholar]
- Takao K., Kikukawa T., Araiso T., Kamo N. Azide accelerates the decay of M-intermediate of pharaonis phoborhodopsin. Biophys Chem. 1998 Jul 13;73(1-2):145–153. doi: 10.1016/s0301-4622(98)00156-2. [DOI] [PubMed] [Google Scholar]
- Tsuda M., Hazemoto N., Kondo M., Kamo N., Kobatake Y., Terayama Y. Two photocycles in halobacterium halobium that lacks bacteriorhodopsin. Biochem Biophys Res Commun. 1982 Oct 15;108(3):970–976. doi: 10.1016/0006-291x(82)92094-0. [DOI] [PubMed] [Google Scholar]
- Wegener A. A., Chizhov I., Engelhard M., Steinhoff H. J. Time-resolved detection of transient movement of helix F in spin-labelled pharaonis sensory rhodopsin II. J Mol Biol. 2000 Aug 25;301(4):881–891. doi: 10.1006/jmbi.2000.4008. [DOI] [PubMed] [Google Scholar]
- Yan B., Cline S. W., Doolittle W. F., Spudich J. L. Transformation of a bop-hop-sop-I-sop-II-Halobacterium halobium mutant to bop+: effects of bacteriorhodopsin photoactivation on cellular proton fluxes and swimming behavior. Photochem Photobiol. 1992 Oct;56(4):553–561. doi: 10.1111/j.1751-1097.1992.tb02200.x. [DOI] [PubMed] [Google Scholar]
- Zhang W., Brooun A., Mueller M. M., Alam M. The primary structures of the Archaeon Halobacterium salinarium blue light receptor sensory rhodopsin II and its transducer, a methyl-accepting protein. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8230–8235. doi: 10.1073/pnas.93.16.8230. [DOI] [PMC free article] [PubMed] [Google Scholar]