Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 Mar 28;92(7):3036–3040. doi: 10.1073/pnas.92.7.3036

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.

R Seidel 1, B Scharf 1, M Gautel 1, K Kleine 1, D Oesterhelt 1, M Engelhard 1
PMCID: PMC42354  PMID: 7708770

Abstract

The blue-light receptor genes (sopII) of sensory rhodopsin (SR) II were cloned from two species, the halophilic bacteria Haloarcula vallismortis (vSR-II) and Natronobacterium pharaonis (pSR-II). Upstream of both sopII gene loci, sequences corresponding to the halobacterial transducer of rhodopsin (Htr) II were recognized. In N. pharaonis, psopII and phtrII are transcribed as a single transcript. Comparison of the amino acid sequences of vHtr-II and pHtr-II with Htr-I and the chemotactic methyl-accepting proteins from Escherichia coli revealed considerable identities in the signal domain and methyl-accepting sites. Similarities with Htr-I in Halobacterium salinarium suggest a common principle in the phototaxis of extreme halophiles. Alignment of all known retinal protein sequences from Archaea identifies both SR-IIs as an additional subgroup of the family. Positions defining the retinal binding site are usually identical with the exception of Met-118 (numbering is according to the bacteriorhodopsin sequence), which might explain the typical blue color shift of SR-II to approximately 490 nm. In archaeal retinal proteins, the function can be deduced from amino acids in positions 85 and 96. Proton pumps are characterized by Asp-85 and Asp-96; chloride pumps by Thr-85 and Ala-96; and sensors by Asp-85 and Tyr-96 or Phe-96.

Full text

PDF
3036

Images in this article

3039Fig. 2
on p.3039
3040Fig. 3
on p.3040

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bivin D. B., Stoeckenius W. Photoactive retinal pigments in haloalkaliphilic bacteria. J Gen Microbiol. 1986 Aug;132(8):2167–2177. doi: 10.1099/00221287-132-8-2167. [DOI] [PubMed] [Google Scholar]
  2. Blanck A., Oesterhelt D., Ferrando E., Schegk E. S., Lottspeich F. Primary structure of sensory rhodopsin I, a prokaryotic photoreceptor. EMBO J. 1989 Dec 20;8(13):3963–3971. doi: 10.1002/j.1460-2075.1989.tb08579.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Charlebois R. L., Hofman J. D., Schalkwyk L. C., Lam W. L., Doolittle W. F. Genome mapping in halobacteria. Can J Microbiol. 1989 Jan;35(1):21–29. doi: 10.1139/m89-004. [DOI] [PubMed] [Google Scholar]
  4. Chomczynski P., Qasba P. K. Alkaline transfer of DNA to plastic membrane. Biochem Biophys Res Commun. 1984 Jul 18;122(1):340–344. doi: 10.1016/0006-291x(84)90480-7. [DOI] [PubMed] [Google Scholar]
  5. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  6. Ferrando-May E., Krah M., Marwan W., Oesterhelt D. The methyl-accepting transducer protein HtrI is functionally associated with the photoreceptor sensory rhodopsin I in the archaeon Halobacterium salinarium. EMBO J. 1993 Aug;12(8):2999–3005. doi: 10.1002/j.1460-2075.1993.tb05968.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Greenhalgh D. A., Farrens D. L., Subramaniam S., Khorana H. G. Hydrophobic amino acids in the retinal-binding pocket of bacteriorhodopsin. J Biol Chem. 1993 Sep 25;268(27):20305–20311. [PubMed] [Google Scholar]
  8. Henderson R., Baldwin J. M., Ceska T. A., Zemlin F., Beckmann E., Downing K. H. Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J Mol Biol. 1990 Jun 20;213(4):899–929. doi: 10.1016/S0022-2836(05)80271-2. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Hu J., Griffin R. G., Herzfeld J. Synergy in the spectral tuning of retinal pigments: complete accounting of the opsin shift in bacteriorhodopsin. Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):8880–8884. doi: 10.1073/pnas.91.19.8880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Imamoto Y., Shichida Y., Yoshizawa T., Tomioka H., Takahashi T., Fujikawa K., Kamo N., Kobatake Y. Photoreaction cycle of phoborhodopsin studied by low-temperature spectrophotometry. Biochemistry. 1991 Jul 30;30(30):7416–7424. doi: 10.1021/bi00244a008. [DOI] [PubMed] [Google Scholar]
  12. Krah M., Marwan W., Verméglio A., Oesterhelt D. Phototaxis of Halobacterium salinarium requires a signalling complex of sensory rhodopsin I and its methyl-accepting transducer HtrI. EMBO J. 1994 May 1;13(9):2150–2155. doi: 10.1002/j.1460-2075.1994.tb06491.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Langridge J., Langridge P., Bergquist P. L. Extraction of nucleic acids from agarose gels. Anal Biochem. 1980 Apr;103(2):264–271. doi: 10.1016/0003-2697(80)90266-3. [DOI] [PubMed] [Google Scholar]
  14. Marwan W., Schäfer W., Oesterhelt D. Signal transduction in Halobacterium depends on fumarate. EMBO J. 1990 Feb;9(2):355–362. doi: 10.1002/j.1460-2075.1990.tb08118.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Rath P., Olson K. D., Spudich J. L., Rothschild K. J. The Schiff base counterion of bacteriorhodopsin is protonated in sensory rhodopsin I: spectroscopic and functional characterization of the mutated proteins D76N and D76A. Biochemistry. 1994 May 10;33(18):5600–5606. doi: 10.1021/bi00184a032. [DOI] [PubMed] [Google Scholar]
  17. Reiter W. D., Hüdepohl U., Zillig W. Mutational analysis of an archaebacterial promoter: essential role of a TATA box for transcription efficiency and start-site selection in vitro. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9509–9513. doi: 10.1073/pnas.87.24.9509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rice M. S., Dahlquist F. W. Sites of deamidation and methylation in Tsr, a bacterial chemotaxis sensory transducer. J Biol Chem. 1991 May 25;266(15):9746–9753. [PubMed] [Google Scholar]
  19. Rowlands T., Baumann P., Jackson S. P. The TATA-binding protein: a general transcription factor in eukaryotes and archaebacteria. Science. 1994 May 27;264(5163):1326–1329. doi: 10.1126/science.8191287. [DOI] [PubMed] [Google Scholar]
  20. Scharf B., Engelhard M. Blue halorhodopsin from Natronobacterium pharaonis: wavelength regulation by anions. Biochemistry. 1994 May 31;33(21):6387–6393. doi: 10.1021/bi00187a002. [DOI] [PubMed] [Google Scholar]
  21. Scharf B., Engelhard M. Halocyanin, an archaebacterial blue copper protein (type I) from Natronobacterium pharaonis. Biochemistry. 1993 Nov 30;32(47):12894–12900. doi: 10.1021/bi00210a043. [DOI] [PubMed] [Google Scholar]
  22. Scharf B., Hess B., Engelhard M. Chromophore of sensory rhodopsin II from Halobacterium halobium. Biochemistry. 1992 Dec 15;31(49):12486–12492. doi: 10.1021/bi00164a027. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Scharf B., Wolff E. K. Phototactic behaviour of the archaebacterial Natronobacterium pharaonis. FEBS Lett. 1994 Feb 28;340(1-2):114–116. doi: 10.1016/0014-5793(94)80183-5. [DOI] [PubMed] [Google Scholar]
  25. Schimz A. Methylation of membrane proteins is involved in chemosensory and photosensory behavior of Halobacterium halobium. FEBS Lett. 1981 Mar 23;125(2):205–207. doi: 10.1016/0014-5793(81)80719-3. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Spudich E. N., Takahashi T., Spudich J. L. Sensory rhodopsins I and II modulate a methylation/demethylation system in Halobacterium halobium phototaxis. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7746–7750. doi: 10.1073/pnas.86.20.7746. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Spudich J. L. Color sensing in the Archaea: a eukaryotic-like receptor coupled to a prokaryotic transducer. J Bacteriol. 1993 Dec;175(24):7755–7761. doi: 10.1128/jb.175.24.7755-7761.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Tittor J., Soell C., Oesterhelt D., Butt H. J., Bamberg E. A defective proton pump, point-mutated bacteriorhodopsin Asp96----Asn is fully reactivated by azide. EMBO J. 1989 Nov;8(11):3477–3482. doi: 10.1002/j.1460-2075.1989.tb08512.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Yan B., Takahashi T., Johnson R., Spudich J. L. Identification of signaling states of a sensory receptor by modulation of lifetimes of stimulus-induced conformations: the case of sensory rhodopsin II. Biochemistry. 1991 Nov 5;30(44):10686–10692. doi: 10.1021/bi00108a012. [DOI] [PubMed] [Google Scholar]
  32. Yao V. J., Spudich J. L. Primary structure of an archaebacterial transducer, a methyl-accepting protein associated with sensory rhodopsin I. Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11915–11919. doi: 10.1073/pnas.89.24.11915. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES