Biochemistry (Moscow)

, Volume 81, Issue 4, pp 414–419 | Cite as

Na+-translocating rhodopsin from Dokdonia sp. PRO95 does not contain carotenoid antenna

  • Y. V. Bertsova
  • A. M. Arutyunyan
  • A. V. BogachevEmail author


Carotenoid-binding properties of Na+-translocating rhodopsin (NaR) from Dokdonia sp. PRO95 were studied. Carotenoids were extracted from Dokdonia sp. PRO95 cells. It was found that zeaxanthin is the predominant carotenoid of this bacterium. Incubation of recombinant NaR purified from Escherichia coli cells with carotenoids from Dokdonia sp. PRO95 did not result in any changes in optical absorption or circular dichroism spectra, indicating the absence of binding of the carotenoids by NaR. The same results were obtained using salinixanthin as the carotenoid. These data along with genome analysis of Dokdonia sp. PRO95 and other flavobacteria indicate that NaR from Dokdonia sp. PRO95 and possibly the other flavobacterial Na+-translocating rhodopsins do not contain a carotenoid antenna.


Na+-translocating rhodopsin xanthorhodopsin carotenoid antenna zeaxanthin salinixanthin flavobacteria 



circular dichroism


n-dodecyl β-D-maltoside


Na+-translocating rhodopsin


thin-layer chromatography

Δ\({\bar \mu _{{H^ + }}}\)

transmembrane differences in H+ electrochemical potentials


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Skulachev, V. P., Bogachev, A. V., and Kasparinsky, F. O. (2013) Principles of Bioenergetics, Springer.CrossRefGoogle Scholar
  2. 2.
    Croce, R., and Van Amerongen, H. (2014) Natural strategies for photosynthetic light harvesting, Nat. Chem. Biol., 10, 492–501.CrossRefPubMedGoogle Scholar
  3. 3.
    Balashov, S. P., Imasheva, E. S., Boichenko, V. A., Anton, J., Wang, J. M., and Lanyi, J. K. (2005) Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna, Science, 309, 2061–2064.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Boichenko, V. A., Wang, J. M., Anton, J., Lanyi, J. K., and Balashov, S. P. (2006) Functions of carotenoids in xanthorhodopsin and archaerhodopsin, from action spectra of photoinhibition of cell respiration, Biochim. Biophys. Acta, 1757, 1649–1656.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Lutnaes, B. F., Oren, A., and Liaaen-Jensen, S. (2002) New C40-carotenoid acyl glycoside as principal carotenoid in Salinibacter ruber, an extremely halophilic eubacterium, J. Nat. Prod., 65, 1340–1343.CrossRefPubMedGoogle Scholar
  6. 6.
    Luecke, H., Schobert, B., Stagno, J., Imasheva, E. S., Wang, J. M., Balashov, S. P., and Lanyi, J. K. (2008) Crystallographic structure of xanthorhodopsin, the lightdriven proton pump with a dual chromophore, Proc. Natl. Acad. Sci. USA, 105, 16561–16565.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Balashov, S. P., Imasheva, E. S., and Lanyi, J. K. (2006) Induced chirality of the light-harvesting carotenoid salinixanthin and its interaction with the retinal of xanthorhodopsin, Biochemistry, 45, 10998–11004.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Imasheva, E. S., Balashov, S. P., Wang, J. M., and Lanyi, J. K. (2011) Removal and reconstitution of the carotenoid antenna of xanthorhodopsin, J. Membr. Biol., 239, 95–104.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Balashov, S. P., Imasheva, E. S., Choi, A. R., Jung, K. H., Liaaen-Jensen, S., and Lanyi, J. K. (2010) Reconstitution of gloeobacter rhodopsin with echinenone: role of the 4keto group, Biochemistry, 49, 9792–9799.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Imasheva, E. S., Balashov, S. P., Choi, A. R., Jung, K. H., and Lanyi, J. K. (2009) Reconstitution of Gloeobacter violaceus rhodopsin with a light-harvesting carotenoid antenna, Biochemistry, 48, 10948–10955.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Grote, M., Engelhard, M., and Hegemann, P. (2014) Of ion pumps, sensors and channels–perspectives on microbial rhodopsins between science and history, Biochim. Biophys. Acta, 1837, 533–545.CrossRefPubMedGoogle Scholar
  12. 12.
    Inoue, K., Ono, H., Abe-Yoshizumi, R., Yoshizawa, S., Ito, H., Kogure, K., and Kandori, H. (2013) A light-driven sodium ion pump in marine bacteria, Nat. Commun., 4, 1678.CrossRefPubMedGoogle Scholar
  13. 13.
    Gushchin, I., Shevchenko, V., Polovinkin, V., Kovalev, K., Alekseev, A., Round, E., Borshchevskiy, V., Balandin, T., Popov, A., Gensch, T., Fahlke, C., Bamann, C., Willbold, D., Buldt, G., Bamberg, E., and Gordeliy, V. (2015) Crystal structure of a light-driven sodium pump, Nat. Struct. Mol. Biol., 22, 390–395.PubMedGoogle Scholar
  14. 14.
    Kato, H. E., Inoue, K., Abe-Yoshizumi, R., Kato, Y., Ono, H., Konno, M., Hososhima, S., Ishizuka, T., Hoque, M. R., Kunitomo, H., Ito, J., Yoshizawa, S., Yamashita, K., Takemoto, M., Nishizawa, T., Taniguchi, R., Kogure, K., Maturana, A. D., Iino, Y., Yawo, H., Ishitani, R., Kandori, H., and Nureki, O. (2015) Structural basis for Na+ transport mechanism by a light-driven Na+ pump, Nature, 521, 48–53.CrossRefPubMedGoogle Scholar
  15. 15.
    Bertsova, Y. V., Bogachev A. V., and Skulachev, V. P. (2015) Proteorhodopsin from Dokdonia sp. PRO95 is a light-driven Na+-pump, Biochemistry (Moscow), 80, 449–454.CrossRefGoogle Scholar
  16. 16.
    Riedel, T., Gomez-Consarnau, L., Tomasch, J., Martin, M., Jarek, M., Gonzalez, J. M., Spring, S., Rohlfs, M., Brinkhoff, T., Cypionka, H., Goker, M., Fiebig, A., Klein, J., Goesmann, A., Fuhrman, J. A., and Wagner-Dobler, I. (2013) Genomics and physiology of a marine flavobacterium encoding a proteorhodopsin and a xanthorhodopsinlike protein, PLoS One, 8, e57487.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Anton, J., Oren, A., Benlloch, S., Rodriguez-Valera, F., Amann, R., and Rossello-Mora, R. (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.CrossRefPubMedGoogle Scholar
  18. 18.
    Sommerburg, O., Keunen, J. E. E., Bird, A. C., and Van Kuijk, F. J. G. M. (1998) Fruits and vegetables that are sources for lutein and zeaxanthin: the macular pigment in human eyes, Br. J. Ophthalmol., 82, 907–910.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Imasheva, E. S., Balashov, S. P., Wang, J. M., Smolensky, E., Sheves, M., and Lanyi, J. K. (2008) Chromophore interaction in xanthorhodopsin: retinal dependence of salinixanthin binding, Photochem. Photobiol., 84, 977–984.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Zang, L. Y., Sommerburg, O., and Van Kuijk, F. J. (1997) Absorbance changes of carotenoids in different solvents, Free Radic. Biol. Med., 23, 1086–1089.CrossRefPubMedGoogle Scholar
  21. 21.
    Shindo, K., Kikuta, K., Suzuki, A., Katsuta, A., Kasai, H., Yasumoto-Hirose, M., Matsuo, Y., Misawa, N., and Takaichi, S. (2007) Rare carotenoids, (3R)-saproxanthin and (3R,2′S)-myxol, isolated from novel marine bacteria (Flavobacteriaceae) and their antioxidative activities, Appl. Microbiol. Biotechnol., 74, 1350–1357.CrossRefPubMedGoogle Scholar
  22. 22.
    Britton, G., Brown, D. J., Goodwin, T. W., Leuenberger, F. J., and Schocher, A. J. (1977) The carotenoids of Flavobacterium strain R1560, Arch. Microbiol., 113, 33–37.CrossRefPubMedGoogle Scholar
  23. 23.
    Takatani, N., Nakanishi, M., Meirelles, P., Mino, S., Suda, W., Oshima, K., Hattori, M., Ohkuma, M., Hosokawa, M., Miyashita, K., Thompson, F. L., Niwa, A., and Sawabe, T. (2014) Draft genome sequences of marine flavobacterium Algibacter lectus strains SS8 and NR4, Genome Announc., 2, e01168–14, doi: 10.1128/genomeA.01168-14.PubMedPubMedCentralGoogle Scholar
  24. 24.
    Prabhu, S., Rekha, P. D., and Arun, A. B. (2014) Zeaxanthin biosynthesis by members of the genus Muricauda, Pol. J. Microbiol., 63, 115–119.PubMedGoogle Scholar
  25. 25.
    Sieiro, C., Poza, M., De Miguel, T., and Villa, T. G. (2003) Genetic basis of microbial carotenogenesis, Int. Microbiol., 6, 11–16.PubMedGoogle Scholar
  26. 26.
    Gruszecki, W. I., Zelent, B., and Leblanc, R. M. (1990) Fluorescence of zeaxanthin and violaxanthin in aggregated forms, Chem. Phys. Lett., 171, 563–568.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2016

Authors and Affiliations

  • Y. V. Bertsova
    • 1
  • A. M. Arutyunyan
    • 1
  • A. V. Bogachev
    • 1
    Email author
  1. 1.Belozersky Institute of Physico-Chemical BiologyLomonosov Moscow State UniversityMoscowRussia

Personalised recommendations