Biochemistry (Moscow)

, Volume 83, Supplement 1, pp S163–S175 | Cite as

Investigations of Photosensitive Proteins by Serial Crystallography

  • G. K. Selikhanov
  • M. S. Fando
  • M. V. Dontsova
  • A. G. GabdulkhakovEmail author


This review contains recent data on serial femtosecond X-ray crystallography (SFX), based on a femtosecond X-ray free electron laser, as well as on the possibilities of its application for studying photosensitive proteins. Development of this method began rather recently, and it has already shown its effectiveness and some unique advantages over conventional X-ray structural analysis. This technology is especially promising for structural studies of membrane proteins and for kinetic studies. The main principle of the method, the possibility of its application in structural biology, its advantages and disadvantages, as well as its prospects for further development are analyzed in this review. Special attention is given to publications in which the SFX method has been used to study photosensitive proteins.


X-ray free electron laser serial crystallography photosensitive proteins 



lipid cubic phase


lipid sponge phase


photosystem I(II)


photoactive yellow protein


reaction center


serial femtosecond X-ray analysis


X-ray free-electron laser


X-ray diffraction analysis


  1. 1.
    Skarzynski, T., Mistry, A., Wonacott, A., Hutchinson, S. E., Kelly, V. A., and Duncan, K. (1996) Structure of UDP-N-acetylglucosamine enolpyruvyl transferase, an enzyme essential for the synthesis of bacterial peptidoglycan, complexed with substrate UDP-N-acetylglucosamine and the drug fosfomycin, Structure, 4, 1465–1474.PubMedGoogle Scholar
  2. 2.
    Liu, J., Tse, A. G. D., Chang, H.-C., Liu, J.-H., Wang, J., Hussey, R. E., Chishti, Y., Rheinhold, B., Spoerl, R., Nathenson, S. G., Sacchettini, J. C., and Reinherz, E. L. (1996) Crystallization of a deglycosylated T cell receptor (TCR) complexed with an anti-TCR Fab fragment, J. Biol. Chem., 271, 33639–33646.CrossRefPubMedGoogle Scholar
  3. 3.
    Wikoff, W. R., Tsai, C. J., Wang, G., Baker, T. S., and Johnson, J. E. (1997) The structure of cucumber mosaic virus: cryoelectron microscopy, X-ray crystallography, and sequence analysis, Virology, 232, 91–97.PubMedGoogle Scholar
  4. 4.
    Wenzel, S., Martins, B. M., Rosch, P., and Wohrl, B. M. (2010) Crystal structure of the human transcription elongation factor DSIF hSpt4 subunit in complex with the hSpt5 dimerization interface, Biochem. J., 425, 373–380.CrossRefGoogle Scholar
  5. 5.
    Hamiaux, C., Stanley, D., Greenwood, D. R., Baker, E. N., and Newcomb, R. D. (2009) Crystal structure of Epiphyas postvittana takeout 1 with bound ubiquinone supports a role as ligand carriers for takeout proteins in insects, J. Biol. Chem., 284, 3496–3503.CrossRefPubMedGoogle Scholar
  6. 6.
    Gabdulkhakov, A. G., Dontsova, M. V., and Saenger, W. (2011) Three-dimensional structure of photosystem II from Thermosynechococcus elongates in complex with terbutryn, Crystallogr. Rep., 56, 1054–1059.CrossRefGoogle Scholar
  7. 7.
    Gabadinho, J., Beteva, A., Guijarro, M., Rey-Bakaikoa, V., Spruce, D., Bowler, M. W., Brockhauser, S., Flot, D., Gordon, E. J., Hall, D. R., Lavault, B., McCarthy, A. A., McCarthy, J., Mitchell, E., Monaco, S., Mueller-Dieckmann, C., Nurizzo, D., Ravelli, R. B. G., Thibault, X., Walsh, M. A., Leonard, G. A., and McSweeney, S. M. (2010) MxCuBE: a synchrotron beamline control environment customized for macromolecular crystallography experiments, J. Synchrotron Radiat., 17, 700–707.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Huang, Z., and Kim, K.-J. (2007) Review of X-ray free-electron laser theory, Phys. Rev. Spec. Top. Accel. Beams, 10, 034801–034826.CrossRefGoogle Scholar
  9. 9.
    Margaritondo, G., and Rebernik Ribic, P. (2011) A simplified description of X-ray free-electron lasers, J. Synchrotron Radiat., 18, 101–108.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Struder, L., Epp, S., Rolles, D., Hartmann, R., Holl, P., Lutz, G., Soltau, H., Eckart, R., Reich, C., Heinzinger, K., Thamm, C., Rudenko, A., Krasniqi, F., Kuhnel, K.-U., Bauer, C., Schroter, C.-D., Moshammer, R., Techert, S., Miessner, D., Porro, M., Halker, O., Meidinger, N., Kimmel, N., Andritschke, R., Schopper, F., Weidenspointner, G., Ziegler, A., Pietschner, D., Herrmann, S., Pietsch, U., Walenta, A., Leitenberger, W., Bostedt, C., Moller, T., Rupp, D., Adolph, M., Graafsma, H., Hirsemann, H., Gartner, K., Richter, R., Foucar, L., Shoeman, R. L., Schlichting, I., and Ullrich, J. (2010) Large-format, high-speed, X-ray pnCCDs combined with electron and ion imaging spectrometers in a multipurpose chamber for experiments at 4th generation light sources, Nucl. Instrum. Methods Phys. Res. Sect. Accel. Spectrometers Detect. Assoc. Equip., 614, 483–496.CrossRefGoogle Scholar
  11. 11.
    Carroll, D. (2011) Overview of high energy lasers: past, present, and future, in 42nd AIAA Plasmadynamics and Lasers Conf. in conjunction with the 18th Int. Conf. on MHD Energy Conversion (ICMHD), p. 3102.Google Scholar
  12. 12.
    European XFEL–Overview–In comparison (https:// Scholar
  13. 13.
    Massover, W. H. (2007) Radiation damage to protein specimens from electron beam imaging and diffraction: a minireview of antidamage approaches, with special reference to synchrotron X-ray crystallography, J. Synchrotron Radiat., 14, 116–127.PubMedGoogle Scholar
  14. 14.
    Smyth, M. S. (2000) X-ray crystallography, Mol. Pathol., 53, 8–14.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Holton, J. M., and Frankel, K. A. (2010) The minimum crystal size needed for a complete diffraction data set, Acta Crystallogr. D Biol. Crystallogr., 66, 393–408.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Neutze, R., Wouts, R., Van der Spoel, D., Weckert, E., and Hajdu, J. (2000) Potential for biomolecular imaging with femtosecond X-ray pulses, Nature, 406, 752–757.CrossRefPubMedGoogle Scholar
  17. 17.
    Chapman, H. N., Barty, A., Bogan, M. J., Boutet, S., Frank, M., Hau-Riege, S. P., Marchesini, S., Woods, B. W., Bajt, S., Benner, W. H., London, R. A., Plonjes, E., Kuhlmann, M., Treusch, R., Dusterer, S., Tschentscher, T., Schneider, J. R., Spiller, E., Moller, T., Bostedt, C., Hoener, M., Shapiro, D. A., Hodgson, K. O., Van der Spoel, D., Burmeister, F., Bergh, M., Caleman, C., Huldt, G., Seibert, M. M., Maia, F. R. N. C., Lee, R. W., Szoke, A., Timneanu, N., and Hajdu, J. (2006) Femtosecond diffractive imaging with a soft-X-ray free-electron laser, Nat. Phys., 2, 839–843.CrossRefGoogle Scholar
  18. 18.
    Chapman, H. N., Hau-Riege, S. P., Bogan, M. J., Bajt, S., Barty, A., Boutet, S., Marchesini, S., Frank, M., Woods, B. W., Benner, W. H., London, R. A., Rohner, U., Szoke, A., Spiller, E., Moller, T., Bostedt, C., Shapiro, D. A., Kuhlmann, M., Treusch, R., Plonjes, E., Burmeister, F., Bergh, M., Caleman, C., Huldt, G., Seibert, M. M., and Hajdu, J. (2007) Femtosecond time-delay X-ray holography, Nature, 448, 676–679.CrossRefPubMedGoogle Scholar
  19. 19.
    Weierstall, U., Spence, J. C. H., and Doak, R. B. (2012) Injector for scattering measurements on fully solvated biospecies, Rev. Sci. Instrum., 83, 035108–035120.CrossRefPubMedGoogle Scholar
  20. 20.
    Deponte, D. P., Mckeown, J. T., Weierstall, U., Doak, R. B., and Spence, J. C. H. (2011) Towards ETEM serial crystallography: electron diffraction from liquid jets, Ultramicroscopy, 111, 824–827.CrossRefPubMedGoogle Scholar
  21. 21.
    Liu, W., Wacker, D., Wang, C., Abola, E., and Cherezov, V. (2014) Femtosecond crystallography of membrane proteins in the lipidic cubic phase, Philos. Trans. R. Soc. B Biol. Sci., 369, 20130314–20130324.CrossRefGoogle Scholar
  22. 22.
    Landau, E. M., and Rosenbusch, J. P. (1996) Lipidic cubic phases: a novel concept for the crystallization of membrane proteins, Proc. Natl. Acad. Sci. USA, 93, 14532–14535.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Wadsten, P., Wohri, A. B., Snijder, A., Katona, G., Gardiner, A. T., Cogdell, R. J., Neutze, R., and Engstrom, S. (2006) Lipidic sponge phase crystallization of membrane proteins, J. Mol. Biol., 364, 44–53.CrossRefPubMedGoogle Scholar
  24. 24.
    Johansson, L. C., Arnlund, D., White, T. A., Katona, G., DePonte, D. P., Weierstall, U., Doak, R. B., Shoeman, R. L., Lomb, L., Malmerberg, E., Davidsson, J., Nass, K., Liang, M., Andreasson, J., Aquila, A., Bajt, S., Barthelmess, M., Barty, A., Bogan, M. J., Bostedt, C., Bozek, J. D., Caleman, C., Coffee, R., Coppola, N., Ekeberg, T., Epp, S. W., Erk, B., Fleckenstein, H., Foucar, L., Graafsma, H., Gumprecht, L., Hajdu, J., Hampton, C. Y., Hartmann, R., Hartmann, A., Hauser, G., Hirsemann, H., Holl, P., Hunter, M. S., Kassemeyer, S., Kimmel, N., Kirian, R. A., Maia, F. R. N. C., Marchesini, S., Martin, A. V., Reich, C., Rolles, D., Rudek, B., Rudenko, A., Schlichting, I., Schulz, J., Seibert, M. M., Sierra, R. G., Soltau, H., Starodub, D., Stellato, F., Stern, S., Struder, L., Timneanu, N., Ullrich, J., Wahlgren, W. Y., Wang, X., Weidenspointner, G., Wunderer, C., Fromme, P., Chapman, H. N., Spence, J. C. H., and Neutze, R. (2012) Lipidic phase membrane protein serial femtosecond crystallography, Nat. Methods, 9, 263–265.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Beerlink, A., Wilbrandt, P.-J., Ziegler, E., Carbone, D., Metzger, T. H., and Salditt, T. (2008) X-ray structure analysis of free-standing lipid membranes facilitated by micromachined apertures, Langmuir, 24, 4952–4958.CrossRefPubMedGoogle Scholar
  26. 26.
    Chapman, H. N., Fromme, P., Barty, A., White, T. A., Kirian, R. A., Aquila, A., Hunter, M. S., Schulz, J., DePonte, D. P., Weierstall, U., Doak, R. B., Maia, F. R. N. C., Martin, A. V., Schlichting, I., Lomb, L., Coppola, N., Shoeman, R. L., Epp, S. W., Hartmann, R., Rolles, D., Rudenko, A., Foucar, L., Kimmel, N., Weidenspointner, G., Holl, P., Liang, M., Barthelmess, M., Caleman, C., Boutet, S., Bogan, M. J., Krzywinski, J., Bostedt, C., Bajt, S., Gumprecht, L., Rudek, B., Erk, B., Schmidt, C., Homke, A., Reich, C., Pietschner, D., Struder, L., Hauser, G., Gorke, H., Ullrich, J., Herrmann, S., Schaller, G., Schopper, F., Soltau, H., Kuhnel, K.-U., Messerschmidt, M., Bozek, J. D., Hau-Riege, S. P., Frank, M., Hampton, C. Y., Sierra, R. G., Starodub, D., Williams, G. J., Hajdu, J., Timneanu, N., Seibert, M. M., Andreasson, J., Rocker, A., Jonsson, O., Svenda, M., Stern, S., Nass, K., Andritschke, R., Schroter, C.-D., Krasniqi, F., Bott, M., Schmidt, K. E., Wang, X., Grotjohann, I., Holton, J. M., Barends, T. R. M., Neutze, R., Marchesini, S., Fromme, R., Schorb, S., Rupp, D., Adolph, M., Gorkhover, T., Andersson, I., Hirsemann, H., Potdevin, G., Graafsma, H., Nilsson, B., and Spence, J. C. H. (2011) Femtosecond X-ray protein nanocrystallography, Nature, 470, 73–77.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Fraser, J. S., Van den Bedem, H., Samelson, A. J., Lang, P. T., Holton, J. M., Echols, N., and Alber, T. (2011) Accessing protein conformational ensembles using room-temperature X-ray crystallography, Proc. Natl. Acad. Sci. USA, 108, 16247–16252.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Bourgeois, D., Schotte, F., Brunori, M., and Vallone, B. (2007) Time-resolved methods in biophysics. 6. Time-resolved Laue crystallography as a tool to investigate photo-activated protein dynamics, Photochem. Photobiol. Sci., 6, 1047–1056.CrossRefPubMedGoogle Scholar
  29. 29.
    Stowell, M. H. (1997) Light-induced structural changes in photosynthetic reaction center: implications for mechanism of electron–proton transfer, Science, 276, 812–816.CrossRefPubMedGoogle Scholar
  30. 30.
    Ihee, H., Rajagopal, S., Srajer, V., Pahl, R., Anderson, S., Schmidt, M., Schotte, F., Anfinrud, P. A., Wulff, M., and Moffat, K. (2005) From the cover: visualizing reaction pathways in photoactive yellow protein from nanoseconds to seconds, Proc. Natl. Acad. Sci. USA, 102, 7145–7150.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Ren, Z., Perman, B., Srajer, V., Teng, T.-Y., Pradervand, C., Bourgeois, D., Schotte, F., Ursby, T., Kort, R., Wulff, M., and Moffat, K. (2001) A molecular movie at 1.8 Å resolution displays the photocycle of photoactive yellow protein, a eubacterial blue-light receptor, from nanoseconds to seconds, Biochemistry, 40, 13788–13801.PubMedGoogle Scholar
  32. 32.
    Baxter, R. H. G., Ponomarenko, N., Srajer, V., Pahl, R., Moffat, K., and Norris, J. R. (2004) Time-resolved crystallographic studies of light-induced structural changes in the photosynthetic reaction center, Proc. Natl. Acad. Sci. USA, 101, 5982–5987.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Moffat, K., Szebenyi, D., and Bilderback, D. (1984) X-ray Laue diffraction from protein crystals, Science, 223, 1423–1425.CrossRefPubMedGoogle Scholar
  34. 34.
    Schotte, F. (2003) Watching a protein as it functions with 150-ps time-resolved X-ray crystallography, Science, 300, 1944–1947.CrossRefPubMedGoogle Scholar
  35. 35.
    Barends, T. R. M., Foucar, L., Ardevol, A., Nass, K., Aquila, A., Botha, S., Doak, R. B., Falahati, K., Hartmann, E., Hilpert, M., Heinz, M., Hoffmann, M. C., Kofinger, J., Koglin, J. E., Kovacsova, G., Liang, M., Milathianaki, D., Lemke, H. T., Reinstein, J., Roome, C. M., Shoeman, R. L., Williams, G. J., Burghardt, I., Hummer, G., Boutet, S., and Schlichting, I. (2015) Direct observation of ultrafast collective motions in CO myoglobin upon ligand dissociation, Science, 350, 445–450.CrossRefPubMedGoogle Scholar
  36. 36.
    Panneels, V., Wu, W., Tsai, C.-J., Nogly, P., Rheinberger, J., Jaeger, K., Cicchetti, G., Gati, C., Kick, L. M., Sala, L., Capitani, G., Milne, C., Padeste, C., Pedrini, B., Li, X.-D., Standfuss, J., Abela, R., and Schertler, G. (2015) Time-resolved structural studies with serial crystallography: a new light on retinal proteins, Struct. Dyn., 2, 041718–041726.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Ginn, H. M., Messerschmidt, M., Ji, X., Zhang, H., Axford, D., Gildea, R. J., Winter, G., Brewster, A. S., Hattne, J., Wagner, A., Grimes, J. M., Evans, G., Sauter, N. K., Sutton, G., and Stuart, D. I. (2015) Structure of CPV17 polyhedrin determined by the improved analysis of serial femtosecond crystallographic data, Nat. Commun., 6, 6435–6443.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Cohen, A. E., Soltis, S. M., Gonzalez, A., Aguila, L., Alonso-Mori, R., Barnes, C. O., Baxter, E. L., Brehmer, W., Brewster, A. S., Brunger, A. T., Calero, G., Chang, J. F., Chollet, M., Ehrensberger, P., Eriksson, T. L., Feng, Y., Hattne, J., Hedman, B., Hollenbeck, M., Holton, J. M., Keable, S., Kobilka, B. K., Kovaleva, E. G., Kruse, A. C., Lemke, H. T., Lin, G., Lyubimov, A. Y., Manglik, A., Mathews, I. I., McPhillips, S. E., Nelson, S., Peters, J. W., Sauter, N. K., Smith, C. A., Song, J., Stevenson, H. P., Tsai, Y., Uervirojnangkoorn, M., Vinetsky, V., Wakatsuki, S., Weis, W. I., Zadvornyy, O. A., Zeldin, O. B., Zhu, D., and Hodgson, K. O. (2014) Goniometer-based femtosecond crystallography with X-ray free electron lasers, Proc. Natl. Acad. Sci. USA, 111, 17122–17127.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Lunin, V. Y., Grum-Grzhimailo, A. N., Gryzlova, E. V., Sinitsyn, D. O., Petrova, T. E., Lunina, N. L., Balabaev, N. K., Tereshkina, K. B., Stepanov, A. S., and Krupyanskii, Y. F. (2015) Efficient calculation of diffracted intensities in the case of nonstationary scattering by biological macromolecules under XFEL pulses, Acta Crystallogr. D Biol. Crystallogr., 71, 293–303.CrossRefPubMedGoogle Scholar
  40. 40.
    Pande, K., Hutchison, C. D. M., Groenhof, G., Aquila, A., Robinson, J. S., Tenboer, J., Basu, S., Boutet, S., DePonte, D. P., Liang, M., White, T. A., Zatsepin, N. A., Yefanov, O., Morozov, D., Oberthuer, D., Gati, C., Subramanian, G., James, D., Zhao, Y., Koralek, J., Brayshaw, J., Kupitz, C., Conrad, C., Roy-Chowdhury, S., Coe, J. D., Metz, M., Xavier, P. L., Grant, T. D., Koglin, J. E., Ketawala, G., Fromme, R., Rajer, V., Henning, R., Spence, J. C. H., Ourmazd, A., Schwander, P., Weierstall, U., Frank, M., Fromme, P., Barty, A., Chapman, H. N., Moffat, K., Van Thor, J. J., and Schmidt, M. (2016) Femtosecond structural dynamics drives the trans/cis isomerization in photoactive yellow protein, Science, 352, 725–729.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Blankenship, R. E. (2014) Molecular Mechanisms of Photosynthesis, Wiley/Blackwell, Chichester, West Sussex, p.296.Google Scholar
  42. 42.
    Nelson, N. (2009) Plant photosystem I–the most efficient nano-photochemical machine, J. Nanosci. Nanotechnol., 9, 1709–1713.CrossRefPubMedGoogle Scholar
  43. 43.
    Jordan, P., Fromme, P., Witt, H. T., Klukas, O., Saenger, W., and Krauβ, N. (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution, Nature, 411, 909–917.CrossRefPubMedGoogle Scholar
  44. 44.
    Aquila, A., Hunter, M. S., Doak, R. B., Kirian, R. A., Fromme, P., White, T. A., Andreasson, J., Arnlund, D., Bajt, S., Barends, T. R. M., Barthelmess, M., Bogan, M. J., Bostedt, C., Bottin, H., Bozek, J. D., Caleman, C., Coppola, N., Davidsson, J., DePonte, D. P., Elser, V., Epp, S. W., Erk, B., Fleckenstein, H., Foucar, L., Frank, M., Fromme, R., Graafsma, H., Grotjohann, I., Gumprecht, L., Hajdu, J., Hampton, C. Y., Hartmann, A., Hartmann, R., Hau-Riege, S., Hauser, G., Hirsemann, H., Holl, P., Holton, J. M., Homke, A., Johansson, L., Kimmel, N., Kassemeyer, S., Krasniqi, F., Kuhnel, K.-U., Liang, M., Lomb, L., Malmerberg, E., Marchesini, S., Martin, A. V., Maia, F. R. N. C., Messerschmidt, M., Nass, K., Reich, C., Neutze, R., Rolles, D., Rudek, B., Rudenko, A., Schlichting, I., Schmidt, C., Schmidt, K. E., Schulz, J., Seibert, M. M., Shoeman, R. L., Sierra, R., Soltau, H., Starodub, D., Stellato, F., Stern, S., Struder, L., Timneanu, N., Ullrich, J., Wang, X., Williams, G. J., Weidenspointner, G., Weierstall, U., Wunderer, C., Barty, A., Spence, J. C. H., and Chapman, H. N. (2012) Time-resolved protein nanocrystallography using an X-ray free-electron laser, Opt. Express, 20, 2706–2716.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Imamoto, Y., and Kataoka, M. (2007) Structure and photoreaction of photoactive yellow protein, a structural prototype of the PAS domain superfamily, Photochem. Photobiol., 83, 40–49.PubMedGoogle Scholar
  46. 46.
    Moffat, K. (1989) Time-resolved macromolecular crystallography, Annu. Rev. Biophys. Biophys. Chem., 18, 309–332.CrossRefPubMedGoogle Scholar
  47. 47.
    Tenboer, J., Basu, S., Zatsepin, N., Pande, K., Milathianaki, D., Frank, M., Hunter, M., Boutet, S., Williams, G. J., Koglin, J. E., Oberthuer, D., Heymann, M., Kupitz, C., Conrad, C., Coe, J., Roy-Chowdhury, S., Weierstall, U., James, D., Wang, D., Grant, T., Barty, A., Yefanov, O., Scales, J., Gati, C., Seuring, C., Srajer, V., Henning, R., Schwander, P., Fromme, R., Ourmazd, A., Moffat, K., Van Thor, J. J., Spence, J. C. H., Fromme, P., Chapman, H. N., and Schmidt, M. (2014) Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein, Science, 346, 1242–1246.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Deisenhofer, J., Epp, O., Miki, K., Huber, R., and Michel, H. (1985) Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3 Å resolution, Nature, 318, 618–624.CrossRefPubMedGoogle Scholar
  49. 49.
    Fromme, P., and Witt, H. T. (1998) Improved isolation and crystallization of photosystem I for structural analysis, Biochim. Biophys. Acta, 1365, 175–184.CrossRefGoogle Scholar
  50. 50.
    Johansson, L. C., Arnlund, D., Katona, G., White, T. A., Barty, A., DePonte, D. P., Shoeman, R. L., Wickstrand, C., Sharma, A., Williams, G. J., Aquila, A., Bogan, M. J., Caleman, C., Davidsson, J., Doak, R. B., Frank, M., Fromme, R., Galli, L., Grotjohann, I., Hunter, M. S., Kassemeyer, S., Kirian, R. A., Kupitz, C., Liang, M., Lomb, L., Malmerberg, E., Martin, A. V., Messerschmidt, M., Nass, K., Redecke, L., Seibert, M. M., Sjohamn, J., Steinbrener, J., Stellato, F., Wang, D., Wahlgren, W. Y., Weierstall, U., Westenhoff, S., Zatsepin, N. A., Boutet, S., Spence, J. C. H., Schlichting, I., Chapman, H. N., Fromme, P., and Neutze, R. (2013) Structure of a photosynthetic reaction center determined by serial femtosecond crystallography, Nat. Commun., 4, 2911–2917.PubMedPubMedCentralGoogle Scholar
  51. 51.
    Vinyard, D. J., Ananyev, G. M., and Charles Dismukes, G. (2013) Photosystem II: the reaction center of oxygenic photosynthesis, Annu. Rev. Biochem., 82, 577–606.CrossRefPubMedGoogle Scholar
  52. 52.
    Kok, B., Forbush, B., and McGloin, M. (1970) Cooperation of charges in photosynthetic O2 evolution. I. A linear four-step mechanism, Photochem. Photobiol., 11, 457–475.CrossRefPubMedGoogle Scholar
  53. 53.
    Zouni, A., Witt, H.-T., Kern, J., Fromme, P., Krauss, N., Saenger, W., and Orth, P. (2001) Crystal structure of photo-system II from Synechococcus elongatus at 3.8 Å resolution, Nature, 409, 739–743.CrossRefPubMedGoogle Scholar
  54. 54.
    Guskov, A., Kern, J., Gabdulkhakov, A., Broser, M., Zouni, A., and Saenger, W. (2009) Cyanobacterial photo-system II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride, Nat. Struct. Mol. Biol., 16, 334–342.CrossRefPubMedGoogle Scholar
  55. 55.
    Loll, B., Kern, J., Saenger, W., Zouni, A., and Biesiadka, J. (2005) Towards complete cofactor arrangement in the 3.0 Åresolution structure of photosystem II, Nature, 438, 1040–1044.CrossRefPubMedGoogle Scholar
  56. 56.
    Ferreira, K. N. (2004) Architecture of the photosynthetic oxygen-evolving center, Science, 303, 1831–1838.CrossRefPubMedGoogle Scholar
  57. 57.
    Biesiadka, J., Loll, B., Kern, J., Irrgang, K.-D., and Zouni, A. (2004) Crystal structure of cyanobacterial photosystem II at 3.2 Å resolution: a closer look at the Mncluster, Phys. Chem. Chem. Phys., 6, 4733–4736.CrossRefGoogle Scholar
  58. 58.
    Kamiya, N., and Shen, J.-R. (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution, Proc. Natl. Acad. Sci. USA, 100, 98–103.CrossRefPubMedGoogle Scholar
  59. 59.
    Umena, Y., Kawakami, K., Shen, J.-R., and Kamiya, N. (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å, Nature, 473, 55–60.CrossRefPubMedGoogle Scholar
  60. 60.
    Yano, J., Kern, J., Irrgang, K.-D., Latimer, M. J., Bergmann, U., Glatzel, P., Pushkar, Y., Biesiadka, J., Loll, B., Sauer, K., Messinger, J., Zouni, A., and Yachandra, V. K. (2005) X-ray damage to the Mn4Ca complex in single crystals of photosystem II: a case study for metalloprotein crystallography, Proc. Natl. Acad. Sci. USA, 102, 12047–12052.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Glockner, C., Kern, J., Broser, M., Zouni, A., Yachandra, V., and Yano, J. (2013) Structural changes of the oxygen-evolving complex in photosystem II during the catalytic cycle, J. Biol. Chem., 288, 22607–22620.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Grabolle, M., Haumann, M., Muller, C., Liebisch, P., and Dau, H. (2006) Rapid loss of structural motifs in the manganese complex of oxygenic photosynthesis by X-ray irradiation at 10-300 K, J. Biol. Chem., 281, 4580–4588.CrossRefPubMedGoogle Scholar
  63. 63.
    Kern, J., Alonso-Mori, R., Hellmich, J., Tran, R., Hattne, J., Laksmono, H., Glockner, C., Echols, N., Sierra, R. G., Sellberg, J., Lassalle-Kaiser, B., Gildea, R. J., Glatzel, P., Grosse-Kunstleve, R. W., Latimer, M. J., McQueen, T. A., DiFiore, D., Fry, A. R., Messerschmidt, M., Miahnahri, A., Schafer, D. W., Seibert, M. M., Sokaras, D., Weng, T.-C., Zwart, P. H., White, W. E., Adams, P. D., Bogan, M. J., Boutet, S., Williams, G. J., Messinger, J., Sauter, N. K., Zouni, A., Bergmann, U., Yano, J., and Yachandra, V. K. (2012) Room temperature femtosecond X-ray diffraction of photosystem II microcrystals, Proc. Natl. Acad. Sci. USA, 109, 9721–9726.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Kern, J., Alonso-Mori, R., Tran, R., Hattne, J., Gildea, R. J., Echols, N., Glockner, C., Hellmich, J., Laksmono, H., Sierra, R. G., Lassalle-Kaiser, B., Koroidov, S., Lampe, A., Han, G., Gul, S., DiFiore, D., Milathianaki, D., Fry, A. R., Miahnahri, A., Schafer, D. W., Messerschmidt, M., Seibert, M. M., Koglin, J. E., Sokaras, D., Weng, T.-C., Sellberg, J., Latimer, M. J., Grosse-Kunstleve, R. W., Zwart, P. H., White, W. E., Glatzel, P., Adams, P. D., Bogan, M. J., Williams, G. J., Boutet, S., Messinger, J., Zouni, A., Sauter, N. K., Yachandra, V. K., Bergmann, U., and Yano, J. (2013) Simultaneous femtosecond X-ray spectroscopy and diffraction of photosystem II at room temperature, Science, 340, 491–495.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Gabdulkhakov, A., and Dontsova, M. (2013) Structural studies on photosystem II of cyanobacteria, Biochemistry (Moscow), 78, 1524–1538.CrossRefGoogle Scholar
  66. 66.
    Suga, M., Akita, F., Hirata, K., Ueno, G., Murakami, H., Nakajima, Y., Shimizu, T., Yamashita, K., Yamamoto, M., Ago, H., and Shen, J.-R. (2014) Native structure of photo-system II at 1.95 Å resolution viewed by femtosecond X-ray pulses, Nature, 517, 99–103.CrossRefPubMedGoogle Scholar
  67. 67.
    Young, I. D., Ibrahim, M., Chatterjee, R., Gul, S., Fuller, F. D., Koroidov, S., Brewster, A. S., Tran, R., Alonso-Mori, R., Kroll, T., Michels-Clark, T., Laksmono, H., Sierra, R. G., Stan, C. A., Hussein, R., Zhang, M., Douthit, L., Kubin, M., de Lichtenberg, C., Vo Pham, L., Nilsson, H., Cheah, M. H., Shevela, D., Saracini, C., Bean, M. A., Seuffert, I., Sokaras, D., Weng, T.-C., Pastor, E., Weninger, C., Fransson, T., Lassalle, L., Brauer, P., Aller, P., Docker, P. T., Andi, B., Orville, A. M., Glownia, J. M., Nelson, S., Sikorski, M., Zhu, D., Hunter, M. S., Lane, T. J., Aquila, A., Koglin, J. E., Robinson, J., Liang, M., Boutet, S., Lyubimov, A. Y., Uervirojnangkoorn, M., Moriarty, N. W., Liebschner, D., Afonine, P. V., Waterman, D. G., Evans, G., Wernet, P., Dobbek, H., Weis, W. I., Brunger, A. T., Zwart, P. H., Adams, P. D., Zouni, A., Messinger, J., Bergmann, U., Sauter, N. K., Kern, J., Yachandra, V. K., and Yano, J. (2016) Structure of photosystem II and substrate binding at room temperature, Nature, 540, 453–457.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Suga, M., Akita, F., Sugahara, M., Kubo, M., Nakajima, Y., Nakane, T., Yamashita, K., Umena, Y., Nakabayashi, M., Yamane, T., Nakano, T., Suzuki, M., Masuda, T., Inoue, S., Kimura, T., Nomura, T., Yonekura, S., Yu, L.-J., Sakamoto, T., Motomura, T., Chen, J.-H., Kato, Y., Noguchi, T., Tono, K., Joti, Y., Kameshima, T., Hatsui, T., Nango, E., Tanaka, R., Naitow, H., Matsuura, Y., Yamashita, A., Yamamoto, M., Nureki, O., Yabashi, M., Ishikawa, T., Iwata, S., and Shen, J.-R. (2017) Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL, Nature, 543, 131–135.CrossRefPubMedGoogle Scholar
  69. 69.
    Voet, D., and Voet, J. G. (2011) Biochemistry, John Wiley & Sons.Google Scholar
  70. 70.
    Hucho, F. (1986) Neurochemistry: Fundamentals and Concepts, VCH, Weinheim.Google Scholar
  71. 71.
    Frank, M., Carlson, D. B., Hunter, M. S., Williams, G. J., Messerschmidt, M., Zatsepin, N. A., Barty, A., Benner, W. H., Chu, K., Graf, A. T., Hau-Riege, S. P., Kirian, R. A., Padeste, C., Pardini, T., Pedrini, B., Segelke, B., Seibert, M. M., Spence, J. C. H., Tsai, C.-J., Lane, S. M., Li, X.-D., Schertler, G., Boutet, S., Coleman, M., and Evans, J. E. (2014) Femtosecond X-ray diffraction from two-dimensional protein crystals, IUCrJ, 1, 95–100.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Pedrini, B., Tsai, C.-J., Capitani, G., Padeste, C., Hunter, M. S., Zatsepin, N. A., Barty, A., Benner, W. H., Boutet, S., Feld, G. K., Hau-Riege, S. P., Kirian, R. A., Kupitz, C., Messerschmitt, M., Ogren, J. I., Pardini, T., Segelke, B., Williams, G. J., Spence, J. C. H., Abela, R., Coleman, M., Evans, J. E., Schertler, G. F. X., Frank, M., and Li, X.-D. (2014) 7 Å resolution in protein two-dimensional-crystal X-ray diffraction at Linac Coherent Light Source, Philos. Trans. R. Soc. B Biol. Sci., 369, 20130500–20130505.CrossRefGoogle Scholar
  73. 73.
    Fujiyoshi, Y. (2011) Electron crystallography for structural and functional studies of membrane proteins, Microscopy, 60, S149–S159.CrossRefGoogle Scholar
  74. 74.
    Srivastava, S. K., Gayathri, S., Manjasetty, B. A., and Gopal, B. (2012) Analysis of conformational variation in macromolecular structural models, PLoS One, 7, e39993.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Davis, S. J. (1999) Bacteriophytochromes: phytochrome-like photoreceptors from nonphotosynthetic eubacteria, Science, 286, 2517–2520.CrossRefPubMedGoogle Scholar
  76. 76.
    Auldridge, M. E., and Forest, K. T. (2011) Bacterial phytochromes: more than meets the light, Crit. Rev. Biochem. Mol. Biol., 46, 67–88.CrossRefPubMedGoogle Scholar
  77. 77.
    Edlund, P., Takala, H., Claesson, E., Henry, L., Dods, R., Lehtivuori, H., Panman, M., Pande, K., White, T., Nakane, T., Berntsson, O., Gustavsson, E., Bath, P., Modi, V., Roy-Chowdhury, S., Zook, J., Berntsen, P., Pandey, S., Poudyal, I., Tenboer, J., Kupitz, C., Barty, A., Fromme, P., Koralek, J. D., Tanaka, T., Spence, J., Liang, M., Hunter, M. S., Boutet, S., Nango, E., Moffat, K., Groenhof, G., Ihalainen, J., Stojkovic, E. A., Schmidt, M., and Westenhoff, S. (2016) The room temperature crystal structure of a bacterial phytochrome determined by serial femtosecond crystallography, Sci. Rep., 6, 35279–35288.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • G. K. Selikhanov
    • 1
  • M. S. Fando
    • 1
  • M. V. Dontsova
    • 1
  • A. G. Gabdulkhakov
    • 1
    Email author
  1. 1.Institute of Protein ResearchRussian Academy of SciencesPushchinoRussia

Personalised recommendations