Skip to main content
Log in

Investigations of Photosensitive Proteins by Serial Crystallography

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

LCP:

lipid cubic phase

LSP:

lipid sponge phase

PSI(II):

photosystem I(II)

PYP:

photoactive yellow protein

RC:

reaction center

SFX:

serial femtosecond X-ray analysis

XFEL:

X-ray free-electron laser

XRD:

X-ray diffraction analysis

References

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  Google Scholar 

  9. Margaritondo, G., and Rebernik Ribic, P. (2011) A simplified description of X-ray free-electron lasers, J. Synchrotron Radiat., 18, 101–108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  Google Scholar 

  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. European XFEL–Overview–In comparison (https:// www.xfel.eu/facility/comparison/index_eng.html).

  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.

    CAS  PubMed  Google Scholar 

  14. Smyth, M. S. (2000) X-ray crystallography, Mol. Pathol., 53, 8–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  29. Stowell, M. H. (1997) Light-induced structural changes in photosynthetic reaction center: implications for mechanism of electron–proton transfer, Science, 276, 812–816.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Moffat, K., Szebenyi, D., and Bilderback, D. (1984) X-ray Laue diffraction from protein crystals, Science, 223, 1423–1425.

    Article  CAS  PubMed  Google Scholar 

  34. Schotte, F. (2003) Watching a protein as it functions with 150-ps time-resolved X-ray crystallography, Science, 300, 1944–1947.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Blankenship, R. E. (2014) Molecular Mechanisms of Photosynthesis, Wiley/Blackwell, Chichester, West Sussex, p.296.

    Google Scholar 

  42. Nelson, N. (2009) Plant photosystem I–the most efficient nano-photochemical machine, J. Nanosci. Nanotechnol., 9, 1709–1713.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  46. Moffat, K. (1989) Time-resolved macromolecular crystallography, Annu. Rev. Biophys. Biophys. Chem., 18, 309–332.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  49. Fromme, P., and Witt, H. T. (1998) Improved isolation and crystallization of photosystem I for structural analysis, Biochim. Biophys. Acta, 1365, 175–184.

    Article  CAS  Google Scholar 

  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.

    PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  56. Ferreira, K. N. (2004) Architecture of the photosynthetic oxygen-evolving center, Science, 303, 1831–1838.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Gabdulkhakov, A., and Dontsova, M. (2013) Structural studies on photosystem II of cyanobacteria, Biochemistry (Moscow), 78, 1524–1538.

    Article  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  69. Voet, D., and Voet, J. G. (2011) Biochemistry, John Wiley & Sons.

    Google Scholar 

  70. Hucho, F. (1986) Neurochemistry: Fundamentals and Concepts, VCH, Weinheim.

    Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  Google Scholar 

  73. Fujiyoshi, Y. (2011) Electron crystallography for structural and functional studies of membrane proteins, Microscopy, 60, S149–S159.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Davis, S. J. (1999) Bacteriophytochromes: phytochrome-like photoreceptors from nonphotosynthetic eubacteria, Science, 286, 2517–2520.

    Article  CAS  PubMed  Google Scholar 

  76. Auldridge, M. E., and Forest, K. T. (2011) Bacterial phytochromes: more than meets the light, Crit. Rev. Biochem. Mol. Biol., 46, 67–88.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. G. Gabdulkhakov.

Additional information

Original Russian Text © G. K. Selikhanov, M. S. Fando, M. V. Dontsova, A. G. Gabdulkhakov, 2018, published in Uspekhi Biologicheskoi Khimii, 2018, Vol. 58, pp. 347–376.

To whom correspondence should be addressed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Selikhanov, G.K., Fando, M.S., Dontsova, M.V. et al. Investigations of Photosensitive Proteins by Serial Crystallography. Biochemistry Moscow 83 (Suppl 1), S163–S175 (2018). https://doi.org/10.1134/S0006297918140134

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297918140134

Keywords

Navigation