The room temperature crystal structure of a bacterial phytochrome determined by serial femtosecond crystallography

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Edlund, Petra ^a   Takala, Heikki ^a,b,c   Claesson, Elin ^a   Henry, Leócadie ^a   Dods, Robert ^a   Lehtivuori, Heli ^b   Panman, Matthijs ^a   Pande, Kanupriya ^d   White, Thomas ^d   Nakane, Takanori ^e   Berntsson, Oskar ^a   Gustavsson, Emil ^a   Båth, Petra ^a   Modi, Vaibhav ^b   Roy Chowdhury, Shatabdi ^f   Zook, James ^f   Berntsen, Peter ^g   Pandey, Suraj ^h   Poudyal, Ishwor ^h   Tenboer, Jason ^h   Kupitz, Christopher ^h   Barty, Anton ^d   Fromme, Petra ^f   Koralek, Jake D ⁱ   Tanaka, Tomoyuki ^j   Spence, John ^f   Liang, Mengning ⁱ   Hunter, Mark S ⁱ   Boutet, Sebastien ⁱ   Nango, Eriko ^j   Moffat, Keith ^k,l   Groenhof, Gerrit ^b   Ihalainen, Janne ^b   Stojkovi, Emina A ^m   Schmidt, Marius ^h   Westenhoff, Sebastian ^a   more..

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d DESY   (Germany)

^e UNIVERSITY OF TOKYO   (Japan)

^f ARIZONA STATE UNIVERSITY   (United States)

^g LA TROBE UNIVERSITY   (Australia)

^h UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

ⁱ SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^j RIKEN SPring 8 Center   (Japan)

^k UNIVERSITY OF CHICAGO   (United States)

^l ARGONNE NATIONAL LABORATORY   (United States)

^m NORTHEASTERN ILLINOIS UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

PHYTOCHROME;

CHEMISTRY; CRYSTALLIZATION; DEINOCOCCUS; PROTEIN CONFORMATION; TEMPERATURE; X RAY CRYSTALLOGRAPHY;

CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; DEINOCOCCUS; PHYTOCHROME; PROTEIN CONFORMATION; TEMPERATURE;

EID: 84992161882     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep35279     Document Type: Article

References (44)

1. Bae, G., Choi, G. Decoding of light signals by plant phytochromes and their interacting proteins. Annu. Rev. Plant Biol. 59, 281-311 (2008).
2. Hughes, J. Phytochrome cytoplasmic signaling. Annu. Rev. Plant Biol. 64, 377-402 (2013).
3. Gan, F. et al. Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345, 1312-1317 (2014).
4. Davis, S. J., Vener, A. V., Vierstra, R. D. Bacteriophytochromes: Phytochrome-like photoreceptors from nonphotosynthetic eubacteria. Science 286, 2517-2520 (1999).
5. Auldridge, M. E., Forest, K. T. Bacterial phytochromes: More than meets the light. Crit. Rev. Biochem. Mol. Biol. 46, 67-88 (2011).
6. Yang, X., Kuk, J., Moffat, K. Crystal structure of Pseudomonas aeruginosa bacteriophytochrome: Photoconversion and signal transduction. Proc. Natl. Acad. Sci. USA 105, 14715-14720 (2008).
7. Essen, L. O., Mailliet, J., Hughes, J. The structure of a complete phytochrome sensory module in the Pr ground state. Proc. Natl. Acad. Sci. USA 105, 14709-14714 (2008).
8. Wagner, J. R., Zhang, J. R., Brunzelle, J. S., Vierstra, R. D., Forest, K. T. High resolution structure of Deinococcus bacteriophytochrome yields new insights into phytochrome architecture and evolution. J. Biol. Chem. 282, 12298-12309 (2007).
9. Burgie, E. S. et al. Crystallographic and electron microscopic analyses of a bacterial phytochrome reveal local and global rearrangements during photoconversion. J. Biol. Chem. 289, 24573-24587 (2014).
10. Takala, H. et al. Signal amplification and transduction in phytochrome photosensors. Nature 509, 245-248 (2014).
11. Stojkovi?, E. A. et al. FTIR Spectroscopy Revealing Light-Dependent Refolding of the Conserved Tongue Region of Bacteriophytochrome. J. Phys. Chem. Lett. 5, 2512-2515 (2014).
12. Song, C. et al. Two ground state isoforms and a chromophore D-ring photoflip triggering extensive intramolecular changes in a canonical phytochrome. Proc. Natl. Acad. Sci. USA 108, 3842-3847 (2011).
13. Wagner, J. R., Brunzelle, J. S., Forest, K. T., Vierstra, R. D. A light-sensing knot revealed by the structure of the chromophorebinding domain of phytochrome. Nature 438, 325-331 (2005).
14. Burgie, E. S., Zhang, J., Vierstra, R. D. Crystal Structure of Deinococcus Phytochrome in the Photoactivated State Reveals a Cascade of Structural Rearrangements during Photoconversion. Structure 24, 448-457 (2016).
15. Tenboer, J. et al. Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein. Science 346, 1242-1246 (2014).
16. Chapman, H. N. et al. Femtosecond X-ray protein nanocrystallography. Nature 470, 73-78 (2011).
17. Kirian, R. A. et al. Structure-factor analysis of femtosecond microdiffraction patterns from protein nanocrystals. Acta Crystallogr. A. 67, 131-140 (2011).
18. Barends, T. R. M. et al. Direct observation of ultrafast collective motions in CO myoglobin upon ligand dissociation. Science 350, 445-450 (2015).
19. Neutze, R., Wouts, R., van der Spoel, D., Weckert, E., Hajdu, J. Potential for biomolecular imaging with femtosecond X-ray pulses. Nature 406, 752-757 (2000).
20. Hirata, K. et al. Determination of damage-free crystal structure of an X-ray-sensitive protein using an XFEL. Nat. Methods 11, 734-736 (2014).
21. Bhattacharya, S., Auldridge, M. E., Lehtivuori, H., Ihalainen, J. A., Forest, K. T. Origins of fluorescence in evolved bacteriophytochromes. J. Biol. Chem. 289, 32144-32152 (2014).
22. DePonte, D. P. et al. Gas dynamic virtual nozzle for generation of microscopic droplet streams. J. Phys. D. Appl. Phys. 41, 195505 (2008).
23. Boutet, S., Williams, G. J The Coherent X-ray Imaging (CXI) instrument at the Linac Coherent Light Source (LCLS). New J. Phys. 12, 035024 (2010).
24. Barty, A. et al. Cheetah: software for high-throughput reduction and analysis of serial femtosecond X-ray diffraction data. J. Appl. Crystallogr. 47, 1118-1131 (2014).
25. White, T. A. et al. CrystFEL: a software suite for snapshot serial crystallography. J. Appl. Crystallogr. 45, 335-341 (2012).
26. Fraser, J. S. et al. Accessing protein conformational ensembles using room-temperature X-ray crystallography. Proc. Natl. Acad. Sci. USA 108, 16247-16252 (2011).
27. Sugahara, M. et al. Grease matrix as a versatile carrier of proteins for serial crystallography. Nat. Methods 12, 61-63 (2015).
28. Auldridge, M. E., Satyshur, K. A., Anstrom, D. M., Forest, K. T. Structure-guided engineering enhances a phytochrome-based infrared fluorescent protein. J. Biol. Chem. 287, 7000-7009 (2012).
29. Burgie, E. S., Bussell, A. N., Walker, J. M., Dubiel, K., Vierstra, R. D. Crystal structure of the photosensing module from a red/farred light-absorbing plant phytochrome. Proc. Natl. Acad. Sci. USA 111, 10179-10184 (2014).
30. Li, F. et al. X-ray radiation induces deprotonation of the bilin chromophore in crystalline D. radiodurans phytochrome. J. Am. Chem. Soc. 137, 2792-2795 (2015).
31. Kim, P. W., Rockwell, N. C., Martin, S. S., Lagarias, J. C., Larsen, D. S. Dynamic inhomogeneity in the photodynamics of cyanobacterial phytochrome Cph1. Biochemistry 53, 2818-2826 (2014).
32. Weierstall, U. et al. Lipidic cubic phase injector facilitates membrane protein serial femtosecond crystallography. Nat. Commun. 5, 3309 (2014).
33. Dasgupta, J., Frontiera, R. R., Taylor, K. C., Lagarias, J. C., Mathies, R. A. Ultrafast excited-state isomerization in phytochrome revealed by femtosecond stimulated Raman spectroscopy. Proc. Natl. Acad. Sci. USA 106, 1784-1789 (2009).
34. Toh, K. C. et al. Primary Reactions of Bacteriophytochrome Observed with Ultrafast Mid-Infrared Spectroscopy. J. Phys. Chem. A 115, 3778-3786 (2011).
35. Lehtivuori, H. et al. Fluorescence properties of the chromophore-binding domain of bacteriophytochrome from Deinococcus radiodurans. J Phys Chem B 117, 11049-11057 (2013).
36. Kabsch, W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795-800 (1993).
37. Karplus, P. A., Diederichs, K. Linking Crystallographic Model and Data Quality. Science 336, 1030-1033 (2012).
38. Tono, K. et al. Beamline, experimental stations and photon beam diagnostics for the hard X-ray free electron laser of SACLA. New J. Phys. 15, 083035 (2013).
39. Tono, K. et al. Diverse application platform for hard X-ray diffraction in SACLA (DAPHNIS): application to serial protein crystallography using an X-ray free-electron laser. J. Synchrotron Radiat. 22, 532-537 (2015).
40. Kameshima, T. et al. Development of an X-ray pixel detector with multi-port charge-coupled device for X-ray free-electron laser experiments. Rev. Sci. Instrum. 85, 033110 (2014).
41. Nakane, T. et al. Data processing pipeline for serial femtosecond crystallography at SACLA. J. Appl. Crystallogr. 49, 1035-1041 (2016).
42. Storoni, L. C., McCoy, A. J., Read, R. J. Likelihood-enhanced fast rotation functions. Acta Crystallogr. D 60, 432-438 (2004).
43. Emsley, P., Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
44. Murshudov, G. N. et al. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D 67, 355-367 (2011).