Crystal structures of virus-like photosystem I complexes from the mesophilic cyanobacterium Synechocystis PCC 6803

eLife

Volumn 2014, Issue 3, 2014, Pages

  Mazor, Yuval ^a   Nataf, Daniel ^a   Toporik, Hila ^a   Nelson, Nathan ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME;

ARTICLE; BACTERIUM CULTURE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; CYANOBACTERIUM; ELECTRON TRANSPORT; KINETICS; NONHUMAN; ORGANISMS BY ELECTRON DONOR; PHOTOSYNTHESIS; PHOTOSYSTEM I; PHOTOSYSTEM II; POLYMERASE CHAIN REACTION; SYNECHOCYSTIS; ULTRACENTRIFUGATION;

EID: 84898713850     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01496.001     Document Type: Article

References (56)

1. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta crystallographica Section D, Biological crystallography 66:213-221. doi: 10.1107/S0907444909052925.
2. Ali K, Santabarbara S, Heathcote P, Evans MC, Purton S. 2006. Bidirectional electron transfer in photosystem I: replacement of the symmetry-breaking tryptophan close to the PsaB-bound phylloquinone A1B with a glycine residue alters the redox properties of A1B and blocks forward electron transfer at cryogenic temperatures. Biochimica et Biophysica Acta 1757:1623-1633. doi: 10.1016/j.bbabio.2006.07.006.
3. Alperovitch-Lavy A, Sharon I, Rohwer F, Aro EM, Glaser F, Milo R, Nelson N, Beja O. 2011. Reconstructing a puzzle: existence of cyanophages containing both photosystem-I and photosystem-II gene suites inferred from oceanic metagenomic datasets. Environmental Microbiology 13:24-32. doi: 10.1111/j.1462-2920.2010.02304.x.
4. Amunts A, Drory O, Nelson N. 2007. The structure of a plant photosystem I supercomplex at 3.4 A resolution. Nature 447:58-63. doi: 10.1038/nature05687.
5. Amunts A, Toporik H, Borovikova A, Nelson N. 2010. Structure determination and improved model of plant photosystem I. The Journal of Biological Chemistry 285:3478-3486. doi: 10.1074/jbc.M109.072645.
6. Barber J. 2004. Engine of life and big bang of evolution: a personal perspective. Photosynthesis Research 80:137-155. doi: 10.1023/B:PRES.0000030662.04618.27.
7. Baymann F, Brugna M, Muhlenhoff U, Nitschke W. 2001. Daddy, where did (PS)I come from? Biochimica et Biophysica Acta 1507:291-310. doi: 10.1016/S0005-2728(01)00209-2.
8. Ben-Shem A, Frolow F, Nelson N. 2003. Crystal structure of plant photosystem I. Nature 426:630-635. doi: 10.1038/nature02200.
9. Blankenship RE, Hartman H. 1998. The origin and evolution of oxygenic photosynthesis. Trends in Biochemical Sciences 23:94-97. doi: 10.1016/S0968-0004(98)01186-4.
10. Buttner M, Xie DL, Nelson H, Pinther W, Hauska G, Nelson N. 1992. Photosynthetic reaction center genes in green sulfur bacteria and in photosystem 1 are related. Proceedings of the National Academy of Sciences of the United States of America 89:8135-8139. doi: 10.1073/pnas.89.17.8135.
11. Chitnis PR, Purvis D, Nelson N. 1991. Molecular cloning and targeted mutagenesis of the gene psaF encoding subunit III of photosystem I from the cyanobacterium Synechocystis sp. PCC 6803. The Journal of Biological Chemistry 266:20146-20151.
12. Chitnis VP, Chitnis PR. 1993. PsaL subunit is required for the formation of photosystem I trimers in the cyanobacterium Synechocystis sp. PCC 6803. FEBS letters 336:330-334. doi: 10.1016/0014-5793(93)80831-E.
13. Croce R, van Amerongen H. 2013. Light-harvesting in photosystem I. Photosynthesis Research 116:153-166. doi: 10.1007/s11120-013-9838-x.
14. Evans P. 2006. Scaling and assessment of data quality. Acta crystallographica Section D, Biological crystallography 62:72-82. doi: 10.1107/S0907444905036693.
15. Farah J, Rappaport F, Choquet Y, Joliot P, Rochaix JD. 1995. Isolation of a psaF-deficient mutant of Chlamydomonas reinhardtii: efficient interaction of plastocyanin with the photosystem I reaction center is mediated by the PsaF subunit. The EMBO Journal 14:4976-4984.
16. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S. 2004. Architecture of the photosynthetic oxygen-evolving center. Science 303:1831-1838. doi: 10.1126/science.1093087.
17. Fromme P, Mathis P. 2004. Unraveling the photosystem I reaction center: a history, or the sum of many efforts. Photosynthesis Research 80:109-124. doi: 10.1023/B:PRES.0000030657.88242.e1.
18. Gobets B, van Stokkum IH, Rogner M, Kruip J, Schlodder E, Karapetyan NV, Dekker JP, van Grondelle R. 2001. Time-resolved fluorescence emission measurements of photosystem I particles of various cyanobacteria: a unified compartmental model. Biophysical Journal 81:407-424. doi: 10.1016/S0006-3495(01)75709-8.
19. Hauska G, Schoedl T, Remigy H, Tsiotis G. 2001. The reaction center of green sulfur bacteria(1). Biochimica et biophysica acta 1507:260-277. doi: 10.1016/S0005-2728(01)00200-6.
20. Hervas M, Diaz-Quintana A, Kerfeld CA, Krogmann DW, De la Rosa MA, Navarro JA. 2005. Cyanobacterial Photosystem I lacks specificity in its interaction with cytochrome c(6) electron donors. Photosynthesis Research 83:329-333. doi: 10.1007/s11120-005-1002-9.
21. Hippler M, Reichert J, Sutter M, Zak E, Altschmied L, Schroer U, Herrmann RG, Haehnel W. 1996. The plastocyanin binding domain of photosystem I. The EMBO Journal 15:6374-6384.
22. Jekow P, Fromme P, Witt HT, Saenger W. 1995. Photosystem-i from Synechococcus-elongatus-preparation and crystallization of monomers with Varying subunit compositions. Bba-Bioenergetics 1229:115-120. doi: 10.1016/0005-2728(94)00201-F.
23. Jekow P, Schubert WD, Fromme P, Kruip J, Chitnis PR, Rogner M, Saenger W. 1996. Crystallization of intact and subunit L-deficient monomers from Synechocystis PCC 6803 photosystem I. Z Naturforsch C 51:195-199.
24. Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N. 2001. Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature 411:909-917. doi: 10.1038/35082000.
25. Kabsch W. 2010. Xds. Acta crystallographica Section D, Biological crystallography 66:125-132. doi: 10.1107/S0907444909047337.
26. Liebl U, Mockensturm-Wilson M, Trost JT, Brune DC, Blankenship RE, Vermaas W. 1993. Single core polypeptide in the reaction center of the photosynthetic bacterium Heliobacillus mobilis: structural implications and relations to other photosystems. Proceedings of the National Academy of Sciences of the United States of America 90:7124-7128. doi: 10.1073/pnas.90.15.7124.
27. Mann NH, Cook A, Millard A, Bailey S, Clokie M. 2003. Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 424:741. doi: 10.1038/424741a.
28. Mazor Y, Greenberg I, Toporik H, Beja O, Nelson N. 2012. The evolution of photosystem I in light of phage-encoded reaction centres. Philosophical transactions of the Royal Society of London Series B, Biological sciences 367:3400-3405. doi: 10.1098/rstb.2012.0057.
29. Mulkidjanian AY, Junge W. 1997. On the origin of photosynthesis as inferred from sequence analysis-a primordial UV-protector as common ancestor of reaction centers and antenna proteins. Photosynthesis Research 51:27-42. doi: 10.1023/A:1005726809084.
30. Murshudov GN, Skubak P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Winn MD, Long F, Vagin AA. 2011. REFMAC5 for the refinement of macromolecular crystal structures. Acta crystallographica Section D, Biological crystallography 67:355-367. doi: 10.1107/S0907444911001314.
31. Naithani S, Hou JM, Chitnis PR. 2000. Targeted inactivation of the psaK1, psaK2 and psaM genes encoding subunits of Photosystem I in the cyanobacterium Synechocystis sp. PCC 6803. Photosynthesis Research 63:225-236. doi: 10.1023/A:1006463932538.
32. Nelson N. 2011. Photosystems and global effects of oxygenic photosynthesis. Biochimica et Biophysica Acta 1807:856-863. doi: 10.1016/j.bbabio.2010.10.011.
33. Nelson N, Ben-Shem A. 2004. The complex architecture of oxygenic photosynthesis. Nature Reviews Molecular Cell Biology 5:971-982. doi: 10.1038/nrm1525.
34. Nelson N, Ben-Shem A. 2005. The structure of photosystem I and evolution of photosynthesis. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology 27:914-922. doi: 10.1002/bies.20278.
35. Nelson N, Yocum CF. 2006. Structure and function of photosystems I and II. Annual Review of Plant Biology 57:521-565. doi: 10.1146/annurev.arplant.57.032905.105350.
36. Nicholls RA, Long F, Murshudov GN. 2012. Low-resolution refinement tools in REFMAC5. Acta Crystallographica Section D, Biological Crystallography 68:404-417. doi: 10.1107/S090744491105606X.
37. Palsson LO, Flemming C, Gobets B, van Grondelle R, Dekker JP, Schlodder E. 1998. Energy transfer and charge separation in photosystem I: P700 oxidation upon selective excitation of the long-wavelength antenna chlorophylls of Synechococcus elongatus. Biophysical Journal 74:2611-2622. doi: 10.1016/S0006-3495(98)77967-6.
38. Pan X, Li M, Wan T, Wang L, Jia C, Hou Z, Zhao X, Zhang J, Chang W. 2011. Structural insights into energy regulation of light-harvesting complex CP29 from spinach. Nature Structural & Molecular Biology 18:309-315. doi: 10.1038/nsmb.2008.
39. Peisajovich SG, Rockah L, Tawfik DS. 2006. Evolution of new protein topologies through multistep gene rearrangements. Nature Genetics 38:168-174. doi: 10.1038/ng1717.
40. Philosof A, Battchikova N, Aro EM, Beja O. 2011. Marine cyanophages: tinkering with the electron transport chain. The ISME Journal 5:1568-1570. doi: 10.1038/ismej.2011.43.
41. Rutherford AW, Osyczka A, Rappaport F. 2012. Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O(2). FEBS Letters 586:603-616. doi: 10.1016/j.febslet.2011.12.039.
42. Savitsky A, Niklas J, Golbeck JH, Mobius K, Lubitz W. 2013. Orientation resolving dipolar high-field EPR spectroscopy on disordered solids: II. Structure of Spin-Correlated Radical pairs in photosystem I. The Journal of Physical Chemistry B 117:11184-11199. doi: 10.1021/jp401573z.
43. Sharon I, Alperovitch A, Rohwer F, Haynes M, Glaser F, Atamna-Ismaeel N, Pinter RY, Partensky F, Koonin EV, Wolf YI, Nelson N, Beja O. 2009. Photosystem I gene cassettes are present in marine virus genomes. Nature 461:258-262. doi: 10.1038/nature08284.
44. Sharon I, Battchikova N, Aro EM, Giglione C, Meinnel T, Glaser F, Pinter RY, Breitbart M, Rohwer F, Beja O. 2011. Comparative metagenomics of microbial traits within oceanic viral communities. The ISME Journal 5:1178-1190. doi: 10.1038/ismej.2011.2.
45. Sullivan MB, Waterbury JB, Chisholm SW. 2003. Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424:1047-1051. doi: 10.1038/nature01929.
46. Standfuss R, van Scheltinga ACT, Lamborghini M, Kuhlbrandt W. 2005. Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5A resolution. EMBO Journal 24:919-928. doi: 10.1038/sj.emboj.7600585.
47. Sullivan MB, Lindell D, Lee JA, Thompson LR, Bielawski JP, Chisholm SW. 2006. Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLOS Biology 4:e234. doi: 10.1371/journal.pbio.0040234.
48. Tang HD, Chitnis PR. 2000. Addition of C-terminal histidyl tags to PsaL and PsaK1 proteins of cyanobacterial photosystem I. Indian Journal of Biochemistry & Biophysics 37:433-440.
49. Umena Y, Kawakami K, Shen JR, Kamiya N. 2011. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 angstrom. Nature 473:55-U65. doi: 10.1038/nature09913.
50. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. 2009. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189-1191. doi: 10.1093/bioinformatics/btp033.
51. Wientjes E, Roest G, Croce R. 2012. From red to blue to far-red in Lhca4: how does the protein modulate the spectral properties of the pigments? Biochimica et Biophysica Acta 1817:711-717. doi: 10.1016/j.bbabio.2012.02.030.
52. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS. 2011. Overview of the CCP4 suite and current developments. Acta Crystallographica Section D, Biological Crystallography 67:235-242. doi: 10.1107/S0907444910045749.
53. Xu Q, Hoppe D, Chitnis VP, Odom WR, Guikema JA, Chitnis PR. 1995. Mutational analysis of photosystem I polypeptides in the cyanobacterium Synechocystis sp. PCC 6803. Targeted inactivation of psaI reveals the function of psaI in the structural organization of psaL. The Journal of Biological Chemistry 270:16243-16250. doi: 10.1074/jbc.270.27.16243.
54. Xu Q, Odom WR, Guikema JA, Chitnis VP, Chitnis PR. 1994a. Targeted deletion of psaJ from the cyanobacterium Synechocystis sp. PCC 6803 indicates structural interactions between the PsaJ and PsaF subunits of photosystem I. Plant Molecular Biology 26:291-302. doi: 10.1007/BF00039540.
55. Xu Q, Yu L, Chitnis VP, Chitnis PR. 1994b. Function and organization of photosystem I in a cyanobacterial mutant strain that lacks PsaF and PsaJ subunits. The Journal of Biological Chemistry 269:3205-3211.
56. Zeidner G, Bielawski JP, Shmoish M, Scanlan DJ, Sabehi G, Beja O. 2005. Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. Environmental Microbiology 7:1505-1513. doi: 10.1111/j.1462-2920.2005.00833.x.