Structural and kinetic properties of Rhodobacter sphaeroides photosynthetic reaction centers containing exclusively Zn-coordinated bacteriochlorophyll as bacteriochlorin cofactors

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1837, Issue 3, 2014, Pages 366-374

  Saer, Rafael G ^a   Pan, Jie ^b   Hardjasa, Amelia ^a   Lin, Su ^b   Rosell, Federico ^a   Mauk, A Grant ^a   Woodbury, Neal W ^b   Murphy, Michael E P ^a   Beatty, J Thomas ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Bacteriochlorophyll; Bacteriopheophytin; Electron transfer; Reaction center; Rhodobacter sphaeroides; Spectroscopy

Indexed keywords

BACTERIOCHLORIN; BACTERIOCHLOROPHYLL; BACTERIOPHEOPHYTIN; COORDINATION COMPOUND; HISTIDINE; LIGAND; METAL; UNCLASSIFIED DRUG; ZINC; ZINC BACTERIOCHLOROPHYLL;

ABSORPTION SPECTROSCOPY; ANIMAL CELL; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON TRANSPORT; KINETICS; NONHUMAN; PHOTOSYNTHESIS; PHOTOTROPHIC BACTERIUM; PRIORITY JOURNAL; PROTEIN FUNCTION; RHODOBACTER SPHAEROIDES; SEPARATION TECHNIQUE; X RAY CRYSTALLOGRAPHY;

RHODOBACTER SPHAEROIDES;

BACTERIOCHLOROPHYLL; BACTERIOPHEOPHYTIN; ELECTRON TRANSFER; REACTION CENTER; RHODOBACTER SPHAEROIDES; SPECTROSCOPY;

BACTERIAL PROTEINS; BACTERIOCHLOROPHYLLS; CRYSTALLOGRAPHY, X-RAY; KINETICS; MODELS, MOLECULAR; MUTATION; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PORPHYRINS; PROTEIN CONFORMATION; RHODOBACTER SPHAEROIDES; ZINC;

EID: 84892399993     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2013.11.015     Document Type: Article

References (47)

1. A.J. Hoff, and J. Deisenhofer Photophysics of photosynthesis. Structure and spectroscopy of reaction centers of purple bacteria Phys. Rep. 287 1997 1 247 (Pubitemid 127167669)
2. R.J. Cogdell Photosynthetic reaction centers Annu. Rev. Plant Phys. 34 1983 21 45
3. W.W. Parson, and A. Warshel Mechanism of charge separation in purple bacterial reaction centers C.N. Hunter, F. Daldal, M. Thurnauer, J.T. Beatty, The Purple Phototrophic Bacteria 2008 Springer Netherlands 355 377
4. J.P. Allen, G. Feher, T.O. Yeates, H. Komiya, and D.C. Rees Structure of the reaction center from Rhodobacter sphaeroides R-26: the protein subunits Proc. Natl. Acad. Sci. U. S. A. 84 1987 6162 6166
5. J.P. Allen, G. Feher, T.O. Yeates, H. Komiya, and D.C. Rees Structure of the reaction center from Rhodobacter sphaeroides R-26: the cofactors Proc. Natl. Acad. Sci. U. S. A. 84 1987 5730 5734
6. B. Feniouk, and W. Junge Proton translocation and ATP synthesis by the FoF1-ATPase of purple bacteria C.N. Hunter, F. Daldal, M. Thurnauer, J.T. Beatty, The Purple Phototrophic Bacteria 2008 Springer Netherlands 475 493
7. R. Berera, R. van Grondelle, and J.T. Kennis Ultrafast transient absorption spectroscopy: principles and application to photosynthetic systems Photosynth. Res. 101 2009 105 118
8. C.C. Moser, J.M. Keske, K. Warncke, R.S. Farid, and P.L. Dutton Nature of biological electron transfer Nature 355 1992 796 802
9. S. Lin, P.R. Jaschke, H. Wang, M. Paddock, A. Tufts, J.P. Allen, F.I. Rosell, A.G. Mauk, N.W. Woodbury, and J.T. Beatty Electron transfer in the Rhodobacter sphaeroides reaction center assembled with zinc bacteriochlorophyll Proc. Natl. Acad. Sci. U. S. A. 106 2009 8537 8542
10. B. Neupane, P. Jaschke, R. Saer, J.T. Beatty, M. Reppert, and R. Jankowiak Electron transfer in Rhodobacter sphaeroides reaction centers containing Zn-bacteriochlorophylls: a hole-burning study J. Phys. Chem. B 116 2012 3457 3466
11. C. Kirmaier, D. Gaul, R. DeBey, D. Holten, and C.C. Schenck Charge separation in a reaction center incorporating bacteriochlorophyll for photoactive bacteriopheophytin Science 251 1991 922 927 (Pubitemid 21926183)
12. M. Kobayashi, M. Yamamura, M. Akiyama, H. Kise, K. Inoue, M. Hara, N. Wakao, K. Yahara, and T. Watanabe Acid resistance of Zn-bacteriochlorophyll a from an acidophilic bacteria Acidiphilium rubrum Anal. Sci. 14 1998 1149 1152
13. N. Wakao, N. Yokoi, N. Isoyama, A. Hiraishi, K. Shimada, M. Kobayashi, H. Kise, M. Iwaki, S. Itoh, S. Takaichi, and Y. Sakurai Discovery of natural photosynthesis using Zn-containing bacteriochlorophyll in an aerobic bacterium Acidiphilium rubrum Plant Cell Physiol. 37 1996 889 893 (Pubitemid 26405187)
14. T.A. Evans, and J.J. Katz Evidence for 5- and 6-coordinated magnesium in bacteriochlorophyll a from visible absorption spectroscopy Biochim. Biophys. Acta 396 1975 414 426
15. D. Noy, L. Fiedor, G. Hartwich, H. Scheer, and A. Scherz Metal-substituted bacteriochlorophylls. 2. Changes in redox potentials and electronic transition energies are dominated by intramolecular electrostatic interactions J. Am. Chem. Soc. 120 1998 3684 3693 (Pubitemid 28218445)
16. G. Hartwich, L. Fiedor, I. Simonin, E. Cmiel, W. Schafer, D. Noy, A. Scherz, and H. Scheer Metal-substituted bacteriochlorophylls. 1. Preparation and influence of metal and coordination on spectra J. Am. Chem. Soc. 120 1998 3675 3683 (Pubitemid 28218444)
17. J.T. Beatty, and H. Gest Generation of succinyl coenzyme-A in photosynthetic bacteria Arch. Microbiol. 129 1981 335 340 (Pubitemid 11001037)
18. D. Jun, R.G. Saer, J.D. Madden, and J.T. Beatty Use of new strains of Rhodobacter sphaeroides and a modified simple culture medium to increase yield and facilitate purification of the reaction centre Photosynth. Res. 2013 1 9
19. A. Tehrani, and J.T. Beatty Effects of precise deletions in Rhodobacter sphaeroides reaction center genes on steady-state levels of reaction center proteins: a revised model for reaction center assembly Photosynth. Res. 79 2004 101 108 (Pubitemid 38184779)
20. R.G. Saer, A. Hardjasa, F.I. Rosell, A.G. Mauk, M.E. Murphy, and J.T. Beatty Role of Rhodobacter sphaeroides photosynthetic reaction center residue M214 in the composition, absorbance properties, and conformations of H(A) and B(A) cofactors Biochemistry 52 2013 2206 2217
21. J.O. Goldsmith, and S.G. Boxer Rapid isolation of bacterial photosynthetic reaction centers with an engineered poly-histidine tag Biochim. Biophys. Acta-Bioenergetics 1276 1996 171 175 (Pubitemid 26321078)
22. J. Pan, R.G. Saer, S. Lin, Z. Guo, J.T. Beatty, and N.W. Woodbury The protein environment of the bacteriopheophytin anion modulates charge separation and charge recombination in bacterial reaction centers J. Phys. Chem. B 117 2013 7179 7189
23. A.G.W. Leslie, and H.R. Powell Processing diffraction data with MOSFLM Nato. Sci. Ser. II Math. 2007 41 51
24. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, R.M. Keegan, E.B. Krissinel, A.G. Leslie, A. McCoy, S.J. McNicholas, G.N. Murshudov, N.S. Pannu, E.A. Potterton, H.R. Powell, R.J. Read, A. Vagin, and K.S. Wilson Overview of the CCP4 suite and current developments Acta Crystallogr. D Biol. Crystallogr. 67 2011 235 242
25. A.A. Vagin, R.A. Steiner, A.A. Lebedev, L. Potterton, S. McNicholas, F. Long, and G.N. Murshudov REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use Acta Crystallogr. D Biol. Crystallogr. 60 2004 2184 2195 (Pubitemid 41742770)
26. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132 (Pubitemid 41742764)
27. C. Kirmaier, L. Laporte, C.C. Schenck, and D. Holten The nature and dynamics of the charge-separated Intermediate in reaction centers in which bacteriochlorophyll replaces the photoactive bacteriopheophytin.1. Spectral characterization of the transient state J. Phys. Chem. 99 1995 8903 8909
28. J. Koepke, E.M. Krammer, A.R. Klingen, P. Sebban, G.M. Ullmann, and G. Fritzsch pH modulates the quinone position in the photosynthetic reaction center from Rhodobacter sphaeroides in the neutral and charge separated states J. Mol. Biol. 371 2007 396 409 (Pubitemid 47048266)
29. T.O. Yeates, H. Komiya, A. Chirino, D.C. Rees, J.P. Allen, and G. Feher Structure of the reaction center from Rhodobacter-sphaeroides R-26 and 2.4.1-protein-cofactor (bacteriochlorophyll, bacteriopheophytin, and carotenoid) interactions.4. Proc. Natl. Acad. Sci. U. S. A. 85 1988 7993 7997
30. S. Lin, A.K.W. Taguchi, and N.W. Woodbury Excitation wavelength dependence of energy transfer and charge separation in reaction centers from Rhodobacter sphaeroides: evidence for adiabatic electron transfer J. Phys. Chem. 100 1996 17067 17078 (Pubitemid 126787144)
31. M.G. Muller, K. Griebenow, and A.R. Holzwarth Primary processes in isolated bacterial reaction centers from Rhodobacter sphaeroides studied by picosecond fluorescence kinetics Chem. Phys. Lett. 199 1992 465 469
32. C. Kirmaier, L. Laporte, C.C. Schenck, and D. Holten The nature and dynamics of the charge-separated intermediate in reaction centers in which bacteriochlorophyll replaces the photoactive bacteriopheophytin.2. The rates and yields of charge separation and recombination J. Phys. Chem. 99 1995 8910 8917
33. J.L. Martin, J. Breton, A.J. Hoff, A. Migus, and A. Antonetti Femtosecond spectroscopy of electron transfer in the reaction center of the photosynthetic bacterium Rhodopseudomonas sphaeroides R-26: Direct electron transfer from the dimeric bacteriochlorophyll primary donor to the bacteriopheophytin acceptor with a time constant of 2.8 +/- 0.2 psec Proc. Natl. Acad. Sci. U. S. A. 83 1986 957 961
34. I.H. van Stokkum, D.S. Larsen, and R. van Grondelle Global and target analysis of time-resolved spectra Biochim. Biophys. Acta 1657 2004 82 104 (Pubitemid 38952870)
35. P.R. Jaschke, and J.T. Beatty The photosystem of Rhodobacter sphaeroides assembles with zinc bacteriochlorophyll in a bchD (magnesium chelatase) mutant Biochemistry 46 2007 12491 12500 (Pubitemid 350022401)
36. W.W. Parson, R.K. Clayton, and R.J. Cogdell Excited-states of photosynthetic reaction centers at low redox potentials Biochim. Biophys. Acta 387 1975 265 278
37. - in a leucine M214 to histidine mutant of the Rhodobacter sphaeroides reaction center using femtosecond midinfrared spectroscopy Biophys. J. 96 2009 4956 4965
38. H.Y. Wang, Y.W. Hao, Y. Jiang, S. Lin, and N.W. Woodbury Role of protein dynamics in guiding electron-transfer pathways in reaction centers from Rhodobacter sphaeroides J. Phys. Chem. B 116 2012 711 717
39. T. Masuda, K. Inoue, M. Masuda, M. Nagayama, A. Tamaki, H. Ohta, H. Shimada, and K. Takamiya Magnesium insertion by magnesium chelatase in the biosynthesis of zinc bacteriochlorophyll a in an aerobic acidophilic bacterium Acidiphilium rubrum J. Biol. Chem. 274 1999 33594 33600 (Pubitemid 129511671)
40. T. Tomi, Y. Shibata, Y. Ikeda, S. Taniguchi, C. Haik, N. Mataga, K. Shimada, and S. Itoh Energy and electron transfer in the photosynthetic reaction center complex of Acidiphilium rubrum containing Zn-bacteriochlorophyll a studied by femtosecond up-conversion spectroscopy Biochim. Biophys. Acta 1767 2007 22 30 (Pubitemid 46096887)
41. M.R. Jones Structural plasticity of reaction centers from purple bacteria C.N. Hunter, F. Daldal, M. Thurnauer, J.T. Beatty, The Purple Phototrophic Bacteria 2008 Springer Netherlands 295 321
42. B cofactor is not required for assembly or core function of the Rhodobacter sphaeroides complex Biochim. Biophys. Acta 1710 2005 34 46 (Pubitemid 41566997)
43. A, B Photosynth. Res. 44 1995 55 65
44. - state Biochim. Biophys. Acta Bioenerg. 1319 1997 242 250 (Pubitemid 27156895)
45. 2-hydroxy-bacteriochlorophyll FEBS Lett. 261 1990 385 388 (Pubitemid 20075000)
46. H. Scheer, and G. Hartwich Bacterial reaction centers with modified tetrapyrrole chromophores R. Blankenship, M. Madigan, C. Bauer, Anoxygenic Photosynthetic Bacteria 1995 Springer Netherlands 649 663
47. P.R. Jaschke, A. Hardjasa, E.L. Digby, C.N. Hunter, and J.T. Beatty A bchD (magnesium chelatase) mutant of Rhodobacter sphaeroides synthesizes zinc-bacteriochlorophyll through novel zinc-containing intermediates J. Biol. Chem. 286 2011 20313 20322