Developing a structure-function model for the cryptophyte phycoerythrin 545 using ultrahigh resolution crystallography and ultrafast laser spectroscopy

Journal of Molecular Biology

Volumn 344, Issue 1, 2004, Pages 135-153

  Doust, Alexander B ^a   Marai, Christopher N J ^a   Harrop, Stephen J ^b,c   Wilk, Krystyna E ^b   Curmi, Paul M G ^b,c   Scholes, Gregory D ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c ST VINCENT S HOSPITAL   (Australia)

Author keywords

cryptophyte; energy transfer; photosynthesis; phycoerythrin; ultrahigh resolution X ray crystallography

Indexed keywords

PHYCOERYTHRIN;

ABSORPTION SPECTROSCOPY; ALGA; ARTICLE; CHROMATOPHORE; COMPUTER MODEL; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENERGY TRANSFER; FLAME PHOTOMETRY; LASER; MEMBRANE BINDING; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; QUANTUM CHEMISTRY; SPECTROSCOPY; STRUCTURE ACTIVITY RELATION; ULTRAFAST LASER SPECTROSCOPY;

ALGAE; CRYPTOPHYTA; CYANOBACTERIA; RHODOMONAS; RHODOPHYTA;

EID: 7044235387     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.09.044     Document Type: Article

References (90)

1. W.A. Sidler Phycobilisome and phycobiliprotein structures D.A. Bryant The Molecular Biology of Cyanobacteria Advances in Photosynthesis vol. 1 1994 Kluwer Academic Publishers Dordrecht, The Netherlands 139 216
2. K.E. Wilk, S.J. Harrop, L. Jankova, D. Edler, G. Keenan, and F. Sharples Evolution of a light-harvesting protein by addition of new subunits and rearrangement of conserved elements: crystal structure of a cryptophyte phycoerythrin at 1.63-Å resolution Proc. Natl Acad. Sci.USA 96 1999 8901 8906
3. E. Gantt Structure and function of phycobilisomes: light harvesting pigment complexes in red and blue-green algae Int. Rev. Cyt. 66 1980 45 80
4. R. MacColl, and D. Guard-Friar Phycobiliproteins 1987 CRC Press Boca Raton, FL
5. E. Morschel, and E. Rhiel J.R. Harris R.W. Horne Electron Microscopy of Proteins 6th edit. 1987 Academic Press New York 209 554
6. A.N. Glazer Phycobilisome. A macromolecular complex optimized for light energy transfer Biochim. Biophys. Acta 768 1984 29 51
7. B.J. Homoelle, M.D. Edington, W.M. Diffey, and W.F. Beck Stimulated photon-echo and transient-grating studies of protein-matrix solvation dynamics and interexciton-state radiationless decay in α-phycocyanin and allophycocyanin J. Phys. Chem. B 102 1998 3044 3052
8. R. MacColl, H. Malak, I. Gryczynski, L.E. Eisele, G.J. Mizejewski, and E. Franklin Phycoerythrin 545: monomers, energy migration, bilin topography, and monomer/dimer equilibrium Biochemistry 37 1998 417 423
9. A.N. Glazer Light harvesting by phycobilisomes Ann. Rev. Biophys. Biophys. Chem. 14 1985 47 77
10. I. Yamazaki, M. Mimuro, T. Murao, T. Yamazaki, K. Yoshihara, and Y. Fujita Exciton energy transfer in the light harvesting antenna system of the red alga porphyridium-cruentum and the blue-green alga Anacystis nidulans - analysis of the time-resolved fluorescence spectra Photochem. Photobiol. 39 1984 233 240
11. L. Spear-Bernstein, and K.R. Miller Unique location of the phycobiliprotein light-harvesting pigment in the Cryptophyceae J. Phycol. 25 1989 412 419
12. E. Gantt Phycobiliproteins of cryptophyceae M. Levandowsky S.H. Hutner 2nd edit. Biochemistry and Physiology of Protazoa vol. 1 1979 Academic Press New York 121 137
13. D. Bruce, J. Biggins, T. Steiner, and M. Thewalt Excitation energy transfer in the cryptophytes. Fluorescence excitation spectra and picosecond time-resolved emission spectra of intact algae at 77 K Photochem. Photobiol. 44 1986 519 525
14. G.J. Wedemayer, D.G. Kidd, and A.N. Glazer Cryptomonad biliproteins: bilin types and locations Photosynth. Res. 48 1996 163 170
15. A.Y. Borisov Transfer of excitation energy in photosynthesis: some thoughts Photosynth. Res. 20 1989 35 38
16. S.E. Braslavsky, A.R. Holzwarth, and K. Schaffner Solution conformations, photophysics, and photochemistry of bile pigments; bilirubin and biliverdin dimethyl esters and related linear tetrapyrroles Angew. Chem. Int. Ed. Engl. 22 1983 656 674
17. H. Scheer, and W. Kufer Studies on plant bile pigments. IV. Conformational studies on C-phycocyanin from Spirulina platensis Z. Naturforsch. C: J. Biosci. 32C 1977 513 519
18. R. MacColl, D. Guard-Friar, and T.J. Ryan Biliprotein light-harvesting strategies, phycoerythrin 566 Biochemistry 29 1990 430 435
19. L. Cheng, and L. Jiang Spectroscopic properties of the phycobilins and their derivatives Chin. Chem. Letters 2 7 1991 589 592
20. R. Huber A structural basis of light energy and electron transfer in biology EMBO J. 8 1989 2125 2147
21. C.D. Martin, and R.G. Hiller Subunits and chromophores of a type I phycoerythrin from a Chroomonas sp. (Cryptophyceae) Biochim. Biophys. Acta 923 1987 88 97
22. R.G. Hiller, and C.D. Martin Multiple forms of a type I phycoerythrin from a Chroomonas sp. (Cryptophyceae) varying in subunit composition Biochim. Biophys. Acta 923 1987 98 102
23. K.S. Rowan Photosynthetic Pigments of Algae 1989 Cambridge University Press Cambridge
24. D.R.A. Hill, and K.S. Rowan The biliproteins of the Cryptophyceae Phycologia 28 1989 455 463
25. R. MacColl, I. Lam, C.Y. Choi, and J. Kim Exciton splitting in phycoerythrin 545 J. Biol. Chem. 269 1994 25465 25469
26. R. MacColl, L.E. Eisele, M. Dhar, J.P. Ecuyer, S. Hopkins, and J. Marrone Bilin organization in cryptomonad biliproteins Biochemistry 38 1999 4097 4105
27. R. MacColl, L.E. Eisele, and J. Marrone Fluorescence polarization studies on four biliproteins and a bilin model for phycoerythrin 545 Biochim. Biophys. Acta 1412 1999 230 239
28. O. Nanba, and K. Satoh Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559 Proc. Natl Acad. Sci. USA 84 1987 109 112
29. B. Zickendraht-Wendelstadt, J. Friedrich, and W. Rüdiger Spectral characterization of monomeric C-phycoerythrin from Pseudanabaena W 1173 and its α and β subunits: energy transfer in isolated subunits and C-phycoerythrin Photochem. Photobiol. 31 1980 367 376
30. A.R. Holzwarth Structure-function relationships and energy transfer in phycobiliprotein antennae Physiologia Plantarum 83 1991 518 528
31. H. Marten, M.H. Vos, J. Breton, and J-L. Martin Electronic energy transfer within the hexamer cofactor system of bacterial reaction centers J. Phys. Chem. B 101 1997 9820 9832
32. J.M. Salverda, M. Vengris, B.P. Krueger, G.D. Scholes, A.R. Czarnoleski, and V. Novoderezhkin Energy transfer in light-harvesting complexes LHCII and CP29 of spinach studied with three pulse echo peak shift and transient grating Biophys. J. 84 2003 450 465
33. D.M. Jonas, M.J. Lang, Y. Nagasawa, T. Joo, and G.R. Fleming Pump-probe polarization anisotropy study of femtosecond energy transfer within the photosynthetic reaction center of Rhodobacter sphaeroides R26 J. Phys. Chem. 100 1996 12660 12673
34. S.E. Bradforth, R. Jimenez, F. Van Mourik, R. Van Grondelle, and G.R. Fleming Excitation transfer in the core light-harvesting complex (LH-1) of Rhodobacter sphaeroides: an ultrafast fluorescence depolarization and annihilation study J. Phys. Chem. 99 1995 16179 16191
35. L.D. Book, A.E. Ostafin, N. Ponomarenko, J.R. Norris, and N.F. Scherer Exciton Delocalization and initial dephasing dynamics of purple bacterial LH2 J. Phys. Chem. B 104 2000 8295 8307
36. V.I. Prokhorenko, A.R. Holzwarth, F.R. Nowak, and T.J. Aartsma Growing-in of optical coherence in the FMO antenna complexes J. Phys. Chem. B 106 2002 9923 9933
37. S. Grimme, and M. Parac Substantial errors from time-dependent density functional theory for the calculation of excited states of large π systems ChemPhysChem 3 2003 292 295
38. J. Catalan, and J.L.G. de Paz On the ordering of the first two excited electronic states in all-trans linear polyenes J. Chem. Phys. 120 2004 1864 1872
39. A.L. Sobolewski, and W. Domcke Ab initio study of the excited-state coupled electron-proton-transfer process in the 2-aminopyridine dimer Chem. Phys. 294 2003 73 83
40. M. Mimuro, and H. Kikuchi Light-harvesting antennas in photosynthesis B.R. Green W.W. Parson Antenna Systems and Energy Transfer in Cyanophyta and Rhodophyta 2003 Kluwer Academic Publishers Dordrecht, The Netherlands 281 306 Chapter 9
41. M. Mimuro, N. Tamai, A. Murakami, M. Watanabe, M. Erata, and M.M. Watanabe Multiple pathways of excitation energy flow in the photosynthetic pigment system of a cryptophyte, Cryptomonas sp. (CR-1) Phycol. Res. 46 1998 155 164
42. A.N. Glazer Light guides. Directional energy transfer in a photosynthetic antenna J. Biol. Chem. 264 1989 1 4
43. H. Scheer F.K. Fong Light Reaction Path of Photosynthesis. Molecular Biology, Biochemistry, and Biophysics vol. 35 1982 Springer New York 7 45
44. A.R. Holzwarth Structure-function relationships and energy transfer in phycobiliprotein antennae Physiologia Plantarum 83 1991 518 528
45. H. Kikuchi, T. Sugimoto, and M. Mimuro An electronic state of the chromophore, phycocyanobilin, and its interaction with the protein moiety in C-phycocyanin: protonation of the chromophore Chem. Phys. Letters 274 1997 460 465
46. G.J.S. Fowler, R.W. Visschers, G.G. Grief, R. van Grondelle, and C.N. Hunter Genetically modified photosynthetic antenna complexes with blueshifted absorbance bands Nature 355 1992 848 850
47. T. Pullerits, and V. Sundström Photosynthetic light-harvesting pigment-protein complexes: toward understanding how and why Accts Chem. Res. 29 1996 381 389
48. S.E. Boiadjiev, and D.A. Lightner Optical activity and stereochemistry of linear oligopyrroles and bile pigments Tetrahedron: Asymmetry 10 1999 607 655
49. R. MacColl, H. Malak, J. Cipollo, B. Label, G. Ricci, D. MacColl, and L.E. Eisele Studies on the dissociation of cryptomonad biliproteins J. Biol. Chem. 270 1995 27555 27561
50. H. Sumi Theory on rates of excitation-energy transfer between molecular aggregates through distributed transition dipoles with application to the antenna system in bacterial photosynthesis J. Phys. Chem. B 103 1999 252 260
51. G.D. Scholes, X.J. Jordanides, and G.R. Fleming Adapting the Förster theory of energy transfer for modeling dynamics in aggregated molecular assemblies J. Phys. Chem. B 105 2001 1640 1651
52. J. Robert, R.J. Stanley, B. King, and S.G. Boxer Excited state energy transfer pathways in photosynthetic reaction centers. 1. Structural symmetry effects J. Phys. Chem. 100 1996 12052 12059
53. G. Haran, K. Wynne, C.C. Moser, P.L. Dutton, and R.M. Hochstrasser Level mixing and energy redistribution in bacterial photosynthetic reaction centers J. Phys. Chem. 100 1996 5562 5569
54. D.C. Arnett, C.C. Moser, P.L. Dutton, and N.F. Scherer The first events in photosynthesis: electronic coupling and energy transfer dynamics in the photosynthetic reaction center from Rhodobacter sphaeroides J. Phys. Chem. B 103 1999 2014 2032
55. H.Z. Wang, X.G. Zheng, F.L. Zhao, Z.L. Gao, Z.X. Yu, and J.C. Zhu Time-resolved excitation density dependent fluorescence of R-phycoerythrin single crystal Chem. Phys. Letters 222 1994 204 208
56. R. Van Grondelle Excitation energy transfer, trapping and annihilation in photosynthetic systems Biochim. Biophys. Acta 811 1985 147 195
57. C.W. Mullineaux Excitation energy transfer from phycobilisomes to photosystem I in a cyanobacterium Biochim. Biophys. Acta 1100 1992 285 292
58. F.A.M. Kleinherenbrink, G. Deinum, S.C.M. Otte, A.J. Hoff, and J. Amesz Energy transfer from long-wavelength absorbing antenna bacteriochlorophylls to the reaction center Biochim. Biophys. Acta 1099 1992 175 181
59. H. Van Amerongen, L. Valkunas, and R. Van Grondelle Photosynthetic Excitons 2000 World Scientific Singapore
60. V. Sundström, and T. Pullerits Photosynthetic light harvesting: reconciling dynamics and structure of purple bacterial LH2 reveals function of photosynthetic unit J. Phys. Chem. B 103 1999 2327 2346
61. G.R. Fleming, and R. Van Grondelle Femtosecond spectroscopy of photosynthetic light-harvesting systems Curr. Opin. Struct. Biol. 7 5 1997 738 748
62. K. Sauer, and H. Scheer Excitation transfer in C-phycocyanin. Forster transfer rate and exciton calculations based on new crystal structure data for C-phycocyanins from Agmenellum quadruplicatum and Mastigocladus laminosus Biochim. Biophys. Acta 936 1988 157 170
63. M.P. Debreczeny, K. Sauer, J. Zhou, and D.A. Bryant Comparison of calculated and experimentally resolved rate constants for excitation energy transfer in C-phycocyanin. 1. Monomers J. Phys. Chem. 99 1995 8412 8419
64. C. Scharnagl, and S. Schneider UV-visible absorption and circular dichroism spectra of the subunits of C-phycocyanin II: a quantitative discussion of the chromophore-protein and chromophore-chromophore interactions in the β-subunit J. Photochem. Photobiol. B: Biol. 8 1991 129 157
65. C.N.J. Marai, G.A. Chass, A.B. Doust, and G.D. Scholes An ab initio conformational study on 2,3-dihydrobilin-1,19(21H,24H)-dione, a model compound for open-chain tetrapyrroles J. Mol. Struct. (Theochem) 680 2004 219 225
66. A.N. Macpherson, and R.G. Hiller Light-harvesting antennas in photosynthesis B.R. Green W.W. Parson Light-Harvesting Systems in Chlorophyll c-Containing Algae 2003 Kluwer Academic Publishers Dordrecht, The Netherlands 323 352 Chapter 11
67. G.D. Scholes Long-range resonance energy transfer in molecular systems Annu. Rev. Phys. Chem. 54 2003 57 87
68. R.G. Hiller, C.D. Scaramuzzi, and J. Breton The organisation of photosynthetic pigments in a cryptophyte alga: a linear dichroism study Biochim. Biophys. Acta 1102 1992 360 364
69. R.L. Guillard, and J.H. Ryther Studies of marine planktonic diatoms. I. Cyclotella nana and Detonula confervacea Can. J. Microbiol. 8 1962 229 239
70. Leslie, A. G. W. (1992). Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4+ESF-EAMCB Newsletter on Protein Crystallography, 26.
71. Collaborative Computing Project No. 4. (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D, 50, 760-763.
72. Jones, T. A., Zou, J. Y., Cowan, S. W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A, 47, 110-119.
73. Murshudov, G. N., Vagin, A. A. & Dodson, E. J. (1997). Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallog. sect. D, 53, 240-255.
74. J.R. Lakowicz Principles of Fluorescence Spectroscopy 1st edit. 1983 Plenum Press New York pp. 111-153
75. M. Van Gurp, G. Van Ginkel, and Y.K. Levine Fluorescence anisotropy of chlorophyll a and chlorophyll b in castor oil Biochim. Biophys. Acta 973 1989 405 413
76. T. Wilhelm, J. Piel, and E. Riedle Sub-20- fs pulses tunable across the visible from a blue-pumped single-pass noncollinear parametric converter Opt. Letters 22 1997 1494 1496
77. G.D. Scholes, D.S. Larsen, G.R. Fleming, G. Rumbles, and P.L. Burn Origin of line broadening in the electronic absorption spectra of conjugated polymers: three-pulse-echo studies of MEH-PPV in toluene Phys. Rev. B 61 2000 13670 13678
78. T. Joo, Y. Jia, J-Y. Yu, M.J. Lang, and G.R. Fleming Third-order nonlinear time domain probes of salvation dynamics J. Chem. Phys. 104 1996 6089 6108
79. M.R. Salvador, M.A. Hines, and G.D. Scholes Exciton-bath coupling and inhomogeneous broadening in the optical spectroscopy of semiconductor quantum dots J. Chem. Phys. 118 2003 9380 9388
80. A.D. Becke Density-functional thermochemistry. III. The role of exact exchange J. Chem. Phys. 98 1993 5648 5652
81. R. Ditchfield, W.J. Hehre, and J.A. Pople Self-consistent molecular-orbital methods. IX. An extended Gaussian-type basis for molecular-orbital studies of organic molecules J. Chem. Phys. 54 1971 724 728
82. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R. et al. (1998). Gaussian 98, Revision A.9. Gaussian, Inc., Pittsburgh PA.
83. A.D. Bacon, and M.C. Zerner An intermediate neglect of differential overlap theory for transition metal complexes: Fe, Co, and Cu chlorides Theor. Chim. Acta 53 1979 21 54
84. J.B. Foresman, M. Head-Gordon, J.A. Pople, and M.J. Frisch Towards a systematic molecular orbital theory for excited states J. Phys. Chem. 96 1992 135 149
85. J.S. Binkley, J.A. Pople, and W.J. Hehre Self-consistent molecular orbital methods. 21. Small split-valence basis sets for first-row elements J. Am. Chem. Soc. 102 1980 939 947
86. R. Krishnan, J.S. Binkley, R. Seeger, and J.A. Pople Self-consistent molecular orbital methods. XX. A basis set for correlated wave functions J. Chem. Phys. 72 1980 650 654
87. J.M.O. Matos, B.O. Roos, and P.A. Malmqvist A CASSCF-CCI study of the valence and lower excited states of the benzene molecule J. Chem. Phys. 86 1987 1458 1466
88. J.M.O. Matos, and B.O. Roos A CAS-SCF study of the singlet-singlet and triplet-triplet spectroscopy of naphthalene Theor. Chim. Acta 74 1988 363 379
89. C. Jamorski, M.E. Casida, and D.R.J. Salahub Dynamic polarizabilities and excitation spectra from a molecular implementation of time-dependent density-functional response theory: N2 as a case study J. Chem. Phys. 104 1996 5134 5147
90. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Cryst. 26 1993 283 291