Preferential pathways for light-trapping involving β-ligated chlorophylls

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1787, Issue 10, 2009, Pages 1254-1265

  Balaban, Teodor Silviu ^a,b,c   Braun, Paula ^d   Hättig, Christof ^a,e   Hellweg, Arnim ^a,e,f   Kern, Jan ^g   Saenger, Wolfram ^h   Zouni, Athina ^g  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF KARLSRUHE   (Germany)

^c AIX MARSEILLE UNIVERSITÉ   (France)

^d UNIVERSITY OF MUNICH   (Germany)

^e RUHR UNIVERSITY BOCHUM   (Germany)

^f COSMOlogic GmbH and CoKG ^*  (Germany)

^g TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^h FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

ab initio calculation; Chlorophyll complex; Crystal structure; Diastereotopicity; Photosystem I; Photosystem II

Indexed keywords

BACTERIOCHLOROPHYLL A; CHLORIDE; CHLOROPHYLL; DIMER; LIGAND; LIPID; MAGNESIUM; MONOMER; PROTEIN SUBUNIT; QUINONE DERIVATIVE;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYANOBACTERIUM; ENERGY TRANSFER; MOLECULAR INTERACTION; MOLECULAR MODEL; PHOTOSYNTHESIS; PHOTOSYSTEM I; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTEIN BINDING;

BACTERIAL PROTEINS; BACTERIOCHLOROPHYLLS; BINDING SITES; CHLOROPHYLL; HISTIDINE; LIGANDS; LIGHT; LIGHT-HARVESTING PROTEIN COMPLEXES; MODELS, CHEMICAL; PHOTOSYSTEM I PROTEIN COMPLEX; PHOTOSYSTEM II PROTEIN COMPLEX; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEOBACTERIA; SPECTRUM ANALYSIS; THERMODYNAMICS;

ALGAE; CYANOBACTERIA; PHOTOBACTERIA; PROTEOBACTERIA;

EID: 67650165620     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2009.05.010     Document Type: Article

References (57)

1. Blankenship R.E. Molecular Mechanisms of Photosynthesis (2002), Blackwell, Oxford
2. Balaban T.S. Light-harvesting nanostructures. In: Nalwa H.S. (Ed). Encyclopedia of Nanoscience and Nanotechnology Vol. 4 (2004), American Scientific Publishers, Los Angeles 505-559
3. Balaban T.S., Tamiaki H., and Holzwarth A.R. Chlorins programmed for self-assembly. In: Würthner F. (Ed). Topics Curr. Chem. Supramolecular Dye Chemistry 258 (2005), Springer Verlag: Heidelberg 1-38
4. van Grondelle R., Dekker J.P., Gillbro T., and Sundstrom V. Energy transfer and trapping in photosynthesis. Biochim. Biophys. Acta 1187 (1994) 1-65
5. Deisenhofer J., Epp O., Miki K., Huber R., and Michel H. Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution. Nature 318 (1985) 618-624
6. Jordan P., Fromme P., Witt H.-T., Klukas O., Saenger W., and Krauss N. Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411 (2001) 909-917
7. Byrdin M., Jordan P., Krauss N., Fromme P., Stehlik D., and Schlodder E. Light harvesting in photosystem I: modeling based on the 2.5 Å structure of photosystem I from Synechococcus elongatus. Biophys. J. 83 (2002) 433-457
8. Ben-Shem A., Frolow F., and Nelson N. Crystal structure of plant photosystem I. Nature 426 (2003) 630-635
9. Zouni A., Witt H.-T., Kern J., Fromme P., Krauss N., Saenger W., and Orth P. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409 (2001) 739-743
10. Fereira K.N., Iverson T.M., Maghlaoui K., Barber J., and Iwata S. Architecture of the photosynthetic oxygen-evolving center. Science 303 (2004) 1831-1838
11. Loll B., Kern J., Saenger W., Zouni A., and Biesiadka J. Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438 (2005) 1040-1044
12. Loll B., Kern J., Zouni A., Saenger W., Biesiadka J., and Irrgang K.-D. The antenna system of photosystem II from Thermosynechococus elongatus at 3.2 Å resolution. Photosynth. Res. 86 (2005) 175-184
13. Guskov A., Kern J., Gabdulkhakov A., Broser M., Zouni A., and Saenger W. Cyanobacterial photosystem II at 2.9 Å resolution: role of quinones, lipids, channels and chloride. Nat. Struct. Mol. Biol. 16 (2009) 334-342
14. Roszak A.W., Howard T.D., Southwall J., Gardiner A.T., Law C.J., Isaacs N.W., and Cogdell R.J. Crystal structure of the RC-LH 1 core complex from Rhodopseudomonas palustris. Science 302 (2003) 1969-1972
15. Bahatyrova S., Frese R.N., Siebert C.A., Olsen J.D., van der Werf K., van Grondelle R., Niederman R.A., Bullough P.A., Otto C., and Hunter C.N. The native architecture of a photosynthetic membrane. Nature 430 (2004) 1058-1062
16. McDermott G., Prince S.M., Freer A.A., Hawthornthwaite-Lawless A.M., Papiz M.Z., Cogdell R.J., and Isaacs N.W. Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374 (1995) 517-521
17. Koepke J., Hu X., Muencke C., Schulten K., and Michel H. The crystal structure of the light-harvesting complex II (B800-850) from Rhodospirillum molischianum. Structure 4 (1996) 581-597
18. Papiz M.Z., Prince S.M., Howard T., Cogdell R.J., and Isaacs N.W. The structure and thermal motion of the B800-850 LH2 complex from Rps. acidophila at 2.0 Å resolution and 100K: new structural features and functionally relevant motions. J. Mol. Biol. 326 (2003) 1523-1538
19. Zhao K.-H., Su P., Tu J.-M., Wang X., Liu H., Plöscher M., Eichacker L., Yang B., Zhou M., and Scheer H. Phycobilin:cystein 84 biliprotein lyase, a near-universal lyase for cystein-84-binding sites in cyanobacterial phycobiliproteins. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 14300-14305 and further references therein
20. 13C-enriched chlorosomes and isolated bacteriochlorophyll-c aggregates of Chlorobium tepidum: the self-organization of pigments is the main structural feature of chlorosomes. Biochemistry 34 (1995) 15259-15266
21. van Rossum B.-J., Stensgaard D.B., Mulder F.M., Boender G.-J., Schaffner K., Holzwarth A.R., and de Groot H.J.M. A refined model of the chlorosomal antennae of the green bacterium Chorobium tepidum from proton chemical shift constraints obtained with high-field 2-D and 3-D MAS NMR dipolar correlation spectroscopy. Biochemistry 40 (2001) 1587-1595
22. Pšenčik J., Ikonen T.P., Laurinmäki P., Merckel M.C., Butcher S.J., Serimaa R.E., and Tuma R. Lamellar organization of pigments in chlorosomes, the light harvesting complexes of green photosynthetic bacteria. Biophys. J. 87 (2004) 1165-1172
23. Balaban T.S. Tailoring porphyrins and chlorins for self-assembly in biomimetic artificial antenna systems. Acc. Chem. Res. 38 (2005) 612-623
24. Jochum T., Reddy C.M., Eichhöfer A., Buth G., Szmytkowski J., Kalt H., Moss D., and Balaban T.S. The supramolecular organization of self-assembling chlorosomal bacteriochlorophyll c, d, or e mimics. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 12736-12741
25. 25Mg NMR. Biochemistry 48 (2009) 74-86
26. Kühlbrandt W., Wang D.N., and Fujiyoshi Y. Atomic model of plant light-harvesting complex by electron crystallography. Nature 367 (1994) 614-621
27. Liu Z., Yan H., Wang K., Kuang J., Gui L., An X., and Chang W. Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428 (2004) 287-292
28. Standfu J., Terwisscha van Scheltinga A.C., Lamborghini M., and Kühlbrandt W. Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 Å resolution. EMBO J. 24 (2005) 919-928
29. 6f complex. Nature 426 (2003) 413-418
30. 6f complex of oxygenic photosynthesis: tuning the cavity. Science 392 (2003) 1009-1014
31. Balaban T.S., Fromme P., Holzwarth A.R., Krauβ N., and Prokhorenko V.I. Relevance of the diastereotopic ligation of magnesium atoms in chlorophylls in Photosystem I. Biochim. Biophys. Acta (Bioenergetics) 1556 (2002) 197-207
32. Balaban T.S. Are syn-ligated (bacterio)chlorophyll dimers energetic traps in light-harvesting systems?. FEBS Lett. 545 (2003) 97-102 Erratum FEBS Lett. 547 (2003) 235
33. Balaban T.S. Relevance of the diastereotopic ligation of magnesium atoms of chlorophylls in the major light-harvesting complex II (LHC II) of higher plants. Photosynth. Res. 86 (2005) 251-262
34. Oba T., and Tamiaki H. Coordination chemistry of chlorophylls: which side of the chlorin macrocycle is favored for the ligand coordination?. J. Photosci. 9 (2002) 362-363
35. Oba T., and Tamiaki H. Which side of the π-macrocycle plane of (bacterio)chlorophylls is favored for binding of the fifth ligand?. Photosynth. Res. 74 (2002) 1-10
36. Oba T., and Tamiaki H. Effects of peripheral substituents on diastereoselectivity of the fifth ligand-binding to chlorophylls, and nomenclature of the asymmetric axial coordination sites. Bioorg. Med. Chem. 13 (2005) 5733-5739
37. Garcia-Martin A., Kwa L.G., Strohmann B., Robert B., Holzwarth A.R., and Braun P. Structural role of bacteriochlorophyll ligated in the energetically unfavourable β-position in light harvesting complex. J. Biol. Chem. 281 (2006) 1062610634
38. Christiansen O., Koch H., and Jørgensen P. The second-order approximate coupled cluster singles and doubles model CC2. Chem. Phys. Lett. 243 (1995) 409-418
39. Head-Gordon M., Rico R.J., Omu M., and Lee T.J. A doubles correction to excited states from configuration-interaction in the space of single substitutions. Chem. Phys. Lett. 219 (1994) 21-29
40. Hättig C., and Weigend F. CC2 excitation energy calculations on large molecules using the resolution of the identity approximation. J. Chem. Phys. 113 (2000) 5154-5161
41. Hättig C., Hellweg A., and Köhn A. Distributed memory parallel implementation of energies and gradients for second-order Møller-Plesset perturbation theory with the resolution-of-the-identity approximation. Phys. Chem. Chem. Phys. 8 (2006) 1159-1169
42. Ahlrichs R., Bär M., Häser M., Horn H., and Kömel C. Electronic structure calculations on workstation computers: the program system Turbomole. Chem. Phys. Lett. 162 (1989) 164-169
43. Weigend F., Köhn A., and Hättig C. Efficient use of the correlation consistent basis sets in resolution of the identity MP2 calculations. J. Chem. Phys. 116 (2002) 3175-3183
44. Sundholm D. Density functional theory calculations of the visible spectrum of chorophyll a. Chem. Phys. Lett. (1999) 480-484
45. Pullerits T., and Sundstrom V. Photosynthetic light-harvesting pigment-protein complexes: toward understanding how and why. Acc. Chem. Res. 29 (1996) 381-389
46. Cai Z.-L., Crossley M.J., Reimers J.R., Kobayashi R., and Amos R.D. Density functional theory for charge transfer: the nature of the N-Bands of porphyrins and chlorophylls revealed through CAM-B3LYP, CASPT2, and SAC-CI calculations. J. Phys. Chem. B 110 (2006) 15623-15624
47. T.S. Balaban, High-five for magnesium complex, Chemical & Engineering News (ACS) May 16 (2005) 6.
48. Heimdal J., Jensen K.P., Devarajan A., and Ryde U. The role of axial ligands for the structure and function of chlorophylls. J. Biol. Inorg. Chem. 12 (2007) 49-61
49. Hoober J.K., Eggink L.L., and Chen M. Chlorophylls, ligands and assembly of light-harvesting complexes in chloroplasts. Photosynth. Res. 94 (2007) 387-400
50. Müh F., El-Amine Madjet M., Adolphs J., Abdurahman A., Rabenstein B., Ishikita H., Knapp E.-W., and Renger T. α-Helices direct excitation energy flow in the Fenna-Matthews-Olson protein. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 16862-16867
51. Kasha M., Rawls H.R., and Ashraf El-Bayaoumi M. The exciton model in molecular spectroscopy. Pure Appl. Chem. 11 (1965) 371-392
52. HyperChem 7.01 Programme Package, HyperCube Inc., Gainesville, Florida 32601, USA.
53. Murray J.W., Duncan J., and Barber J. CP43-like chlorophyll binding proteins: structural and evolutionary implications. Trends Plant Sci. 11 (2006) 152-157
54. Raszewski G., and Renger T. Light harvesting in photosystem II core complexes is limited by the transfer to the trap: can the core complex turn into a photoprotective mode?. J. Am. Chem. Soc. 130 (2008) 4431-4446
55. Shen G., and Vermaas W.F.J. Mutation of chlorophyll ligands in the chlorophyll-binding CP47 protein as studied in a Synechocystis sp. PCC 6803 photosystem I-less background. Biochemistry 33 (1994) 7379-7388
56. Tracewell C.A., and Brudvig G.W. Multiple redox-active chlorophylls in the secondary electron-transfer pathways of oxygen-evolving photosystem II. Biochemistry 47 (2008) 11559-11572
57. Kyu Ahn T., Avenson T.J., Ballottari M., Cheng Y.-C., Niyogi K.K., Bassi R., and Fleming G.R. Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320 (2008) 794-797