Photosynthesis Research

, Volume 111, Issue 1–2, pp 87–101 | Cite as

Structure-based simulation of linear optical spectra of the CP43 core antenna of photosystem II

  • Frank Müh
  • Mohamed El-Amine Madjet
  • Thomas Renger
Regular Paper


The linear optical spectra (absorbance, linear dichroism, circular dichroism, fluorescence) of the CP43 (PsbC) antenna of the photosystem II core complex (PSIIcc) pertaining to the S0 → S1 (QY) transitions of the chlorophyll (Chl) a pigments are simulated by applying a combined quantum chemical/electrostatic method to obtain excitonic couplings and local transition energies (site energies) on the basis of the 2.9 Å resolution crystal structure (Guskov et al., Nat Struct Mol Biol 16:334–342, 2009). The electrostatic calculations identify three Chls with low site energies (Chls 35, 37, and 45 in the nomenclature of Loll et al. (Nature 438:1040–1044, 2005). A refined simulation of experimental spectra of isolated CP43 suggests a modified set of site energies within 143 cm−1 of the directly calculated values (root mean square deviation: 80 cm−1). In the refined set, energy sinks are at Chls 37, 43, and 45 in agreement with earlier fitting results (Raszewski and Renger, J Am Chem Soc 130:4431–4446, 2008). The present structure-based simulations reveal that a large part of the redshift of Chl 37 is due to a digalactosyldiacylglycerol lipid. This finding suggests a new role for lipids in PSIIcc, namely the tuning of optical spectra and the creation of an excitation energy funnel towards the reaction center. The analysis of electrostatic pigment–protein interactions is used to identify amino acid residues that are of potential interest for an experimental approach to an assignment of site energies and energy sinks by site-directed mutagenesis.


Chlorophyll Electrostatic interaction Excitation energy transfer Lipids Mutagenesis Optical spectra 







Density functional theory




Extended dipole


Excitation energy transfer


Electrostatic potential






Nonphotochemical hole-burning


Point dipole




Pigment–protein complex


Photosystem I core complex


Photosystem II core complex




Reaction center




Time-dependent DFT


Transition charges from electrostatic potential


Exchange correlation



We thank G. Kieseritzky, B. Rabenstein, and E. W. Knapp for providing TAPBS and Karlsberg 2.0. This work was financed by the Deutsche Forschungsgemeinschaft through Sonderforschungsbereich 429 (TP A9). F.M. appreciates a research fellowship by the JKU Linz in November 2010.


  1. Adolphs J, Müh F, Madjet ME, Renger T (2008) Calculation of pigment transition energies in the FMO protein. Photosynth Res 95:197–209PubMedCrossRefGoogle Scholar
  2. Adolphs J, Müh F, Madjet ME, Schmidt am Busch M, Renger T (2010) Structure-based calculations of optical spectra of photosystem I suggest an asymmetric light-harvesting process. J Am Chem Soc 132:3331–3343PubMedCrossRefGoogle Scholar
  3. Alfonso M, Montoya G, Cases R, Rodríguez R, Picorel R (1994) Core antenna complexes, CP43 and CP47, of higher plant photosystem II. Spectral properties, pigment stoichiometry, and amino acid composition. Biochemistry 33:10494–10500PubMedCrossRefGoogle Scholar
  4. Baicu SC, Taylor MJ (2002) Acid-base buffering in organ preservation solutions as a function of temperature: new parameters for comparing buffer capacity and efficiency. Cryobiology 45:33–48PubMedCrossRefGoogle Scholar
  5. Bashford D (2004) Macroscopic electrostatic models for protonation states in proteins. Front Biosci 9:1082–1099PubMedCrossRefGoogle Scholar
  6. Bricker TM (1990) The structure and function of CPa-1 and CPa-2 in photosystem II. Photosynth Res 24:1–13CrossRefGoogle Scholar
  7. Bricker TM, Frankel LK (2002) The structure and function of CP47 and CP43 in photosystem II. Photosynth Res 72:131–146PubMedCrossRefGoogle Scholar
  8. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, Karplus M (1983) CHARMM—a program for macromolecular energy, minimization, and dynamics calculations. J Comput Chem 4:187–217CrossRefGoogle Scholar
  9. Brooks BR, Brooks CL, Mackerell AD, Nilsson L, Petrella RJ, Roux B, Won Y, Archontis G, Bartels C, Boresch S, Caflisch A, Caves L, Cui Q, Dinner AR, Feig M, Fischer S, Gao J, Hodoscek M, Im W, Kuczera K, Lazaridis T, Ma J, Ovchinnikov V, Paci E, Pastor RW, Post CB, Pu JZ, Schaefer M, Tidor B, Venable RM, Woodcock HL, Wu X, Yang W, York DM, Karplus M (2009) CHARMM: the biomolecular simulation program. J Comput Chem 30:1545–1614PubMedCrossRefGoogle Scholar
  10. Casazza AP, Szczepaniak M, Müller MG, Zucchelli G, Holzwarth AR (2010) Energy transfer processes in the isolated core antenna complexes CP43 and CP47 of photosystem II. Biochim Biophys Acta 1797:1606–1616PubMedCrossRefGoogle Scholar
  11. Dang NC, Zazubovich V, Reppert M, Neupane B, Picorel R, Seibert M, Jankowiak R (2008) The CP43 proximal antenna complex of higher plant photosystem II revisited: modeling and hole burning study. I. J Phys Chem B 112:9921–9933PubMedCrossRefGoogle Scholar
  12. DeCoursey TE, Cherny VV (1998) Temperature dependence of voltage-gated H+ currents in human neutrophils, rat alveolar epithelial cells, and mammalian phagocytes. J Gen Physiol 112:503–522PubMedCrossRefGoogle Scholar
  13. Douzou P (1977) Cryobiochemistry. Academic Press, LondonGoogle Scholar
  14. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838PubMedCrossRefGoogle Scholar
  15. Green BR, Parson WW (eds) (2003) Light-harvesting antennas in photosynthesis. Advances in phothosynthesis and respiration. Springer (Kluwer Academic Publishers), Dordrecht, The NetherlandsGoogle Scholar
  16. Groot ML, Frese RN, de Weerd FL, Bromek K, Pettersson A, Peterman EJG, van Stokkum IHM, van Grondelle R, Dekker JP (1999) Spectroscopic properties of the CP43 core antenna protein of photosystem II. Biophys J 77:3328–3340PubMedCrossRefGoogle Scholar
  17. Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342PubMedCrossRefGoogle Scholar
  18. Guskov A, Gabdulkhakov A, Broser M, Glöckner C, Hellmich J, Kern J, Frank J, Müh F, Saenger W, Zouni A (2010) Recent progress in the crystallographic studies of photosystem II. ChemPhysChem 11:1160–1171PubMedCrossRefGoogle Scholar
  19. Hirata S, Head-Gordon M (1999) Time-dependent density functional theory within the Tamm-Dancoff approximation. Chem Phys Lett 314:291–299CrossRefGoogle Scholar
  20. Hughes JL, Prince BJ, Arsköld SP, Krausz E, Pace RJ, Picorel R, Seibert M (2004) Photo-conversion of chlorophylls in higher-plant CP43 characterized by persistent spectral hole burning at 1.7 K. J Lumin 108:131–136CrossRefGoogle Scholar
  21. Hughes JL, Picorel R, Seibert M, Krausz E (2006) Photophysical behavior and assignment of the low-energy chlorophyll states in the CP43 proximal antenna protein of higher plant photosystem II. Biochemistry 45:12345–12357PubMedCrossRefGoogle Scholar
  22. Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graphics 14:33–38CrossRefGoogle Scholar
  23. Ishikita H, Knapp EW (2003) Redox potential of quinones in both electron transfer branches of photosystem I. J Biol Chem 278:52002–52011PubMedCrossRefGoogle Scholar
  24. Ishikita H, Loll B, Biesiadka J, Kern J, Irrgang KD, Zouni A, Saenger W, Knapp EW (2007) Function of two β-carotenes near the D1 and D2 proteins in photosystem II dimers. Biochim Biophys Acta 1767:79–87PubMedCrossRefGoogle Scholar
  25. Jankowiak R, Hayes JM, Small GJ (1993) Spectral hole-burning spectroscopy in amorphous molecular solids and proteins. Chem Rev 93:1471–1502CrossRefGoogle Scholar
  26. Jankowiak R, Zazubovich V, Rätsep M, Matsuzaki S, Alfonso M, Picorel R, Seibert M, Small GJ (2000) The CP43 core antenna complex of photosystem II possesses two quasi-degenerate and weakly coupled Qy-trap states. J Phys Chem B 104:11805–11815CrossRefGoogle Scholar
  27. Kieseritzky G, Knapp EW (2008) Optimizing pKA computation in proteins with pH adapted conformations. Proteins 71:1335–1348PubMedCrossRefGoogle Scholar
  28. Knox RS, Spring BQ (2003) Dipole strengths in the chlorophylls. Photochem Photobiol 77:497–501PubMedCrossRefGoogle Scholar
  29. Kong J, White CA, Krylov AI, Sherrill D, Adamson RD, Furlani TR, Lee MS, Lee AM, Gwaltney SR, Adams TR, Ochsenfeld C, Gilbert ATB, Kedziora GS, Rassolov VA, Maurice DR, Nair N, Shao YH, Besley NA, Maslen PE, Dombroski JP, Daschel H, Zhang WM, Korambath PP, Baker J, Byrd EFC, Van Voorhis T, Oumi M, Hirata S, Hsu CP, Ishikawa N, Florian J, Warshel A, Johnson BG, Gill PMW, Head-Gordon M, Pople JA (2000) Q-chem 2.0: a high-performance ab initio electronic structure program package. J Comput Chem 21:1532–1548CrossRefGoogle Scholar
  30. Krueger BP, Scholes GD, Fleming GR (1998) Calculation of couplings and energy-transfer pathways between the pigments of LH2 by the ab initio transition density cube method. J Phys Chem B 102:5378–5386CrossRefGoogle Scholar
  31. Lambrev PH, Várkonyi Z, Krumova S, Kovács L, Miloslavina Y, Holzwarth AR, Garab G (2007) Importance of trimer-trimer interactions for the native state of the plant light-harvesting complex II. Biochim Biophys Acta 1767:847–853PubMedCrossRefGoogle Scholar
  32. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040–1044PubMedCrossRefGoogle Scholar
  33. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2007) Lipids in photosystem II: interactions with protein and cofactors. Biochim Biophys Acta 1767:509–519PubMedCrossRefGoogle Scholar
  34. MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau FTK, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher WE, Roux B, Schlenkrich M, Smith JC, Stote R, Straub J, Watanabe M, Wiorkiewicz-Kuczera J, Yin D, Karplus M (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102:3586–3616CrossRefGoogle Scholar
  35. Madjet ME, Abdurahman A, Renger T (2006) Intermolecular Coulomb couplings from ab initio electrostatic potentials: application to optical transitions of strongly coupled pigments in photosynthetic antennae and reaction centers. J Phys Chem B 110:17268–17281PubMedCrossRefGoogle Scholar
  36. Madjet ME, Müh F, Renger T (2009) Deciphering the influence of short-range electronic couplings on optical properties of molecular dimers: application to “special pairs” in photosynthesis. J Phys Chem B 113:12603–12614CrossRefGoogle Scholar
  37. Müh F, Zouni A (2008) Micelle formation in the presence of photosystem I. Biochim Biophys Acta 1778:2298–2307PubMedCrossRefGoogle Scholar
  38. Müh F, Madjet ME, Adolphs J, Abdurahman A, Rabenstein B, Ishikita H, Knapp EW, Renger T (2007) α-Helices direct excitation energy flow in the Fenna-Matthews-Olson protein. Proc Natl Acad Sci USA 104:16862–16867PubMedCrossRefGoogle Scholar
  39. Müh F, Renger T, Zouni A (2008) Crystal structure of cyanobacterial photosystem II at 3.0 Å resolution: a closer look at the antenna system and the small membrane-intrinsic subunits. Plant Physiol Biochem 46:238–264PubMedCrossRefGoogle Scholar
  40. Müh F, Madjet ME, Renger T (2010a) Spectral simulation of the CP47 core antenna of photosystem II based on the 2.9 Å structure. In: 15th International Congress of Photosynthesis, Beijing, ChinaGoogle Scholar
  41. Müh F, Madjet ME, Renger T (2010b) Structure-based identification of energy sinks in plant light-harvesting complex II. J Phys Chem B 114:13517–13535PubMedCrossRefGoogle Scholar
  42. Neugebauer J (2009) Subsystem-Based Theoretical Spectroscopy of Biomolecules and Biomolecular Assemblies. ChemPhysChem 10:3148–3173PubMedCrossRefGoogle Scholar
  43. Novoderezhkin VI, Palacios MA, van Amerongen H, van Grondelle R (2005) Excitation dynamics in the LHCII complex of higher plants: modeling based on the 2.72 Å crystal structure. J Phys Chem B 109:10493–10504PubMedCrossRefGoogle Scholar
  44. Rabenstein B, Knapp EW (2001) Calculated pH-dependent population and protonation of carbon-monoxy-myoglobin conformers. Biophys J 80:1141–1150PubMedCrossRefGoogle Scholar
  45. Raszewski G, Renger T (2008) 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 130:4431–4446PubMedCrossRefGoogle Scholar
  46. Renger T (2004) Theory of optical spectra involving charge transfer states: dynamic localization predicts a temperature dependent optical band shift. Phys Rev Lett 93:188101PubMedCrossRefGoogle Scholar
  47. Renger G (ed) (2008) Primary processes of photosynthesis, principles and apparatus. Royal Society Chemistry Publishing, CambridgeGoogle Scholar
  48. Renger T (2009) Theory of excitation energy transfer: from structure to function. Photosynth Res 102:471–485PubMedCrossRefGoogle Scholar
  49. Renger T, Marcus RA (2002) On the relation of protein dynamics and exciton relaxation in pigment-protein complexes: an estimation of the spectral density and a theory for the calculation of optical spectra. J Chem Phys 116:9997–10019CrossRefGoogle Scholar
  50. Renger G, Renger T (2008) Photosystem II: the machinery of photosynthetic water splitting. Photosynth Res 98:53–80PubMedCrossRefGoogle Scholar
  51. Renger T, Schlodder E (2010) Primary photophysical processes in photosystem II: bridging the gap between crystal structure and optical spectra. ChemPhysChem 11:1141–1153PubMedCrossRefGoogle Scholar
  52. Renger T, Madjet ME, Müh F, Trostmann I, Schmitt FJ, Theiss C, Paulsen H, Eichler HJ, Knorr A, Renger G (2009) Thermally activated superradiance and intersystem crossing in the water-soluble chlorophyll binding protein. J Phys Chem B 113:9948–9957PubMedCrossRefGoogle Scholar
  53. Renger T, Madjet ME, Knorr A, Müh F (2011) How the molecular structure determines the flow of excitation energy in plant light-harvesting complex II. J Plant Physiol 168:1497–1509PubMedCrossRefGoogle Scholar
  54. Reppert M, Zazubovich V, Dang NC, Seibert M, Jankowiak R (2008) Low-energy chlorophyll states in the CP43 antenna protein complex: simulation of various optical spectra. II. J Phys Chem B 112:9934–9947PubMedCrossRefGoogle Scholar
  55. Schmidt am Busch M, Müh F, Madjet ME, Renger T (2011) The eighth bacteriochlorophyll completes the excitation energy funnel in the FMO protein. J Phys Chem Lett 2:93–98CrossRefGoogle Scholar
  56. Schulze H, Ristau O, Jung C (1994) The proton activity at cryogenic temperatures—a possible influence on the spin-state of the heme iron of cytochrome P-450(Cam) in supercooled buffered solutions. Biochim Biophys Acta 1183:491–498PubMedCrossRefGoogle Scholar
  57. Seemann H, Winter R, Royer CA (2001) Volume, expansivity and isothermal compressibility changes associated with temperature and pressure unfolding of staphylococcal nuclease. J Mol Biol 307:1091–1102PubMedCrossRefGoogle Scholar
  58. Sigfridsson E, Ryde U (1998) Comparison of methods for deriving atomic charges from the electrostatic potential and moments. J Comput Chem 19:377–395CrossRefGoogle Scholar
  59. Tremolieres A, Dainese P, Bassi R (1994) Heterogenous lipid distribution among chlorophyll-binding proteins of photosystem II in maize mesophyll chloroplasts. Eur J Biochem 221:721–730PubMedCrossRefGoogle Scholar
  60. Ullmann GM, Knapp EW (1999) Electrostatic models for computing protonation and redox equilibria in proteins. Eur Biophys J 28:533–551PubMedCrossRefGoogle Scholar
  61. Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60PubMedCrossRefGoogle Scholar
  62. van Amerongen H, Croce R (2008) Structure and function of photosystem II light-harvesting proteins (Lhcb) of higher plants. In: Renger G (ed) Primary processes of photosynthesis, principles and apparatus, vol 1. RSC Publishing, Cambridge, pp 329–367Google Scholar
  63. Vasil’ev S, Bruce D (2006) A protein dynamics study of photosystem II: the effects of protein conformation on reaction center function. Biophys J 90:3062–3073PubMedCrossRefGoogle Scholar
  64. Yang M, Damjanovic A, Vaswani HM, Fleming GR (2003) Energy transfer in photosystem I of cyanobacteria Synechococcus elongatus: model study with structure-based semi-empirical Hamiltonian and experimental spectral density. Biophys J 85:140–158PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Frank Müh
    • 1
  • Mohamed El-Amine Madjet
    • 2
  • Thomas Renger
    • 1
  1. 1.Institut für Theoretische PhysikJohannes Kepler Universität LinzLinzAustria
  2. 2.Center for Free-Electron Laser Science/DESYHamburgGermany

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