Photosynthesis Research

, Volume 137, Issue 2, pp 215–226 | Cite as

The role of charge-transfer states in the spectral tuning of antenna complexes of purple bacteria

  • Michele Nottoli
  • Sandro Jurinovich
  • Lorenzo Cupellini
  • Alastair T. Gardiner
  • Richard Cogdell
  • Benedetta MennucciEmail author
Original Article


The LH2 antenna complexes of purple bacteria occur, depending on light conditions, in various different spectroscopic forms, with a similar structure but different absorption spectra. The differences are related to point changes in the primary amino acid sequence, but the molecular–level relationship between these changes and the resulting spectrum is still not well understood. We undertook a systematic quantum chemical analysis of all the main factors that contribute to the exciton structure, looking at how the environment modulates site energies and couplings in the B800–850 and B800–820 spectroscopic forms of LH2. A multiscale approach combining quantum chemistry and an atomistic classical embedding has been used where mutual polarization effects between the two parts are taken into account. We find that the loss of hydrogen bonds following amino acid changes can only explain a part of the observed blue-shift in the B850 band. The coupling of excitonic states to charge-transfer states, which is different in the two forms, contributes with a similar amount to the overall blue-shift.


Excitonic model Antenna complex Quantum chemistry 



The authors are grateful to Dr. Aleksander W. Roszak for having provided the high-resolution X-ray structure of B800–850 complex. ATG and RJC gratefully acknowledge funding from the Photosynthetic Antenna Research Center, an Energy Frontier Research Center funded by the DOE, Office of Science, Office of Basic Energy Sciences under Award Number DE-SC 0001035.

Supplementary material

11120_2018_492_MOESM1_ESM.pdf (901 kb)
Supplementary material 1 (PDF 901 KB)


  1. Aagaard J, Sistrom WR (1972) Control of synthesis of reaction center bacteriochlorophyll in photosynthetic bacteria. Photochem Photobiol 15(2):209. CrossRefPubMedGoogle Scholar
  2. Anda A, De Vico L, Hansen T (2017) Intermolecular modes between LH2 bacteriochlorophylls and protein residues: the effect on the excitation energies. J Phys Chem B 121(22):5499. CrossRefPubMedGoogle Scholar
  3. Caricato M, Mennucci B, Tomasi J, Ingrosso F, Cammi R, Corni S, Scalmani G (2006) Formation and relaxation of excited states in solution: a new time dependent polarizable continuum model based on time dependent density functional theory. J Chem Phys 124(12):124520. CrossRefPubMedGoogle Scholar
  4. Case DA, Babin V, Berryman JT, Betz RM, Cai Q, Cerutti DS, Cheatham TE, Darden TA, Duke RE, Gohlke H, Goetz AW, Gusarov S, Homeyer N, Janowski P, Kaus J, Kolossváry I, Kovalenko A, Lee TS, LeGrand S, Luchko T, Luo R, Madej B, Merz KM, Paesani F, Roe DR, Roitberg A, Sagui C, Salomon-Ferrer R, Seabra G, Simmerling CL, Smith W, Swails J, Walker Wang J, Wolf RM, Wu X, Kollman PA (2014) Amber 14. University of California, San FranciscoGoogle Scholar
  5. Ceccarelli M, Procacci P, Marchi M (2003) An ab initio force field for the cofactors of bacterial photosynthesis. J Comput Chem 24(2):129. CrossRefPubMedGoogle Scholar
  6. Chmeliov J, Songaila E, Rancova O, Gall A, Robert B, Abramavicius D, Valkunas L (2013) Excitons in the LH3 complexes from purple bacteria. J Phys Chem B 117(38):11058. CrossRefPubMedGoogle Scholar
  7. Chung LW, Hirao H, Li X, Morokuma K (2011) The ONIOM method: its foundation and applications to metalloenzymes and photobiology. Wiley Interdisc Rev 2(2):327Google Scholar
  8. Cogdell RJ, Durant I, Valentine J, Lindsay J, Schmidt K (1983) The isolation and partial characterisation of the light-harvesting pigment-protein complement of Rhodopseudomonas acidophila. Biochim Biophys Acta - Bioenerg 722(3):427. CrossRefGoogle Scholar
  9. Cogdell RJ, Gall A, Köhler J (2006) The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes. Q Rev Biophys 39(3):227. CrossRefPubMedGoogle Scholar
  10. Cupellini L, Jurinovich S, Campetella M, Caprasecca S, Guido CA, Kelly SM, Gardiner AT, Cogdell R, Mennucci B (2016) An ab initio description of the excitonic properties of LH2 and their temperature dependence. J Phys Chem B 120(44):11348. CrossRefPubMedGoogle Scholar
  11. Curutchet C, Kongsted J, Muñoz-Losa A, Hossein-Nejad H, Scholes GD, Mennucci B (2011) Photosynthetic light-harvesting is tuned by the heterogeneous polarizable environment of the protein. J Am Chem Soc 133(9):3078CrossRefPubMedGoogle Scholar
  12. Curutchet C, Mennucci B (2017) Quantum chemical studies of light harvesting. Chem Rev 117(2):294CrossRefPubMedGoogle Scholar
  13. Curutchet C, Muñoz Losa A, Monti S, Kongsted J, Scholes GD, Mennucci B (2009) Electronic energy transfer in condensed phase studied by a polarizable QM/MM model. J Chem Theor Comput 5:1838. CrossRefGoogle Scholar
  14. Curutchet C, Scholes GD, Mennucci B, Cammi R (2007) How solvent controls electronic energy transfer and light harvesting: toward a quantum-mechanical description of reaction field and screening effects. J Phys Chem B 111(46):13253. CrossRefPubMedGoogle Scholar
  15. de Ruijter W, Segura J, Cogdell R, Gardiner A, Oellerich S, Aartsma T (2007) Fluorescence-emission spectroscopy of individual LH2 and LH3 complexes. Chem Phys 341(1–3):320CrossRefGoogle Scholar
  16. Dreuw A, Weisman JL, Head-Gordon M (2003) Long-range charge-transfer excited states in time-dependent density functional theory require non-local exchange. J Chem Phys 119(6):2943. CrossRefGoogle Scholar
  17. Ferretti M, Hendrikx R, Romero E, Southall J, Cogdell RJ, Novoderezhkin VI, Scholes GD, van Grondelle R (2016) Dark states in the light-harvesting complex 2 revealed by two-dimensional electronic spectroscopy. Sci Rep 6:20834. CrossRefPubMedPubMedCentralGoogle Scholar
  18. Fowler GJ, Sockalingum GD, Robert B, Hunter CN (1994) Blue shifts in bacteriochlorophyll absorbance correlate with changed hydrogen bonding patterns in light-harvesting 2 mutants of Rhodobacter sphaeroides with alterations at alpha-Tyr-44 and alpha-Tyr-45. Biochem J 299:695CrossRefPubMedPubMedCentralGoogle Scholar
  19. Fowler GJS, Visschers RW, Grief GG, van Grondelle R, Hunter CN (1992) Genetically modified photosynthetic antenna complexes with blueshifted absorbance bands. Nature 355:848. CrossRefPubMedGoogle Scholar
  20. Freiberg A, Timpmann K, Trinkunas G (2010) Spectral fine-tuning in excitonically coupled cyclic photosynthetic antennas. Chem Phys Lett 500(1–3):111. CrossRefGoogle Scholar
  21. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Scalmani G, Barone V, Petersson GA, Nakatsuji H, Li X, Caricato M, Marenich AV, Bloino J, Janesko BG, Gomperts R, Mennucci B, Hratchian HP, Ortiz JV, Izmaylov AF, Sonnenberg JL, Williams-Young D, Ding F, Lipparini F, Egidi F, Goings J, Peng B, Petrone A, Henderson T, Ranasinghe D, Zakrzewski VG, Gao J, Rega N, Zheng G, Liang W, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Vreven T, Throssell K, Montgomery Jr JA, Peralta JE, Ogliaro F, Bearpark MJ, Heyd JJ, Brothers EN, Kudin KN, Staroverov VN, Keith TA, Kobayashi R, Normand J, Raghavachari K, Rendell AP, Burant JC, Iyengar SS, Tomasi J, Cossi M, Millam JM, Klene M, Adamo C, Cammi R, Ochterski JW, Martin RL, Morokuma K, Farkas O, Foresman JB, Fox DJ (2016) Gaussian 16 Revision A.03. Gaussian Inc. Wallingford CTGoogle Scholar
  22. Gardiner AT, Cogdell RJ, Takaichi S (1993) The effect of growth conditions on the light-harvesting apparatus in Rhodopseudomonas acidophila. Photosynth Res 38(2):159CrossRefPubMedGoogle Scholar
  23. Guareschi R, Valsson O, Curutchet C, Mennucci B, Filippi C (2016) Electrostatic versus resonance interactions in photoreceptor proteins: the case of rhodopsin. J Phys Chem Lett 7(22):4547. CrossRefPubMedGoogle Scholar
  24. Guarnetti-Prandi I, Viani L, Andreussi O, Mennucci B (2016) Combining classical molecular dynamics and quantum mechanical methods for the description of electronic excitations: the case of carotenoids. J Comput Chem 37(11):981. CrossRefGoogle Scholar
  25. Gudowska-Nowak E, Newton MD, Fajer J (1990) Conformational and environmental effects on bacteriochlorophyll optical spectra: correlations of calculated spectra with structural results. J Phys Chem 94(15):5795CrossRefGoogle Scholar
  26. Guido CA, Jacquemin D, Adamo C, Mennucci B (2015) Electronic excitations in solution: the interplay between state specific approaches and a time-dependent density functional theory description. J Chem Theor Comput 11(12):5782. CrossRefGoogle Scholar
  27. Henry SL, Cogdell RJ (2013) The evolution of the purple photosynthetic bacterial light-harvesting system. Adv Bot Res 66:205. CrossRefGoogle Scholar
  28. Higashi M, Kosugi T, Hayashi S, Saito S (2014) Theoretical study on excited states of bacteriochlorophyll a in solutions with density functional assessment. J Phys Chem B 118(37):10906. CrossRefPubMedGoogle Scholar
  29. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, Simmerling C (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins Struct Funct Bioinforma 65(3):712. CrossRefGoogle Scholar
  30. Hsu Cp, You ZQ, Chen HC (2008) Characterization of the short-range couplings in excitation energy transfer. J Phys Chem C 112(4):1204. CrossRefGoogle Scholar
  31. Iozzi MF, Mennucci B, Tomasi J, Cammi R (2004) Excitation energy transfer (EET) between molecules in condensed matter: a novel application of the polarizable continuum model (PCM). J Chem Phys 120(15):7029. CrossRefPubMedGoogle Scholar
  32. Jang S, Rivera E, Montemayor D (2015) Molecular level design principle behind optimal sizes of photosynthetic LH2 complex: taming disorder through cooperation of hydrogen bonding and quantum delocalization. J Phys Chem Lett 6(6):928CrossRefPubMedGoogle Scholar
  33. Jurinovich S, Cupellini L, Guido CA, Mennucci B (2018) EXAT: EXcitonic analysis tool. J Comput Chem 39(5):279. CrossRefPubMedGoogle Scholar
  34. Kaplan S (1978) Control and kinetics of photosynthetic membrane development. In: Clayton RK, Sistrom WR (eds) The photosynthetic bacteria. Plenum Press, New York, pp 809–839Google Scholar
  35. Li X, Parrish RM, Liu F, Kokkila Schumacher SIL, Martínez TJ (2017) An ab initio exciton model including charge-transfer excited states. J Chem Theor Comput 13(8):3493. CrossRefGoogle Scholar
  36. Magdaong NM, LaFountain AM, Greco JA, Gardiner AT, Carey AM, Cogdell RJ, Gibson GN, Birge RR, Frank HA (2014) High efficiency light harvesting by carotenoids in the LH2 complex from photosynthetic bacteria: unique adaptation to growth under low-light conditions. J Phys Chem B 118(38):11172CrossRefPubMedPubMedCentralGoogle Scholar
  37. McLuskey K, Prince SM, Cogdell RJ, Isaacs NW (2001) The crystallographic structure of the B800–820 LH3 light-harvesting complex from the purple bacteria Rhodopseudomonas acidophila strain 7050. Biochemistry 40(30):8783CrossRefPubMedGoogle Scholar
  38. Pajusalu M, Rätsep M, Trinkunas G, Freiberg A (2011) Davydov splitting of excitons in cyclic bacteriochlorophyll a nanoaggregates of bacterial light-harvesting complexes between 4.5 and 263 K. ChemPhysChem 12(3):634. CrossRefPubMedGoogle Scholar
  39. Robert B, Cogdell RJ, van Grondelle R (2003) The light-harvesting system of purple bacteria. In: Green BR, Parson WW (eds) Light-harvesting antennas in photosynthesis. Springer, Netherlands, Dordrecht, pp 169–194CrossRefGoogle Scholar
  40. Scholes GD, Gould IR, Cogdell RJ, Fleming GR (1999) Ab initio molecular orbital calculations of electronic couplings in the LH2 bacterial light-harvesting complex of Rps. acidophila. J Phys Chem B 103(13):2543CrossRefGoogle Scholar
  41. The high-resolution structure was provided by Dr. Aleksander W. Roszak, University of Glasgow, unpublished resultsGoogle Scholar
  42. Voityuk AA, Rösch N (2002) Fragment charge difference method for estimating donor-acceptor electronic coupling: application to DNA \(\pi\)-stacks. J Chem Phys 117(12):5607. CrossRefGoogle Scholar
  43. Wang J, Wolf RM, Caldwell JW, Kollman PA, Case DA (2004) Development and testing of a general amber force field. J Comput Chem 25(9):1157. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Yang CH, Hsu CP (2013) A multi-state fragment charge difference approach for diabatic states in electron transfer: extension and automation. J Chem Phys 139(15):154104. CrossRefPubMedGoogle Scholar
  45. Zuber H, Cogdell RJ (1995) Structure and organization of purple bacterial antenna complexes. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Springer, Netherlands, Dordrecht, pp 315–348Google Scholar

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© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Dipartimento di Chimica e Chimica IndustrialeUniversity of PisaPisaItaly
  2. 2.Glasgow Biomedical Research Centre, Institute of Molecular Cell and Systems BiologyUniversity of GlasgowGlasgowScotland, UK

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