exciton interactions in self-organised bacteriochlorophyll a - aggregates

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  • Exciton interactions in self-organised bacteriochlorophyll

    a - aggregates

    J. Linnanto,* J. A. I. Oksanen and J. E. I. Korppi-Tommola

    Department of Chemistry, University of Jyvaskyla, P.O. Box 35, FIN-40351, Jyvaskyla, Finland.E-mail: Linnanto@tukki.jyu.fi

    Received 24th July 2001, Accepted 28th January 2002First published as an Advance Article on the web 20th May 2002

    Exciton interactions of self-organised bacteriochlorophyll a - aggregates in non-polar solution linked via waterand dioxane have been studied. Absorption and CD spectra of the aggregates show large red shifts typical ofJ-aggregates. Femtosecond excitation of the Qy band of the aggregates is followed by wavelength dependentnon-exponential picosecond relaxation and anisotropy decay takes place in subpicosecond time scale. To explainthese observations exciton theory and semi-empirical MO/CI calculations, that constitute the basis of theCIEM-approach developed by Linnanto et al. (J. Phys. Chem. B, 1999, 103B, 8739) was used. Structural modelsof aggregates were created by using the molecular mechanics method. Absorption and CD spectra of the modelstructures were calculated from excitonic wavefunctions. A stable J-type helical structure of BChl awateraggregate with a diameter of about 20 nm, in agreement with experiment, was obtained. Calculations for thisstructure produced the experimental absorption and CD spectra of the BChl awater aggregate correctly. ForBChl adioxane aggregates several stable H-type linear structures were calculated and blue shifted absorptionand CD spectra with respect to the monomer Qy transition were predicted. Almost a perfect match of the shapeof the calculated CD spectrum with the experimental spectrum suggests that solvent interaction not included inthe calculations is mostly responsible for the red shift observed experimentally for the dioxane aggregates.The results are discussed with reference to molecular interactions of BChls in solution and in light harvestingantenna of photosynthetic bacteria.

    Introduction

    Aggregates of chlorophylls (Chl) and bacteriochlorophylls(BChl) have been studied extensively in the past as they maybe considered as model systems to aggregates of these chromo-phores in photosynthetic bacteria and plants.1 Several spectro-scopic methods have been used to study such bindingmechanisms.2,3 A common feature of Chls and BChls innon-polar solutions is self-assembly, that takes place sponta-neously or when small amounts of polar solvent is added insolution. In the latter case aggregation induces large red shiftsof the Qy absorption band and strong CD signals are observedwith concomitant dramatic reduction of the fluorescencequantum yield and shortening of the fluorescence lifetime.Fundamental questions arise: (i) what are the molecular inter-actions that keep the monomers together and determine thestructure of the aggregate; (ii) can we predict spectral proper-ties, if we can describe binding in the aggregates; (iii) wheredoes excitation energy go in the aggregates?Electron microscopy and neutron scattering methods have

    revealed tubular structures of Chl and BChl aggregates in solu-tion4,5 with diameters ranging from 5 to 20 nm and lengthsfrom a few hundred up to a few thousand nanometers.1,5,6,7

    No crystal structures of self-assembled Chl or BChl aggregatesare available. Structure of crystalline ethyl chlorophyllide a 2H2O (ref. 8) has been used as a model structure of chloro-phylls in several theoretical studies.Aggregates of Chl a and Chl b are functional chromophores

    in photosynthetic complexes of algae and plants.1 Structuraldata on the photosynthetic PSI and PSII complexes9,10 suggestfairly long distances between chromophores and irregular orien-tation of the chromophores in these protein complexes. Weakmolecular interactions between individual chlorophylls and a

    particular chlorophyll and its local protein environment deter-mine the spectral properties and excitation energy transfer ratesand direction of these complexes. The protein environment ofPSI includes also carotenoids and a large number of watermole-cules. The structure reveals special water bound chlorophyllaggregates in PSI.10 To understand optical transitions in suchcomplex systems, reliable computational methods are neededfor estimataion of weak local molecular interactions and meth-ods have to be developed that can handle systems containinghundreds of chromophores. Aggregation of Chl a in hydrocar-bon solution has been studied extensively over the years.3,11,12 Amodel structure of chlorophylldioxane aggregate with twointernal tetramers have been proposed to explain the experimen-tal absorption and fluorescence polarization spectra.13 For Chlawater aggregate, a tube-like structure consisting of helicalstrings and a hydrophilic interior has been proposed. It was con-cluded that both chormophorechromophore interaction andexcess water inside the tube contribute to the experimentallyobserved red shift. Trimeric Chl awater aggregate with struc-ture very similar to that in the helix,13 has now been observedin the crystalline structure of PSI of cyanobacteria.10

    Aggregates of BChls (BChl c, d and e) are present in chloro-somes of green bacteria.6,1416 These bacteriochlorophyll tubu-lar assemblies which contain a large number (10 000 to 20 000)of chromophores, are stacked on top of each other. Tubes arefrom 100 to 200 nm long and have varying diameters from 5to 15 nm depending on the chromophore and the environment.Typical feature of chlorosomes is that they may contain severalhomologues of the same BChl. Chlorosomes show large spec-troscopic shifts (from 60 to 80 nm) of the monomer Qy transi-tion as compared to the monomer absorption at about 660 nm.The shift is very similar to that observed for the Chl awateraggregates and BChl awater aggregates in solution. Reversible

    DOI: 10.1039/b106692g Phys. Chem. Chem. Phys., 2002, 4, 30613070 3061

    This journal is # The Owner Societies 2002

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    View Article Online / Journal Homepage / Table of Contents for this issue

    http://dx.doi.org/10.1039/b106692ghttp://pubs.rsc.org/en/journals/journal/CPhttp://pubs.rsc.org/en/journals/journal/CP?issueid=CP004013

  • aggregation and similar spectroscopic shifts are observed forpure BChl c17,18 and BChl e19 aggregates in solution.Aggregates of BChl a are much less studied, than those of

    Chl a, BChl c and BChl d. This is somewhat surprising sinceBChl a is the functional chromophore in the photosyntheticpurple and green bacteria.20 The dimerization of BChl a in car-bon tetrachloride solution has been studied.21 Aggregates ofBChl a have been claimed to have a low aggregation numberin formamidewater mixture, in Triton X-100, in benzeneand in carbon tetrachloride.2225 BChl a aggregates with largeaggregation number can be prepared in non-polar solutions byusing a bifunctional interpigment ligand.26 Small-angle neu-tron diffraction results indicate that BChl awater aggregatesin hydrocarbon solution have tubular structures with a radiusof 10.5 nm and Qy absorption shifted from monomer value of773 nm to 865 nm (Fig. 1).5 The Qy absorption band of BChladioxane aggregate is red-shifted to 815 nm with a shoulderat 845 nm (Fig. 1).7,27,28

    Aggregates of BChl a perform an important task in purplebacteria, they trap suns light for the use of photosynthesis.Aggregates are located in special light harvesting complexeswhere BChl a monomers are organised into ring-shaped struc-tures with characteristic number of monomers in each ring.29

    Such aggregates of BChl a are found in the LH2 antenna ofRhodopseudomonas (Rps.) acidophila and Rhodospirillum(Rs.) molischianum and in the LH1 antenna of Rps. viridis.The large spectroscopic shifts of the B850 rings of the LH2and the chromophore ring of the LH1 antenna are very similarto those found for Chl awater, BChl awater, BChl c and daggregates in solution. It is likely that the molecular interac-tions responsible of these large shifts are of the same originboth in protein and in solution, strong chromophorechromo-phore and probably weaker environmentchromophoreinteractions.30 In LH2 complexes aggregates with weakinteractions are present in the B800 ring. In this case local pro-tein environment determines the spectroscopic shift observedexperimentally.31 The situation is very similar in solutions ofmonomeric chromophores. Recently, we have shown that sol-vent binding to Chls or BChls induces energy level shifts ofthe excited states of the dyes, especially for the states wheremagnesium atom has high electron density.32 The interactionis weak, but strong enough to induce considerable spectro-scopic shifts, especially in the Qx and Soret regions. A spec-trum of a chromophore in solution or in protein may beconsidered as an ensemble of a large number of transitionsenergetically perturbed by local molecular interactions. Suchperturbations give rise the inhomogeneous line width.To understand the relationship between molecular-level

    interactions and spectroscopic properties of dye molecules in

    various environments quantum chemical methods have beenused extensively. One of the first quantum chemical formalismsfor computation of spectral properties of chlorophyll andbacteriochlorophyll dimers included the classical four-levelmodel.33 Exciton calculations of the absorption spectra ofaggregates of Chl a and BChl a containing from 2 to 10 mono-mers have been reported.34 Since this pioneering work compu-tational possibilities have dramatically improved and quantumchemical methods have been applied to several photosyntheticlight harvesting systems containing BChl a.30,31

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