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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    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

    In the present paper we have used three different approachesin an effort to try to understand inter molecular interactionsbetween bacteriochlorophyll a molecules in self-assembledaggregates and to predict their absorption and CD spectra insolution. As there exists no crystal structures of BChl a aggre-gates model structures were generated by using molecularmechanics optimisation. Such an approach has been used topredict structures and spectroscopic properties of Chl a water, Chl a dioxane and BChl d aggregates.13,35 To calculatespectra of aggregates, the traditional dipoledipole interactionexciton model (DDEM), configuration interaction excitonmodel (CIEM) and quantum chemical semi-empiricalZINDO/S CI method were applied. The calculations suggestthat molecular interactions in the two aggregates studied theBChl awater and BChl adioxane are very different. In theformer a J-like structure with strong chromophorechromo-phore interaction was observed. In the latter, minimum energyH-type model structures (also three-dimensional) could notexplain the experimentally observed red shift, suggesting thatthe environmental shift must be the main factor that inducesthis shift.

    Experimental

    BChl a was dissolved in dry 3-methyl pentane (Fluka Chemica,>99%) to obtain about a 1 104 mol1 solution. The solventwas dried by passing it through a column filled with activatedaluminium oxide and stored over 4 A molecular sieves. Toavoid light induced oxidation of BChl a 3-methyl pentanewas bubbled with dry nitrogen for 15 min before sample pre-paration and solutions were kept in the dark. Dioxane andwater were added in solutions with a microliter Hamilton syr-inge. Aggregates were formed when BChl a : water or dioxaneratio was from 1/30 to 1/60. Gentle stirring of the solutionshelped aggregate formation.Absorption spectra were recorded by using a Jasco 7800

    UV/vis spectrometer and 1 mm path length. A Jasco J-715CD spectrometer was used for CD measurements. For absorp-tion, CD and femtosecond experiments solutions havingabsorbancies between 0.5 to 1.0 were used. For fluorescenceexcitation few tens of milliwatts of CW output at 760 nm froma Coherent MIRA 900 Tisapphire laser pumped by a 15 WCoherent Innowa argon ion laser was used. The fluorescencespectrum was recorded with a spectrometer consisting of animaging monochromator (Acton Research Corporation, Spec-tra Pro 300i) and a CCD detector (Princeton Instruments,TEA/CCD-1024-E/1, 256 1024 pixels). An amplified femto-second Tisapphire laser with a pulse duration of about 250 fswas used for single colour transient absorption measurements.The details of the femtosecond spectrometer used are givenelsewhere.36 The kinetic traces were deconvoluted by usingGlobal Analysis software from the University of Illinois,USA. All measurements were performed at room temperature.

    Computational methods

    The monomer structures of BChl a and dioxane were fullyoptimised at the semi-empirical PM3 (ref. 37) level on a

    Fig. 1 Experimental absorption spectra in the Qy region of (a) mono-meric BChl a, lmax 772 nm; (b) BChl adioxane aggregate,lmax 770 and 815 nm; (c) BChl awater aggregate, lmax 780 and867 nm at room temperature. Monomer spectrum was recorded inacetone, while aggregate spectra were recorded in 3-mehtylpentane,where small amounts of dioxane or water was added.

    3062 Phys. Chem. Chem. Phys., 2002, 4, 30613070

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  • Silicon Graphics Indigo2 workstation by using SPARTAN38

    (Version 5.0) software. The calculated geometry of Bchl awas then used as a starting geometry in the study of differentaggregate structures by using QUANTA (release 3.2) softwareon a Silicon Graphics PERSONAL IRIS 4D/35 TG+ work-station. The standard parameters of QUANTA were usedwith the exception of the bond length between all the nitro-gens and the magnesium atom in the porphyrin ring beingset to 2.086 A. This value was taken from the X-ray structureof ethyl chlorophyllide a dihydrate.8 The aggregate structureswere minimised by using a molecular mechanics methods withthe CHARMm force field and Newton Raphson39 optimisa-tion method. Single point ZINDO/S4042 semi-empirical CIScalculations for the monomers, dimers, trimers, and tetramerswere performed by using HyperChem43 software running on apentium PC.

    The Hamiltonian

    Consider a system of N molecules that form an aggregate with-out excitonphonon coupling with only one relevant molecularelectronic transition from the ground to the excited state andonly one particle-hole excitation. The Hamiltonian is givenin second quantized form as44

    HH XNn1

    enBBnBBn 1

    2

    XNm6nm1

    Jnm BBmBBn BBn BBm

    ; 1

    where en Den+Dn+ dn , Den is the electronic excitationenergy of a single molecule n, Dn is so called environmentalshift,45

    Dn XNm6n

    1n0mh jHHnm 1n0mj i XNm 6n

    0n0mh jHHnm 0n0mj i 2

    where Hnm contains electronelectron, electronnuclear andnuclearnuclear interaction terms between molecules n andm, and the states defined below. dn is the surrounding effect(e.g. solvent, protein, etc.), Jnm is the matrix element of theinteraction operator between the molecules m and n, and theBn operators are Pauli creation (B

    +), and annihil...

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