molecular emission and electronic structure of associated chlorophyll a

Molecular emission and electronic structure of associated chlorophyll a

N. E. BINNIE, L. V. HALEY, T. A. MATTIOLI, D. L. THIBODEAU, W. WANG, AND J . A. KONINGSTEIN' Department of Chemistry, Carleton University, Ottawa, Ont., Canada K l S 5B6

Received February 5, 1987'

N. E. BINNIE, L. V. HALEY, T. A. MATTIOLI, D. L. THIBODEAU, W. WANG, and J. A. KONINGSTEIN. Can. J. Chem. 66, 1728 (1988).

We report the wavelength-selective Raman and fluorescence spectra of monomeric and aggregate species of chlorophyll a in solution. The excitation profile for the molecular emission of the various chlorophyll complexes permit the construction of part of the electronic energy level diagram. For aT-shaped dimeric chlorophyll a , pseudo-exciton splittings of 667 cm-I in the Soret and 397 cm-' in the Q, bands are obtained.

N. E. BINNIE, L. V. HALEY, T. A. MATTIOL~, D. L. THIBODEAU, W. WANG et J. A. KONINGSTEIN. Can. J. Chem. 66, 1728 (1988).

On a determink les spectres Raman et de fluorescence i longueurs d'onde selective d'esptces monomtres et sous forme d'agregats de chlorophylle a en solution. A l'aide des profils d'excitation de 1'Cmission molCculaire des complexes de diverses chlorophylles, on peut construire une partie du diagramme des niveaux d'knergie Clectronique. Pour une chlorophylle a dimtre en forme de T, on a obtenu des sCparations de 667 et de 397 cm-I respectivement pour les bandes de Soret et de Q,..

[Traduit par la revue] . &.

1. Introduction There are numerous reports in the literature which deal with

spectroscopic and other properties of solutions which contain chlorophyll a (Chla). Much attention has been paid to the interpretation of the absorption (1 -4) and fluorescence (5- 13) spectrum of this biologically interesting molecule. It is well known that monomers and aggregates of this and the bacterio- chlorophyll molecule play an important role in the photophysic- a1 process in plants and bacteria. We discuss here spectral properties of the model compound Chla in vitro. In particular, the spectra of aggregates of this compound could be of import- ance in the identification of the spectra of chlorophyll in vivo (14).

The principal features of the absorption spectrum of Chla are the Qy, , (5'1.2 +So) and Soret bands (S3,4 +SO). They occur in the spectral regions of 600-720 nm and 400-450 nm, respectively. Compared to the position of these bands of the less concentrated solutions in non-polar solvents like carbon tetrachloride, benzene, or hexane, the positions are red-shifted in the more concentrated solutions. Furthermore, the bands broaden and the Qy absorption band is split into two components. These spectral features in combination with thermodynamic data, have l6 00

in the past been interpreted (1, 11-15, 35) in terms of the wavenumber cm-' contribution to the absorption spectra of the aggregates. Also,

large changes in the concentration of Chla result in minor FIG. 1. Fluorescence of a 1 x 10" M solution of Chla in hexane. (a) changes in the absorption spectrum (1 1, 16, 17). In addition, the Cell thickness is 10 mm. (b) Same solution as in (a) with a cell absorption spectrum of some of the monomeric species is known thickness of 1 rnrn. Absorption spectrum (.-.-.-.) of this solution. but not that of the aggregates.

In recent publications (1 1- 13) from this laboratory, informa- tor). i he macrocycles of the chlorophyll molecules are thought tion was presented leading to the assignment of the fluorescence to be approximately perpendicular to each other, contrary to the spectrum of monomeric and aggregated Chla in hexane. In dry geometry for another dimer (21) where the rings are parallel but hexane the fluorescence of the penta-coordinated monohydrate translated with respect to each other. This dimer, composed of dominates over that of any other species in highly diluted soh- bacte~ochlorophyll molecules, is found in the reaction center of tions (<lo4 M). For more concentrated solutions the certain bacteria (21). The structure of this dimer is stabilized fluorescence spectrum reveals the presence of an approximately through linkages of the cluster with a protein molecule. In T-shaped dimer (hereafter referred to as the dimer) where bond- contrast, such co-facial dimers are less stable in solution. They ing occurs (16-20,25,26) between the keto group on ring V of are thought to be a minority species in our solutions. one Chla molecule (donor) to the Mg atom of another (accep- 1, the present work we report the results of fluorescence

excitation and nanosecond resonance Raman measurements of ra ill^^ ~ ~ l l ~ ~ 1985-1987. ~~~~~~h by the Natural solutions containing monomeric Chla and the dimer. In addition

Sciences and Engineering Council of Canada. to information which can be obtained from the absorption spec- 'Revision received March 21, 1988. trum, the fluorescence excitation profiles for specific species

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FIG. 2. Fluorescence excitation profiles of a < M solution which contains the Chla monohydrate. (a) Excitation profile in the range of 415-460 nm for the intensity of the emission at 664 nm. (b) Excitation profile between 653 and 670 nm detected at the shoulder of the 664 nm emission: 671 nm (0, upper curve) and 675 nm (-, lower curve).

and the resonance Raman excitation profiles can provide one with sufficient data to obtain the positions of energy levels lying in the Q and Soret bands of the species in solution.

11. Experimental Chla was extracted from fresh spinach according to the method of

Omata and Murata (22) and purity established by standard techniques (23, 24). The pure Chla wa stored in the dark in a nitrogen-purged dry box. Chla was dried by codistillation sequentially three times with dry carbon tetrachloride (Baker Photorex) and two times with dry hexane (Caledon Labs. Inc., spectral grace) prior to preparation of a concentrated stock solution. All solvents were dried by passing through a column of neutral aluminum oxide (Woelm Activity 1, carried out in the nitrogen-purged dry box) and were then degassed.

Samples for fluorescence and Raman measurements were contained in either air-tight quartz optical cells fitted with Teflon stopcocks (fluorescence measurements) or a flowing cell technique was used ensuring that neither oxygen or water wouldenter the solutions (Raman measurements). The dilute lo-'- M Chla hexane solutions were prepared by dilution of the stock solution with degassed solvents of dried hexane (hereafter referred to only as hexane) or undried hexane (used as received) as specified in the text. The samples were equili- brated for a minimum of 1 h before use. The and 104 M solutions were prepared using dried hexane.

Molecular emissions from solutions of chlorophyll dissolved in 2,4-lutidine were also studied. The solvent lutidine (Aldrich 97% pure) was successively distilled over KOH and BaO under reduced pressure. The dried solvents were kept over molecular sieves and purged with Nz before use.

illumination was a critical parameter in the experiments. If the width of the sample was not adjusted with respect to increasing sample concentration, then reabsorption effects distorted the spectra. In Fig. 1 we show the fluorescence spectra of a 10" M Chla solution in hexane where the sample was placd in a 10 mm cell (Fig. l a ) and a 1 mm cell (Fig. lb). Superimposed on the data is the absorption spectrum of this solution. Self absorption is evident across the entire fluorescence spectrum. As a result of this observation, we chose a 1 mm cell for the lo4 M solution, therefore minimizing the spectral distortion due to self absorption.

The light was dispersed by a Jobin-Yvon Ramanor HG2 spectrom- eter equipped with curved holographic ruled gratings. Spectra were recorded with a slit of 3-7 cm-' and the radiation emerging frm the exit slit was detected by a RCA 31034 cooled photomultiplier tube. The pulsed signals were fed into a gated detection system (Stanford Re- search Associates) and the spectra were recorded on a stripchart re- corder or -processed with a computer. If not stated differently, fluorescence spectra were recorded with a gate of 3 ns at a point in time at which the intensity of the fluorescence signal has reached its maximum intensity. The Raman spectra were recorded with a similar gate but at a point in time (to) at which the laser pulse has reached its maximum intensity. Lifetimes were computer-calculated with a modified phase-plane method, and are estimated to contain an uncer- tainty of 0.5 ns.

Our spectroscopic studies in the past and present point to the fact that for equal concentration of dry Chla in the solvents hexane, carbon tetrachloride, or benzene, the concentration of aggregates is higher in hexane. Hence, we chose to use hexane as the solvent to investigate the emission spectra of aggregates of Chla.

Pulsed laser fluorescence and Raman spectroscopy experiments were performed using a tunable dye laser pumped with a Nitrogen or 111. Results and discussion Excimer laser (Lambda Physik F1 2000 and M2000 or Lumonics models TE 430 and EPD 330), pulse FWHM of 5 and 10 ns, respective- *. Fzuorescetzce excitatiorz Vectra ly. The emitted light was observed in the back scattering or reflection Monomer techniques in order to minimize self-absorption. Because both the It is well known that fluorescence from monomeric species of incident light and emitted light were absorbed, the depth of the sample Chla is most conveniently studied if the large molecule is

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1730 CAN. 1 . CHEM. VOL. 66, 1988

dissolved in polar solvents. However, if dissolved in non-polar solvents the fluorescence as well as the absorption spectrum cannot be interpreted in terms of properties of a single species. We have shown in an earlier publication (13) that for solutions which are < M Chla in hexane, the fluorescence spectrum of the monohydrate which has a maximum intensity at 664 nm exceeds that of any other species. Shown in Figs. 2a and b are the excitation profiles of the Soret and Q,, absorption band systems which are characterized by maxima at 426 nm and 660-662 nm. The positions of these maxima coincide with the maxima of the Soret and Q, absorption bands of the monohydrate in solution (13). Therefore there exists a correlation between the absorption spectrum and the fluorescence excitation profile for the red emission of the monohydrate. The observed decay time of this emission if excited at 436 nm is 6.2 ns.

Dimer The results of a wavelength-selective fluorescence study of

Chla for concentrations M in hexane are presented in Figs. 3 and 4. These solutions contain, besides the monohydrate, various aggregates of Chla. It is known that a chemical equilibrium exists between the species in solution (16, 17) as is evident by the appearance of red-shifted absorption features in both the Soret and Q,, spectral regions. In the solvents CClj and hexane, vapour phase osmometry (35) data were directly attri- buted to species having an average aggregation number of approximately 2. Therefore we assume that in our hexane solutions, upon an increase in concentration of Chla, the first species to exhibit fluorescence besides the monohydrate should be the dimer. Some information on the spectroscopic properties of this dimer has been discussed in earlier work (13). In the following discussion we present a comparison of molecular emission (fluorescence and Raman) and other data. These results, in particular the resonance Raman spectra, strongly support the existing picture of the chemical link betwen the two Chla molecules of the dimer.

In Fig. 3 we show the wavelength-dependent fluorescence spectra of a solution which is 5 X M and contains monohydrate species as well as dimers. If the solution is excited at 422 nm the emission of the monohydrate at 664 nm is clearly observed. The apparent shift in the 664 nm emission is due to the effect of reabsorption caused by an increase in the illuminated sample volume as the wavelength of the laser is scanned away from the intensity maximum of the Soret absorption band. Upon excitation between 430 and 457 nm the intensity of an emission at 686 2 1 nm is detectable. Relative to the excitation profile of the monomer (Fig. 2a), that for the band at 686 nm has a maximum between 440 and 448 nm (Fig. 5) and we assign this fluorescence (13) to that of the dimer. The increase in concentration of the dimer with respect to that of the monomer is evident if the results in Figs. 3 and 4 are compared. The spectra shown in Fig. 4 of solutions which are and M are recorded from cells which are, respectively, 10 mm and 1 mm thick, therefore minimizing the relative effect of reabsorption of the fluorescences. The result of mimimizing the effect of reabsorption has permitted us to increase our accuracy so as to establish a reliable emission wavelength for each of the species. Prelimi- nary experimental data for a M solution suggest that the 686 nm emission band still dominates the spectra, indicating that the concentration of the dimer is still high in comparison to that of other species. In an earlier publication (13), a dicussion was given of the emission band assignments in the spectral region of 668-688 nm in terms of fluorescences originating in the accep-

wavenurnber crn-'

FIG. 3. Wavelength-selective fluorescence spectrum of a solution of 5 X M Chla Chla in dry hexane. The vertical bar denotes the position of the fluorescence of the chlorophyll monohydrate molecule at 664 nm. Fluorescence from the donor at 686 nm (14577 c~n- ' ) is selectively excited with the laser wavelength of 457 nm.

tor and donor molecules of the dimer. In the present study we conclude that the donor emits at 686 2 1 nm, and further evidence for this assignment will be given in section B.

B. Nanosecond resonance Raman spectra and excitation profiles

Raman spectra of Chla in hexane, excited with pulsed (27- 29) and cw laser radiation (30-32) have been reported in the literature. If excited with laser radiation tuned to the spectral region of the Soret band of Chla, the intensity of the Raman spectrum is resonance enhanced. Spectra from solutions which are >lop5 M in chlorophyll can be recorded with good signal/noise ratios. The solutions contain more than one species with overlapping Soret bands. The vibrational frequencies of normal modes of the different Chla species are not far apart because the width and the shift of the am an bands are similar. Hence, the resonance Raman excitation profile for the intensity of Raman bands may contain useful information on the position of electronic excited states. Of relevance here is the experimental result that the width of these profiles at resonance is - 100 cm-' as compared to a - 1000 cm-' width for absorption bands of the solutions.

In the present work we are mainly interested in the excitation spectra (see Fig. 5) of one of the most intense Raman bands of

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to record these spectra, the intensity of the laser radiation at 435.2 nm was sufficiently high to produce effective population saturation of lower-lying nanosecond-lived excited states (S,) of the monohydrate, and donor molecule as judged from Q, fluorescence of these entities. From the pulsed laser intensity- dependent value of the sample transmission, it follows that the intensity of the S,, + S, absorption at 435.5 nm is smaller than that of the transition at that wavelength which originates in the ground state (34). Hence we predict ;smaller intensity enhance- ment for vibrational scattering in the electronic excited state at the ground state resonant wavelengths.

Also shown in Fig. 5 is the two-photon induced blue fluorescence from the 1 X lo4 M solution and the excitation profile of the dimer fluorescence band at 686 nm. The width of the fluorescence band is -2000 cm-' as com~ared to 1000 cm-' for the emission in the blue for monomeric chlorophyll in lutidine, see Fig. 6. The large width of the blue fluorescence band is due to contributions of emissions from the monohydrate, dimer, and perhaps even higher aggregates. The maximum intensity of the blue emission is at 455 nm and is assigned to emission of the dimer. This fluorescence originates in the S3 level of the donor molecule. From the Raman excitation spectra we find that resonance with this state occurs if the laser is tuned to 448.2 nm, hence the S3 state of the donor is near 22 300 cm-'.

Wavenurnber (cm-'1 FIG. 4. Pulsed laser fluorescence excitation of Chln in hexane. The

spectra of the 10-'M solution are obtained from a 10 mm cell, and those from the lo4 M solution from a 1 mm cell.

Chla in solution. The excitation profile was obtained by plotting the intensity ratio of the intense Raman band at approximately 1550 cm-' of Chla to that of a band of the solvent as a function of the wavelength of the pulsed laser radiation that induces the spectra. This Raman shift is primarily due to C-C stretching modes of the Chla molecule and its position changes from species to species.

Monomer When the Chla is dissolved in lutidine, aggregation does not

occur (32) and the penta-coordinated Chla complex is the species present in a lo4 M solution. The resonance Raman profile (not shown) for the intensity of the 1550 cm-' band has a maximum between 430 and 445 nm which is close to the cross-over point of the Soret absorption band at 433 nm and the two-photon induced Stokes shifted fluorescence at 444 nm, see Fig. 6. The maximum at 439 nm is assigned to the position of the electronic origin for transitions between the S3 and So electronic surfaces of the chlorophyll-lutidine complex.

Dimer The excitation profile for the Raman band at 1550 cm-' in the

spectral interval of 430-450 nm for 1 X lo4 M Chla in hexane is shown in Fig. 5. The main components in this solution are the monohydrate and the donor-acceptor dimer complex. In order

This position is within experimental error equal to the cross-over point of the two-photon induced blue fluorescence and the contour of the excitation profile for the emission at 686 nm, see Fig. 5.

In order to assign the S, position of the acceptor molecule the following arguments are pertinent. The position of the Soret band for the monohydrate complex is at 426 nm. Although two-photon induced blue fluorescence from solutions containing this complex could not be detected, the Stokes shift for the penta-coordinated lutidine (see above) and other complexes (33, 34) is between 11 and 14 nm. We predict for the monohydrate complex an electronic orgin between 431 and 433 nm. The excitation profile of Fig. 5 shows maxima at 435.2 and 448.2 nm. However, a search for intensity increases in the excitation profile between 426 and 435.2 nm for a lo4 M solution of Chla in hexane was negative. The position of the Soret absorption band of this solution, which yields the excitation profile of Fig. 5 is at 430 nm, and the Soret band of the monohydrate was not detected. Assuming a Stokes shift similar to that of the monomer, an electronic origin of the acceptor would then be expected between 435 and 437 nm. Hence we assign the maximum of the profile at 435.2 nm to the position of an electronic origin (S3) of the acceptor molecule, and that at 448.2 nm to an origin (S3) of the donor. At the resonating wavelengths, the degree of en- hancement of the Raman band intensities of the dimer is in agreement with the difference of the intensity of the absorption bands at 430 and 444 nm.

For the acceptor molecule, the assignment of the electronic origin is supported by wavelength-dependent intensity measurements of Raman bands at 1705 and 1655 cm-' . The band at 1655 cm-' is due to scattering from the Mg-bound C-0 group on ring V of the donor chlorophyll molecule, while the band at 1705 cm-' is the frequency of this mode for the free keto group of the acceptor molecule (30). Compared to the intensity of the band at 1655 cm-' that of the band at 1705 cm-' goes through a maximum if the wavelength of the laser is tuned to 404.9 nm. At this wavelength, resonance occurs with the vibronic side band due to the C=O vibration at 1705 cm-' of the non-ligated keto u

group on ring V of the electronic surface having its origin at

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WAVELENGTH (nm)

FIG. 6. Absorption (-), and two-photon induced blue fluorescence (---) of penta-coordinated Chla in lutidine.

j between the two macrocycles deviates significantly from zero.

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molecular emission and electronic structure of associated chlorophyll a

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