Qy-excitation resonance raman spectra of chlorophyll a and related complexes. Normal mode characteristics of the low-frequency vibrations

Article abstract of DOI:10.1021/jp971965g

Q_y-excitation resonance Raman (RR) spectra are reported for film aggregates of chlorophyll (Chl) a and a series of related complexes. The latter include Mg(II) octaethylporphyrin (MgOEP), Mg(II) trans-octaethylchlorin (MgOEC), methyl-9-desoxomesopyrochlorophyllide (DMPChl) a, and methylpyrochlorophyllide (MPChl) a. These complexes represent a series in which the structural complexities of Chl a (saturated pyrrole ring, isocyclic ring, C₉-keto group, C₂-vinyl group, and C₁₀-carbomethoxy group) are systematically added to the basic tetrapyrrole architecture. On the basis of comparison of the RR scattering characteristics of the different complexes and the predictions of semiempirical normal coordinate calculations, a self-consistent set of vibrational assignments has been developed for all the RR active modes in the low-frequency regime (100-1000 cm^-1). The studies indicate that the low-frequency vibrations encompass a diverse set of motions that include both the ring skeleton and peripheral substituent groups. However, modes in the very low-frequency regime (<250 cm^-1) are primarily due to deformations of the substituent groups. Collectively, the normal mode characteristics of Chl a and the other Mg(II) complexes provide insights into the nature of the vibrational modes that are coupled to the photophysically important, lowest energy excited states of natural photosynthetic assemblies.

Full text of DOI:10.1021/jp971965g

J. Phys. Chem. B 1997, 101, 9635-9644
9635
Qy-Excitation Resonance Raman Spectra of Chlorophyll a and Related Complexes. Normal
Mode Characteristics of the Low-Frequency Vibrations
Chengli Zhou, James R. Diers, and David F. Bocian*
Department of Chemistry, UniVersity of California, RiVerside, California 92521-0403
X
ReceiVed: June 16, 1997; In Final Form: September 11, 1997
y
Q -excitation resonance Raman (RR) spectra are reported for film aggregates of chlorophyll (Chl) a and a
series of related complexes. The latter include Mg(II) octaethylporphyrin (MgOEP), Mg(II) trans-
octaethylchlorin (MgOEC), methyl-9-desoxomesopyrochlorophyllide (DMPChl) a, and methylpyrochloro-
phyllide (MPChl) a. These complexes represent a series in which the structural complexities of Chl a (saturated
9 2
pyrrole ring, isocyclic ring, C -keto group, C -vinyl group, and C10-carbomethoxy group) are systematically
added to the basic tetrapyrrole architecture. On the basis of comparison of the RR scattering characteristics
of the different complexes and the predictions of semiempirical normal coordinate calculations, a self-consistent
set of vibrational assignments has been developed for all the RR active modes in the low-frequency regime
-
1
(
100-1000 cm ). The studies indicate that the low-frequency vibrations encompass a diverse set of motions
that include both the ring skeleton and peripheral substituent groups. However, modes in the very low-
-
1
frequency regime (<250 cm ) are primarily due to deformations of the substituent groups. Collectively, the
normal mode characteristics of Chl a and the other Mg(II) complexes provide insights into the nature of the
vibrational modes that are coupled to the photophysically important, lowest energy excited states of natural
photosynthetic assemblies.
Introduction
frequency vibrational modes involved in these processes has
only recently begun to be elucidated.
1
3c-e,17
Chlorophylls and bacteriochlorophylls serve as the photo-
physically active pigments in the photosynthetic assemblies of
plants and bacteria. The (bacterio)chlorophylls differ from
Both the charge-separation and energy-transfer processes in
photosynthetic assemblies are mediated by the lowest energy,
1
2
a,c
Qy-excited states of the cofactors.
Accordingly, RR probes
porphyrins in that one or two of the pyrrole rings are saturated
of the photophysically relevant vibronically coupled modes must
utilize Qy-excitation. In the case of certain natural photosyn-
thetic assembles, such as reaction centers and chlorosomes, the
acquisition of Qy-excitation RR spectra is possible because the
high level of fluorescence intrinsic to free (bacterio)chlorophylls
(hydroporphyrins) and a fifth, isocyclic ring is added to the basic
tetrapyrrole architecture. The structural differences in (bacterio)-
chlorophylls versus porphyrins lead to altered photophysical and
redox properties between the different classes of macrocycles.
The altered nature of these physical properties is presumably
responsible for the evolutionary selection of hydroporphyrins
as the active pigments in photosynthetic systems.
2
is strongly quenched in the pigment-protein complexes by
13,14
ultrafast energy- and/or electron-transfer processes.
Re-
cently, our group has found that Qy-excitation RR spectra can
Resonance Raman (RR) spectroscopy provides a convenient
and direct method for probing both the ground- and excited-
state properties of chromophores via the characteristics of the
also be obtained for free (bacterio)chlorophylls in a solid film
environment. The film environment red shifts and/or signifi-
17
cantly quenches the emission from the pigments. The op-
portunity to obtain Qy-excitation RR spectra of photosynthetic
pigments external to pigment-protein complexes is essential
for establishing a complete set of benchmarks for characterizing
the vibronically coupled modes.
3
RR frequencies and intensities, respectively. To date, RR
spectroscopic methods have been used to investigate a variety
of photosynthetic pigments, both in isolated form and in protein
4
systems. The majority of these studies have focused on the
-1
high-frequency (1000-1750 cm ) region of the spectrum which
In this paper, we report low-frequency Qy-excitation RR
spectra of film aggregates of chlorophyll (Chl) a and a series
of related complexes. The structures of the complexes inves-
tigated are shown in Figure 1 and include Mg(II) octaethylpor-
phyrin (MgOEP), Mg(II) trans-octaethylchlorin (MgOEC),
methyl-9-desoxomesopyrochlorophyllide (DMPChl) a, and me-
thylpyrochlorophyllide (MPChl) a, in addition to Chl a. These
complexes represent a series in which the structural complexities
of Chl a (saturated pyrrole ring, isocyclic ring, C9-keto group,
C2-vinyl group, and C10-carbomethoxy group) are systematically
added to the basic tetrapyrrole architecture. The focus of the
studies is on the low-frequency vibrational modes of the
complexes. The present studies build on earlier work from our
laboratory which elucidated the high-frequency, Qy-excitation
contains bands due to ring-skeletal and carbonyl stretching
vibrations of the macrocycle.4
-6
These vibrational data have
been used to assess the conformation of the (bacterio)chlorophyll
rings, the ligation state of the Mg(II) ion, and the extent of
hydrogen bonding to the carbonyl substituents on the rings.
Despite the focus on high-frequency vibrations, the low-
-1
frequency (<1000 cm ) region of the spectrum, which contains
bands primarily due to ring-skeletal and substituent deforma-
4
tions, is of considerable interest. For example, it has been
shown that low-frequency vibrational modes are strongly
coupled to the electronic transition which initiates the primary
7
-14
charge-separation process in reaction center proteins
and
the transitions that mediate the energy-transfer process in light-
harvesting assemblies.1
5,16
The exact identity of the low-
18
RR scattering characteristics of this same series of complexes.
[
The earlier studies were performed on Ni(II) complexes rather
X
Abstract published in AdVance ACS Abstracts, November 1, 1997.
than on Mg(II) species because it was not known at the time
S1089-5647(97)01965-2 CCC: $14.00 © 1997 American Chemical Society

9636 J. Phys. Chem. B, Vol. 101, No. 46, 1997
Zhou et al.
et al.20 using MgBr2 (etherate) (Aldrich) as the metal source
and triethylamine as the base. The product was purified on an
alumina column with CH2Cl2 elution yielding residual OEP and
with CH2Cl2/acetone (1:1) elution affording MgOEP. trans-
OEC was obtained from OEP by the method of Whitlock et
21
20
al. Magnesium was inserted by the method of Lindsey et al.
MgOEC was purified in the same manner as described for
MgOEP. Chl a was isolated from spray-dried Spirulina maxima
algae (Earthrise Co., San Rafael, CA) according to the method
22
of Smith et al. The crude product was dissolved in a minimal
amount of CH2Cl2 and chromatographed on an alumina column.
The elution was initiated with n-hexane and then followed by
CH2Cl2 to remove the neutral products. Chl a was the major
green band collected by using 0.5-5% (v/v) propanol in CH2-
Cl2 as the eluting solvent. MPChl a was prepared from methyl
pyropheophorbide a which was obtained from Chl a by the
22
method of Smith et al. Magnesium was inserted by the method
2
0
of Lindsey et al. MPChl a was purified on a sugar column
using n-hexane as the eluting solvent. MDPChl a was prepared
from methyl-9-desoxomesopyropheophorbide a by the method
23
of Abraham et al., in which magnesium was inserted by using
ethylmagnesium bromide and 2,6-di-tert-butyl-4-methylphenol.
Methyl-9-desoxomesopyropheophorbide a was obtained from
methylmesopyropheophorbide a using NaBH4 and trifluoroacetic
acid. This compound was chromatographed on a flash silica
gel column eluting with 1% MeOH-99% CH2Cl2. Methyl-
mesopyropheophorbide a was prepared by the method of Smith
2
2
et al.
RR Spectroscopy. Qy-excitation RR spectra were recorded
at low temperature (15 K) on films deposited directly onto the
cold tip of a closed cycle He refrigeration system (ADP
Cryogenics, DE 202 Displex). The procedure for preparing the
1
7
films has been described in detail previously. B-excitation
RR spectra were collected for both film (15 K) and solution
(293 K) samples of selected complexes. For the solution studies,
benzene and CCl4 were used as the solvents to obtain data in
-
1
the spectral window below and above 900 cm , respectively.
The RR scattering was collected at 90° to the incident laser
beam by using a camera lens (Canon 50 mm f/1.4) and dispersed
by a triple spectrograph (Spex 1877) equipped with either a
1200 groove/mm (Qy-excitation) or 2400 groove/mm (B-
excitation) grating in the final stage. The detection system was
a 1152 × 298 pixel, front-illuminated, UV-enhanced charge-
coupled device (Princeton Instruments LN/CCD equipped with
a EEV 1152-UV chip). The excitation wavelengths were
provided by the outputs of a Kr ion laser (Coherent Innova 200-
K3) or a dye laser (Coherent CR-590) using Rhodamine 590
(Exciton Chemical Co.) pumped by the multiline visible output
of an Ar ion laser (Coherent Innova 400-15UV). The laser
powers at the sample were typically 2 mW. The frequencies
were calibrated using the known frequencies of indene or CCl4.
Figure 1. Structures and labeling scheme for the Mg(II) complexes.
that fluorescence from the Mg(II) complexes is sufficiently
quenched in film aggregates to permit acquisition of Qy-
excitation RR spectra.17 Consequently, fluorescence quenching
was achieved via replacement of the closed shell Mg(II) ion
18
with the open shell Ni(II) ion. ] In addition to the RR
spectroscopic studies reported herein, normal mode descriptions
are obtained for the low-frequency modes using the QCFF/PI
method of Warshel and Karplus.19 Together, the RR studies
and the normal coordinate calculations provide a more detailed
assessment of the nature of the vibrational modes which are
coupled to the Qy-transitions in Chl a type pigments.
The organization of the paper is as follows. First, we present
the results of the RR study and summarize the assignments for
the low-frequency vibrational modes. Next, we discuss the
strategy for obtaining the vibrational assignments. We then
discuss the influence of the different structural elements
Normal Coordinate Calculations. The vibrational frequen-
cies and eigenvectors for the low-frequency modes of the Mg-
19
(
II) complexes were obtained using the QCFF/PI method. The
calculations were performed as described in our earlier studies
(saturated pyrrole ring, isocyclic ring, C9-keto group, C2-vinyl
18
of the Ni(II) analogues of the complexes. However, in the
group, and C10-carbomethoxy group) on the RR spectral features
and normal mode descriptions. Finally, we comment on the
implications of the present work for understanding the nature
of the vibrational modes that are coupled to the Qy-state
transitions of pigments in natural photosynthetic assemblies.
present analysis, the methyl, ethyl, and vinyl substituent groups
were explicitly included in the calculations rather than being
treated as point masses. The keto fragment of the carbomethoxy
group and the ring-adjacent methylene group of the propionate
ester were also explicitly included in the calculations. The
methoxy fragment of the former substituent and the remainder
of the latter substituent were treated as 15 amu point masses.
The torsional coordinates of all the substituent groups were
unconstrained in the energy minimizations. In the resulting
Experimental Section
Sample Preparation. MgOEP was prepared from OEP
(Midcentury Chemicals, Posen, IL) by the method of Lindsey

Qy-Excitation Resonance Raman Spectra
J. Phys. Chem. B, Vol. 101, No. 46, 1997 9637
Figure 2. Low-frequency regions of the Q
the films of the Mg(II) complexes obtained at 15 K. The exciting lines
were as follows: MgOEP, λex ) 580 nm; MgOEC, DMPChl a, λex
20 nm; MPChl a, Chl a, λex ) 647 nm.
y
-excitation RR spectra of
y
Figure 3. High-frequency regions of the Q -excitation RR spectra of
films of the Mg(II) complexes obtained at 15 K. The exciting lines
were as listed in the legend of Figure 2.
)
6
MgOEP and MgOEC yield good quality spectra demonstrates
that the film technique is not specific to photosynthetic pigments
in its utility for acquisition of Qy-excitation RR data. Indeed,
this method appears to be quite general inasmuch as Qy-
excitation RR spectra have been successfully obtained for every
highly fluorescent complex examined to date in our laboratory
minimum energy structures, these groups generally assumed
orientations that are substantially out of the pseudoplane of the
macrocycle. Consequently, many of the low-frequency normal
modes of the complexes and, in particular, those which contain
substantial contributions from motions of the substituent groups
cannot be classified as either in-plane or out-of-plane in
character.
(Ghosh, A.; Diers, J. R.; Bocian, D. F., unpublished results).
Closer inspection of the figures reveals that the quality of the
spectrum obtained for DMPChl a is somewhat poorer than that
of the other complexes. This is particularly evident in the high-
frequency region. The reason that DMChl a yields poorer
quality spectra is uncertain, but most likely involves the detailed
characteristics of the film that this complex forms. In the
Results
Qy-Excitation RR Spectra of Films. The low-frequency
-
1
(
100-825 cm ) regions of the low-temperature (15 K) Qy-
excitation RR spectra of films of MgOEP, MgOEC, DMPChl
-
1
a, MPChl a, and Chl a are shown in Figure 2. The correspond-
frequency regime above 1600 cm (not shown), none of the
complexes yield good quality spectra. This reduction in quality
occurs because the RR wavenumber shift is sufficiently large
that the spectral window falls into a region where there is
considerable interference from fluorescence.
-
1
ing high-frequency (825-1600 cm ) spectra are shown in
Figure 3. [For MgOEP, there is no distinction between the Qy-
and Qx-states owing to (near) degeneracy in the higher symmetry
complex (the electronic symmetry is retained, although the actual
symmetry is lower).24 However, for convenience, the designator
Qy-excitation will also be used to refer to the RR spectra of
this complex.] The specific exciting lines used to obtain the
spectra shown in both figures are given in the legend of Figure
Inspection of Figures 2 and 3 reveals that all of the Mg(II)
complexes exhibit rich RR spectra in both the low- and high-
frequency regions. This behavior parallels that observed in the
Qy-excitation RR spectra of other photosynthetic pigments.1
In general, the spectral complexity systematically increases as
the structural complexities of Chl a are added to the basic
tetrapyrrole architecture. In the low-frequency regime, most
3,14,17
2
. All of the exciting lines fall on the high-energy side of the
Qy absorption band contour. The Qy absorption maxima for all
of the complexes in the film environment are shifted by 10 nm
or less compared with solution.1 The RR spectra obtained
with different exciting lines in the Qy band contour are generally
similar to those shown in the figures with respect to both number
and frequency of the bands; however, some changes in relative
intensity are observed among the various modes. The spectra
obtained with excitation on the high-energy side of the Qy
absorption band contour are presented because excitation in this
7b
-1
of the additional spectral features occur in the 350-750-cm
region. In the high-frequency regime, the additional features
are spread throughout the entire spectral region. A particularly
-1
noteworthy observation is that very low-frequency (<250 cm )
RR bands which are prominent in the spectra of MgOEP and
MgOEC are very weak or absent in the spectra of the structurally
more complicated DMPChl a, MPChl a, and Chl a complexes.
Comparison of the RR spectra of the Mg(II) complexes with
those previously reported for the Ni(II) analogues reveals that
the spectra of the two different metalated complexes are very
17
region generally yields the highest quality spectra. In addition,
the RR data acquisition window can be extended to larger
wavenumber shifts before interference from fluorescence com-
promises the spectra.
1
8
similar to one another. Some differences are observed in the
frequencies and relative intensities of certain RR bands. The
frequency differences are expected because the Mg(II) and Ni-
Inspection of Figures 2 and 3 reveals that all of the complexes
yield high-quality Qy-excitation RR spectra. The fact that

9638 J. Phys. Chem. B, Vol. 101, No. 46, 1997
Zhou et al.
different in the film versus solution than those observed for Chl
a. In particular, the RR intensity enhancements for the low-
-
1
-1
frequency ν8 (347 cm ) and ν9 (265 cm ) modes of MgOEP
are quite large for the film sample but very weak for the solution
sample. Both ν8 and ν9 involve vibrations of the relatively
26
flexible â-ethyl substituents on the macrocycle. Previous RR
studies on different crystalline forms of NiOEP have shown
that the RR intensity enhancements of these modes are very
sensitive to the local environment. The data reported herein
for film samples corroborate this assessment. Despite the RR
intensity differences observed for the low-frequency modes of
MgOEP in the film versus solution environments, the frequen-
cies of the modes are not significantly different.
2
6
Vibrational Assignments. The low-frequency modes (<1000
-
1
cm ) observed in the Qy-excitation RR spectra of all the Mg-
(II) complexes are listed in Table 1 along with a proposed set
of vibrational assignments. For reference, the normal mode
assignments for NiOEP are also included in the table.26 The
normal mode descriptors listed in Table 1 are generic rather
than specific in nature and indicate only the largest contributors
to the vibrational eigenvectors. For DMPChl a, MPChl a, and
Chl a, the presence of the isocyclic ring results in extremely
complicated vibrational eigenvectors for virtually all of the
modes (vide infra). These modes are characterized by contribu-
tions from a very large number of internal coordinates.
Consequently, it is neither reasonable nor particularly informa-
tive to list the complete potential energy distribution in tabular
format. Thus, the fact that certain modes of the different
complexes are given the same generic normal mode descriptor
is not meant to imply that the vibrational eigenvectors for these
modes are in any sense identical. Likewise, the listing of the
NiOEP mode assignments should not be construed to indicate
that the vibrational eigenvectors of the saturated-pyrrole com-
plexes are necessarily similar to those of this complex. Indeed,
the correlations listed in the table are meant only to indicate
that the modes of the different complexes have certain charac-
teristics in common.
Figure 4. Comparison of the B-excitation (λex ) 406.7 nm) RR spectra
of films (15 K) and solutions (293 K) of MgOEP and Chl a.
(
5
II) have different ionic radii.25 In addition, the Mg(II) ion is
-coordinate, whereas the Ni(II) ion is 4-coordinate. The RR
intensity differences occur primarily because the frequencies
of the exciting lines versus the Qy optical transitions are not
identical in the experiments on the Mg(II) and Ni(II) complexes.
The fact that the RR spectra of the Mg(II) and Ni(II) complexes
are very similar lends credence to our earlier assignments of
the high-frequency vibrational modes of Chl a (which were
Discussion
1
8
made exclusively via comparison with the Ni(II) complexes).
The studies of the various Mg(II) tetrapyrrolic complexes
reported herein demonstrate that the film technique permits the
acquisition of Qy-excitation RR spectra for a structurally diverse
group of chromophores. The fact that the frequencies of the
RR active modes of both the natural photosynthetic pigment
Chl a and the porphyrin model complex MgOEP are similar in
the film and solution environments lends credence to the
argument that the film data are generally representative of the
vibrational characteristics of the different type macrocycles. In
the case of Chl a, the similarities between the film and solution
spectra extend to the RR intensity enhancements, further
suggesting that the film environment does not substantially alter
the coupling between the vibrational modes and the electronic
transition(s). In the sections below, we first discuss our strategy
for assigning the RR spectra. We then examine the influence
of the different structural elements on the low-frequency spectral
features and normal mode characteristics. Finally, we comment
on the implications of the present study for understanding
vibronic interactions in natural photosynthetic systems.
B-Excitation RR Spectra of Films versus Solutions. One
question that arises is whether the film environment significantly
affects the RR spectral features observed for the Mg(II)
complexes. To properly address this issue, it would be
necessary to compare the Qy-excitation RR spectra of film versus
solution samples. Such studies are, of course, not feasible owing
to the fluorescence emission from the solution samples.
However, to gain some insight into the influence of the film
environment, B-excitation RR spectra were obtained for both
film and solution samples of selected complexes. Excitation
in resonance with the higher energy B-state yields RR spectra
free from fluorescence.4
a-c
The B-excitation (λex ) 406.7 nm) RR spectra of Chl a in
film and solution environments are compared in Figure 4
(bottom two traces). These data reveal that the RR frequencies
and intensity-enhancement patterns are generally quite similar
for the film versus solution samples. Most of the frequency
-1
differences are less than 5 cm . One exception is the ν(C9dO)
-
1
5
stretching mode, which is observed at 1698 cm (solution)
Vibrational Assignment Strategy. The vibrational assign-
ments for the low-frequency modes of the different Mg(II)
complexes were determined in a stepwise and concerted fashion.
The general procedure parallels that which we have previously
used to assign the high-frequency modes of the Ni(II) analogues
-
1
and 1689 cm (film). The downshift of the ν(C9dO) mode
occurs because the oxygen atom of the C9dO group of a
particular Chl a molecule in the film most likely serves as the
1
7a
axial ligand to the Mg(II) ion of an adjacent Chl a molecule.
1
8
The B-excitation (λex ) 406.7 nm) RR spectra of MgOEP in
film and solution environments are also shown in Figure 4 (top
two traces). The RR spectral signatures for MgOEP are more
of these complexes. The methodology is as follows.
(1) The RR spectra and calculated normal modes of MgOEP
2
6
were compared with those of NiOEP.
This comparison

Qy-Excitation Resonance Raman Spectra
J. Phys. Chem. B, Vol. 101, No. 46, 1997 9639
TABLE 1: Low-Frequency (<1000 cm-1) Modes Observed with Q
-Excitationa
y
MgOEP
MgOEC
DMPChl a
MPChl a
Chl a
assignmentb
NiOEP assignmentc
1
64
153
168
189
γC
δC
â
C
a
γ
17
34
24
1
2
98
28
â
alkyl
ν
γ C
R
C
m
γ
2
3
65
47
267, 283
277
344
262
261
δC
δC
δC
â
alkyl, γC
alkyl
â
C
a
ν
ν
ν
9
, γ
7
3
18
â
17
8
343
357
391
350
387
412
â a â a
C , γC C
395
δring V, δring III
416
δC
δC
â
C
C
c
dC
C
d
4
56
451
â
1
2
δ
4
4
5
69
04
δO
δO
1
C
C
carbo
carbo
O
O
2
, δC
, δC
9
9
dO
dO
1
2
516
518
544
561
570
586
605
δC
γC
9
dO, δring III, δring V
5
45
89
548
550
561
â
C
a
, νC
â
C
a
ν
ν
ν
25
24
7
561
δring II, δring V, δring III
5
69
γ(dC
δC
δring V, δring III
γO , γring V
R m
δC , νC N, δC C
d
H
2
)as, γring I
5
584
608
â
C
a
H, δC H, δC C
b
C
a
R m
599
6
41
1 carbo 2
C O
6
72
662
671
674
690
678
691
R
C
m
C
R
R
6
7
94
28
δring IV
δpyr
ν
ν
16
15
7
7
7
9
9
9
54
69, 780
99
16
38
759
785
799
914
939
749
766
799
909
939
750
775
799
915
746
766, 788
800
δpyr
γCH
2
(rock)
m
γCH
2
3
(rock)
δC
δC
δC
R
C
C
R
, νC
alkyl, γ(dC
b a
alkyl, δC C H
â
C
a
, νMgN
ν
ν
ν
6
914
â
C
C
â
d
2
H )
s
46a
32
â
â
59
δCH
3
δCH
983
985
986
νC
9
C
10
a
MgOEP, λex ) 580 nm; MgOEC, DMPChl a, λex ) 620 nm; MPChl a, Chl a, λex ) 647 nm. b Mode descriptors are as follows: ν ) stretch,
c
δ ) in-plane deformation, and γ ) out-of-plane deformation. Symbols refer to the macrocycle and substituent positions shown in Figure 1. NiOEP
mode descriptions are those given in ref 26.
revealed that the spectral features are similar for the two
complexes (vide infra). The vibrational frequencies and eigen-
vectors obtained for the metalloOEP complexes using the QCFF/
PI method were also compared with those obtained via
conventional valence force field methods. This comparison
revealed that the two computation methods yield generally
similar results.
(3) After assigning the vibrational modes of MgOEC, the
observed and calculated features of DMPChl a, MPChl a, and
Chl a were examined and compared with one another and with
those of MgOEC. For certain of the RR bands of the isocyclic
ring containing complexes, the observed frequencies and
intensity enhancement patterns allowed a relatively straightfor-
ward correlation with those of MgOEC. All of the low-
frequency modes were then plotted in order to assess more
critically the effects of the addition of the isocyclic ring and,
ultimately, the C9dO, C2-vinyl, and C10-carbomethoxy groups.
In general, more modes are calculated than observed in the RR
spectra. Many of these modes were removed from consideration
because their eigenvectors did not contain contributions from
internal coordinates in the new structural elements. However,
in certain cases, multiple modes are calculated that both exhibit
motions in the new structural element and fall very close in
frequency to the observed RR band. In these cases, the mode
closest in frequency to the observed mode was chosen for the
assignment. Finally, we note that for a few vibrations classified
as ring skeletal/â-alkyl modes, the calculated frequencies differ
26
(2) The RR spectra and normal modes of MgOEC were
compared with those of both MgOEP and NiOEP. This
comparison included both the Qy- and B-excitation data for the
two porphyrins because the Qy-excitation RR spectra of met-
allochlorins share features in common with both the B- and Qy-
excitation spectra of metalloporphyrins.2 In particular, B-ex-
citation RR activity is derived from a Franck-Condon mechanism
5c
2
5a
which gives rise to scattering from totally symmetric modes.
In contrast, Qy-excitation RR activity for metalloporphyrins is
derived from a Herzberg-Teller mechanism which gives rise
to scattering from non-totally symmetric modes.2 For MgO-
EC, and metallochlorins in general, Qy-excitation RR activity
is derived predominantly from a Franck-Condon mechanism;
5a
25b,c
-1
thus, totally symmetric modes are predominantly enhanced.
from the observed values by as much as 80 cm (Table 1, vide
Certain of these totally symmetric modes are derived from totally
symmetric modes of metalloporphyrins (observed with B-
excitation), whereas others are derived from non-totally sym-
metric (specifically b1g) modes (observed with Qy-excitation)
infra). These disparities obviously reflect certain deficiencies
in the QCFF/PI vibrational force field. Nevertheless, the fidelity
between the observed and calculated frequencies is far better
for the majority of the modes, lending confidence that the normal
mode descriptors are qualitatively reasonable.
Influence of Different Structural Elements on the Low-
Frequency Vibrational Characteristics. The influence of the
different structural elements on the RR spectral features and
normal mode characteristics is discussed below. First, we
examine the ring-skeletal and alkyl-substituent vibrations. Next,
we turn to the vibrational consequences of addition of the
isocyclic ring. Finally, we describe the features associated with
the C9dO, C2-vinyl, and C10-carbomethoxy groups.
25c
which become symmetric in the lower symmetry environment.
In actuality, a number of totally symmetric modes gain
[
significant RR activity in the Qy-excitation spectra of MgOEP
in films and NiOEP in certain crystalline forms.26 For example,
totally symmetric mode activity is particularly apparent in the
-
1
-1
low-frequency region, where ν7 (672 cm ), ν8 (347 cm ), and
-
1
ν9 (265 cm ) are very strongly enhanced.] The comparison of
the Qy-excitation RR spectra of MgOEC with the B- and Qy-
excitation spectra of both MgOEP and NiOEP permits the
identification of qualitatively analogous features among the
various complexes.
Ring-Skeletal and Alkyl-Substituent Modes. All of the Mg-
(II) complexes share the basic architecture of a tetrapyrrole

9640 J. Phys. Chem. B, Vol. 101, No. 46, 1997
Zhou et al.
Figure 5. Vibrational eigenvectors of low-frequency ring-skeletal and â-alkyl substituent deformations which are common to all of the Mg(II)
complexes. The arrows indicate motion in the x-y pseudoplane of the macrocycle (see text).
containing alkyl substituents on each of the four pyrrole rings
Figure 1). Both MgOEP and MgOEC contain eight â-ethyl
number of features in common with one another and which are
also observed in the spectra of MgOEP and/or NiOEP. In
particular, bands are observed near 270, 350, 550, 670, 750,
(
substituents, whereas DMPChl a, MPChl a, and Chl a contain
methyl, ethyl, and propyl groups. The normal coordinate
calculations predict that many of the low-frequency vibrational
modes of the Mg(II) complexes primarily involve deformations
of the inner-ring core of the tetrapyrrole or deformations of the
substituent groups. Both types of vibrations are somewhat
shielded from the effects of pyrrole ring saturation or addition
of the isocyclic ring. Indeed, the low-frequency RR spectra of
the various Mg(II) dihydroporphyrin complexes exhibit a
-
1
770, 800, and 915 cm for all of the complexes. For the Mg-
(II) dihydroporphyrins, these modes appear to be qualitative
analogues of the porphyrinic vibrations classified as ν9(γ7), ν8,
26
ν25, ν7, ν15, γCH2 (rock), ν6, and ν46a, respectively. [The 550
-
1
cm (ν25) band is observed for NiOEP in certain crystalline
2
6
forms, but not for the MgOEP film.] Other RR bands are
observed for some but not all of the Mg(II) dihydroporphyrins,
which fall at frequencies very similar to those observed for either

Qy-Excitation Resonance Raman Spectra
J. Phys. Chem. B, Vol. 101, No. 46, 1997 9641
MgOEP and/or NiOEP. For example, MgOEC and DMPChl
-
1
a exhibit bands near 160, 195, and 940 cm which appear to
be qualitative analogues of the γ17, ν34, and ν32 substituent
deformations of metalloOEPs.26 [Here again, the 195 cm (ν34)
-1
2
6
mode is observed for NiOEP in certain crystalline films, but
not for the MgOEP film.] Interestingly, these substituent
deformations exhibit significant RR activity only in the Mg(II)
dihydroporphyrins that contain multiple ethyl substituents. This
RR activity could be induced either directly, as a result of ethyl
group orientation, or indirectly, via ethyl-group-mediated struc-
tural changes in the macrocycle core that occur in the aggregate.
The computed vibrational eigenvectors for five ring-skeletal/
â-alkyl substituent deformations that are observed in the RR
spectra of all the Mg(II) complexes are plotted in Figure 5. In
this figure and in all subsequent figures shown below, displace-
ments are shown only for those atoms that contribute signifi-
cantly to the normal mode (10% or greater of the maximum
atomic displacement in a given mode). For all of these ring-
skeletal/â-alkyl vibrations, the primary motions are in the x-y
pseudoplane of the molecule, consistent with their assignments
as qualitative analogues of in-plane deformations of metallopor-
phyrins (vide supra). Inspection of the eigenvectors for the Mg-
(II) dihydroporphyrins, particularly those containing the isocyclic
ring, reveals the complexity of the motions and, hence, the
limited utility of attempting to describe the modes in a tabular
format. This complexity is a general consequence of the effects
of low symmetry on the vibrational characteristics of the
deformation modes of tetrapyrrolic macrocycles.1
8,25c,e
Accord-
ingly, the pictorial format is the only reasonable mechanism
for gaining insight into the characteristics of the normal
modes.
Ring V Modes. The presence of an isocyclic ring is the
common structural element that distinguishes all photosynthetic
pigments from simple porphyrins or hydroporphyrins (Figure
1
). As noted above, this structural element is in large part
responsible for symmetry lowering and the accompanying
increase in complexity of the normal modes. In addition, the
presence of ring V introduces a number of new normal modes
of vibration which can potentially gain enhancement in the RR
spectrum. In particular, the RR spectra of DMPChl a, MPChl
a, and Chl a all exhibit features near 390, 560, 600, and 985
Figure 6. Vibrational eigenvectors of low-frequency modes that contain
subtantial contributions from or occur due to the presence of, ring V.
The arrows indicate motion in the x-y pseudoplane of the macrocycle
(see text).
-1
cm which are not observed in the spectra of MgOEP, NiOEP,
or MgOEC. We attribute all of these bands to vibrations
vibrations are observed in the 400-500-cm- region in five-
1
27
member-ring molecules such as cyclopentanone. Comparison
of the RR spectra of MPChl a and Chl a with those of DMPChl
a reveals that the addition of the C9dO group results in the
appearance of only one additional RR band in the 400-500
-
1
associated with ring V (Table 1). The 390, 560, and 600 cm
-
1
modes are deformations, whereas the 985 cm is a stretching
vibration associated with the single bonds in the ring.
The computed vibrational eigenvectors of four modes of
DMPChl a, MPChl a, and Chl a which have no analogues in
MgOEP or MgOEC and whose frequencies are consistent with
those observed for the ring V vibrations are plotted in Figure
-1
-1
cm region. This band is observed near 517 cm for both
complexes. This spectral characteristic of the Mg(II) complexes
is similar to that previously reported for the Ni(II) analogues,
-1 18
both of which exhibit a single new band near 534 cm . We
6
. For all of these vibrations, the primary motions are in the
attribute these features in both the Mg(II) and Ni(II) complexes
to one of the two deformations of the C9dO group.
The computed vibrational eigenvectors for modes unique to
MPChl a and Chl a and whose composition and frequency are
commensurate with a C9dO deformation are plotted in Figure
x-y pseudoplane of the molecule. Inspection of Figure 6
reveals that the eigenvectors for all of the modes are complex
and involve motions of many atoms in addition to those
explicitly associated with ring V. Consequently, the designator
“
ring V vibration” is only a generic descriptor that indicates
7
. The majority of the C9dO motion is in the x-y pseudoplane
the occurrence of a normal mode that does not occur in
architectures that lack this structural element.
of the molecule; hence, the mode is classified as the in-plane
deformation, δC9dO. [The out-of-plane deformation, γC9dO,
-
1
C9dO Modes. All photosynthetic pigments contain a keto
group at the C9-position of ring V (Figure 1). This group
conjugates into the π-electron system of the macrocycle. The
addition of the C9dO group to the DMPChl a skeleton
introduces only two new normal modes of vibration which could
occur in the low-frequency regime, namely the in-plane and
out-of-plane deformations of the C9dO group. Both of these
is predicted near 400 cm .] However, as is the case for the
other modes associated with ring V, the eigenvector of the
δC9dO vibration contains substantial motions for other atoms
in the macrocycle, particularly in the ring III-V region.
C2-Vinyl Modes. Both MPChl a and Chl a contain a vinyl
group at the C2-position on pyrrole ring I (Figure 1). The RR
scattering characteristics of vinyl substituents on porphyrins have

9642 J. Phys. Chem. B, Vol. 101, No. 46, 1997
Zhou et al.
Figure 7. Vibrational eigenvectors of low-frequency modes that contain
subtantial contributions from the C dO group. The arrows indicate
9
motion in the x-y pseudoplane of the macrocycle (see text).
Figure 8. Vibrational eigenvectors of low-frequency modes that contain
been extensively investigated because these groups are present
on the protoheme IX prosthetic group of myoglobin, hemoglo-
2
subtantial contributions from the C -vinyl group. Motions in both the
x-y pseudoplane of the macrocycle (arrows) and along the z-axis
(circles) are shown (see text).
2
8-34
bin, and the b-type cytochromes.
In the low-frequency
region, there are three normal modes of the C2-vinyl group that
could contribute to the RR spectrum, in particular, the deforma-
tion of the entire vinyl group, δCâCcdCd, and the antisymmetric
and symmetric out-of-plane deformations of the terminal vinyl
hydrogens, γ(dCdH2)as and γ(dCdH2)a. The δCâCcdCd and
γ(dCdH2)s modes are observed in the RR spectra of protoheme
propionate esters are also different in the two pigments;
1
8
however, this does not influence the RR spectrum ). Previous
high-frequency RR studies of (bacterio)chlorophylls have shown
that the stretching vibration, νCcarbodO1, is resonance enhanced
despite the fact that it is not conjugated into the π-system of
6
a,c,35
-
1
31,34
the macrocycle.
This raises the possibility that other
IX near 400 and 920 cm , respectively.
mode has not been observed but is expected near 630 cm .
The γ(dCdH2)as
-
1 34
vibrations of the C10-carbomethoxy group could gain RR
activity. In the low-frequency regime such modes would be
deformations of the entire group with respect to ring V or
deformations of the O1CcarboO2 element. Inspection of the RR
spectra of Chl a reveals that bands are observed near 469, 504,
The RR spectra of both MPChl a and Chl a exhibit bands near
-
1
4
12 and 570 cm which are not observed for DMPChl a,
MgOEC, or MgOEP. We attribute these RR bands to δCâCcdCd
and γ(dCdH2)as, respectively. The frequency of the γ(dCdH2)as
-
1
3
4
and 641 cm which are not observed in the spectra of MPChl
a. We attribute these modes to deformations involving the C10-
carbomethoxy group.
mode is somewhat lower than has been previously suggested.
However, the normal coordinate calculations reported herein
in fact predict a lower frequency for this mode in the
photosynthetic pigments (vide infra). Both MPChl a and Chl
The computed vibrational eigenvectors for modes unique to
Chl a and whose composition and frequency are commensurate
with C10-carbomethoxy group deformations are plotted in Figure
9. The eigenvectors for all three of these vibrations exhibit
displacement in all three dimensions owing to the direction of
-
1
a also exhibit a band near 920 cm which could be due to
γ(dCdH2)s. However, all of the other Mg(II) complexes also
-
1
exhibit a RR band near 920 cm (Figure 2). Accordingly, we
have assigned this band as a δCâCâalkyl mode (Table 1).
-
1
the bond vector connecting the C -carbomethoxy group to ring
Nevertheless, the 920 cm RR bands of both MPChl a and
Chl a are considerably stronger than the analogous bands of
the other three complexes. This observation could indicate that
bands due to both the γ(dCdH2)s and δCâCâalkyl are present
and coincident. This issue can only be resolved via selective
isotopic labeling of the C2-vinyl group.
10
V and the torsional angle of the group. As is the case for the
deformations of other substituent groups, the eigenvectors for
deformations of the C10-carbomethoxy group contain substantial
contributions from motions in other parts of the molecule. This
coupling most likely explains the RR activity for these modes.
The computed vibrational eigenvectors for modes unique to
MPChl a and Chl a and whose composition and frequency are
commensurate with the δCâCcdCd and γ(dCdH2)as deformations
are plotted in Figure 8. The majority of the atomic motion for
the former mode is in the x-y pseudoplane of the molecule,
whereas the majority of the motion for the latter is along the
z-axis. However, both modes exhibit displacements along the
other coordinates because the C2-vinyl group is not in the
pseudoplane of the macrocycle. In addition, the eigenvectors
for both the δCâCcdCd and γ(dCdH2)as deformations contain
substantial contributions from motions in other parts of the
molecule. This characteristic of the motion may explain why
the γ(dCdH2)as vibration is RR active in the photosynthetic
pigments but not in protoheme IX and also why its frequency
Implications for Photosynthetic Assemblies. The special
pair primary electron donor of bacterial photosynthetic reaction
center proteins ((BChl a)2) and the BChl c/d/e aggregates of
chlorosomal light-harvesting assemblies of green photosynthetic
bacteria share the common feature that a number of very low-
-
1
frequency vibrations (<250 cm ) are very strongly coupled to
their photophysically important, lowest energy electronic transi-
tions (which involve the Qy-excited states of the pigments).7
The magnitude of the vibronic coupling for these modes is much
larger than that for the other low- (and high-) frequency modes
that are coupled to the Qy-transition. The studies reported herein
for Chl a and those reported previously for bacteriochlorophyll
-15c,16
1
7a
(BChl) a, both in film aggregates and in reaction center
13c-e
proteins,
indicate that the low-frequency vibrational modes
-
1
is lower than anticipated (570 vs 630 cm ).
that are coupled to the Qy-transition are diverse in character,
ranging from vibrations of the tetrapyrrole skeleton to deforma-
tions of the peripheral substituent groups. However, the
majority of the vibronically coupled modes in the lowest
C10-Carbomethoxy Modes. Chl a contains a carbomethoxy
group at the C10 position on ring V (Figure 1). This structural
element distinguishes the natural pigment from MPChl a (the

Qy-Excitation Resonance Raman Spectra
J. Phys. Chem. B, Vol. 101, No. 46, 1997 9643
similar to Chl a in that they are chlorins/dihydroporphyrins (one
saturated pyrrole ring) rather than bacteriochlorins/tetrahydro-
3
7
porphyrins (two saturated pyrrole rings). The key structural
element that distinguishes BChl c/d/e from Chl a is that the
C2-vinyl group of the latter pigment is hydrated in the former,
yielding an alcohol, CcH(OH)CdH3. The hydoxyl group of the
alcohol mediates the strong association of BChl c/d/e which
occurs both in chlorosomes and for free pigments in solution.37
The vibrational characteristics exhibited by Chl a and the other
Mg(II) complexes studied herein suggest that most of the modes
-
1
below 250 cm involve deformations of the peripheral sub-
stituent groups. Accordingly, the very strongly coupled very
low-frequency modes of BChl c/d/e most likely also involve
motions of these groups. Deformations of the unique CcH(OH)-
CdH3 group of the Bchl c/d/e pigments are the best candidates
for these vibrations. Deformations of this group could modulate
the interchromophore separation between and, hence, the
magnitude of the electronic coupling. The fact that deformations
of the substituent groups are invariably mixed with motions
involving the π-electron framework provides an additional
mechanism for modulating the electronic structure of the
aggregate. Together, the properties of BChl2 and the BChl c/d/e
aggregates suggest that modulation of electronic interactions
via peripheral substituent groups is a general motif for control-
ling electronic communication in photosynthetic assemblies.
Acknowledgment. We thank Professor K. M. Smith for
helpful suggestions concerning the preparation of DMPChl a.
This work was supported by Grant GM36243 (D.F.B.) from
the National Institute of General Medical Sciences.
References and Notes
(1) For recent treatises, see: (a) Chlorophylls; Scheer, H., Ed.; CRC
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I and II. (c) Anoxygenic Photosynthetic Bacteria; Blankenship, R. E.,
Madigan, M. T., Bauer, C. E., Eds.; Kluwer Acdemic Publishers: Dordrect,
Figure 9. Vibrational eigenvectors of low-frequency modes that contain
subtantial contributions from the C10-carbomethoxy group. Motions in
both the x-y pseudoplane of the macrocycle (arrows) and along the
z-axis (circles) are shown (see text).
1
995.
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(
(
-
1
frequency regime (<250 cm ) are due to deformations of the
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4
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3d,e
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3
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