Double helices of a pyridine-appended zinc chlorophyll derivative

Article abstract of DOI:10.1021/ja400493e

Self-assembled structures formed from a pyridine-appended zinc chlorophyll derivative are reported. While the zinc complex forms cyclic oligomers in chloroform solution, as indicated by ¹H NMR studies (including diffusion-ordered spectroscopy), vapor pressure osmometry, and cold-spray ionization mass spectrometry, it forms double-stranded helical coordination polymers in the solid state, as revealed by single-crystal X-ray analysis.

Full text of DOI:10.1021/ja400493e

Communication
pubs.acs.org/JACS
Double Helices of a Pyridine-Appended Zinc Chlorophyll Derivative
Yoshinao Shinozaki,† Gary Richards,† Keizo Ogawa,‡ Akihito Yamano,§ Kazuaki Ohara,∥
Kentaro Yamaguchi,∥ Shin-ichiro Kawano,⊥ Kentaro Tanaka,⊥ Yasuyuki Araki,# Takehiko Wada,#
and Joe Otsuki*,†
†College of Science and Technology, Nihon University, 1-18-14 Kanda Surugadai, Chiyoda-ku, Tokyo 101-8308, Japan
‡Nihon University Junior College, 7-24-1 Narashinodai, Funabashi-shi, Chiba 274-8501, Japan
§X-ray Research Laboratory, Rigaku Corporation, 3-9-12 Matsubara-cho, Akishima-shi, Tokyo 196-8666, Japan
∥Faculty of Pharmaceutical Science at Kagawa Campus, Tokushima Bunri University, 1314-1 Shido, Sanuki, Kagawa 769-2193, Japan
⊥Department of Chemistry, Graduate School of Science, Nagoya University, Furo-cho Chikusa-ku, Nagoya, Aichi 464-8602, Japan
#Institute of Multidisciplinary Research for Advanced Materials, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai 980-8577, Japan
S
* Supporting Information
solution and in the solid state. Zinc complex 2 forms cyclic
1
ABSTRACT: Self-assembled structures formed from a
pyridine-appended zinc chlorophyll derivative are re-
ported. While the zinc complex forms cyclic oligomers in
oligomers in chloroform, as indicated by extensive H NMR
studies, including diffusion-ordered spectroscopy (DOSY);
vapor pressure osmometry (VPO); and cold-spray ionization
mass spectrometry (CSI-MS).17 Single-crystal X-ray diffraction
(XRD) analysis revealed that 2 forms double-stranded helical
coordination polymers in the solid state. This is the first
double-stranded helical crystal structure formed by a porphyrin
analogue. This is also the first crystal structure of a pyridine-
coordinated assembly of a chlorophyll-derived compound,
although the crystal structures of pyridine complexes of
synthetic chlorin derivatives have been reported.18,19
1
chloroform solution, as indicated by H NMR studies
(including diffusion-ordered spectroscopy), vapor pressure
osmometry, and cold-spray ionization mass spectrometry,
it forms double-stranded helical coordination polymers in
the solid state, as revealed by single-crystal X-ray analysis.
upramolecular assemblies of porphyrin analogues have
Sdrawn considerable attention not only for the under-
standing of natural photosynthetic function but also for the
development of synthetic architectures for the absorption of
light and manipulation of excitation energy in materials
science.1,2 Nature uses (bacterio)chlorophyll-based assemblies
as light-harvesting antennae and electron relays in photo-
synthetic bacteria and chloroplasts in plants.3 One type of light-
harvesting antenna consists of chlorophyll−protein complexes,
such as LH1 and LH2 in purple photosynthetic bacteria as well
as light-harvesting complexes found in plants.4 Chlorosomes
found in green photosynthetic bacteria belong to another type
of antenna.5 They consist of agglomerates of bacteriochlor-
ophyll molecules called rod elements that are constructed only
through pigment−pigment interactions without a protein
scaffold.
1
In the H NMR spectrum of the free base 1 in CDCl3, the
signals for the α and β protons of the pyridine moiety appeared
at 8.81 and 7.68 ppm, respectively (Figure 1). Although these
1
Figure 1. H NMR spectrum of (a) free base 1 in CDCl3 and (b, c)
A number of model compounds to mimic the structure and
function of chlorosomes have been prepared.6−12 Most of the
synthetic analogues prepared to date closely follow their natural
counterparts and retain the functional groups believed to be
crucial for the formation of higher-order structures, including
the 31-hydroxy group. In the meantime, less attention has been
paid to the design of structurally diverse chlorophyll derivatives
that could also form novel, highly ordered assemblies. We have
examined the zinc complex of a chlorophyll derivative bearing a
pyridine moiety as a much less explored coordination site in
comparison with hydroxide groups, which may provide more
robust platforms for artificial antenna systems.13−16 Here we
report on the self-assembly of the pyridine-appended zinc
chlorophyll derivative 2 (see Figure 2 for the structure) in
zinc complex 2 in (b) THF-d8 and (c) CDCl3. Asterisks indicate
solvent and water peaks.
protons in 2 appeared in a similar region in tetrahydrofuran-d8
(THF-d8), they underwent marked upfield shifts to 3.40 and
6.11 ppm, respectively, in CDCl3. Signals corresponding to
other protons were also upfield-shifted by successively smaller
amounts as the distance between the protons and the pyridyl
group increased (Figure 2). The magnitudes of the upfield
shifts for the pyridine protons and the trend observed for the
Received: January 17, 2013
Published: March 25, 2013
© 2013 American Chemical Society
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solution to be 828 67 and 2600 190 g mol−1, respectively,
the latter being in good agreement with the value for the
tetramer of 2 (M = 2756 Da) (Figure S11). CSI-MS detected
ions from the monomer up to the pentamer (Figures S12−
S14). From all of the evidence combined, we concluded that 2
exists as stable, cyclic oligomers in solution, with the tetramer
being the predominant species.
Preliminary time-resolved measurements were performed to
probe the excited-state dynamics of the assembly. Excitation of
2 leads to the formation the singlet excited state, as
demonstrated by the transient absorption (TA) spectra (Figure
S15), which were taken in toluene as the materials decomposed
in CHCl3 under our TA measurement conditions. The
fluorescence of 2 (41 μM) in CHCl3 decayed biexponentially
with a major lifetime of 3.3 ns (92%) and a minor, fast
component of 0.47 ns (8%) (Figure S16). In pyridine, the fast
component was drastically different: a fast rising component
appeared (0.19 ns, 10%), while the long component was
slightly affected (3.6 ns, 90%). The rise was also observed in
CHCl3 in the presence of a small amount of pyridine (1−2%),
which would disrupt the assembly. Thus, the difference in the
dynamics of the excited states in CHCl3 and pyridine is not an
effect of the medium but may be ascribed to the cyclic
organization of the assembly. Further study will be needed to
clarify the nature of the rising component and the effects of the
assembly upon it.
Quite interestingly, XRD analysis of a single crystal obtained
from a mixture of CHCl3 and CH3CN using a liquid−liquid
diffusion method revealed that the zinc complex 2 forms
double-stranded coordination helices in the solid state (Figure
4; crystallographic data are summarized in Table S2 in the SI).
Two nonequivalent chlorophyll molecules are contained in the
unit cell (Figure S17). The coordination geometry of the zinc
ion of each molecule is square-pyramidal. The pattern of the
lengths of the bonds between the zinc ion and the inner
nitrogen atoms, among which that between the zinc ion and the
reduced pyrrole nitrogen is the longest, is in accord with that
for a reported zinc tetraphenylchlorin−pyridine complex
[ZnTPC(Py)].18 The displacements of the zinc ion out of
the plane of the central nitrogens are 0.26 and 0.30 Å, which are
somewhat less than that in ZnTPC(Py) (0.33 Å) (Table S3).18
Each of the nonequivalent chlorophyll molecules forms a
double helix, resulting in two nonequivalent double helices, one
of which is shown in bluish colors in Figure 4a,b. Both of the
double helices have similar gross features as follows. The
pyridine group in one molecule coordinates axially to the zinc
ion in the next molecule. The array of coordination makes a
right-handed helical structure with a pitch consisting of three
molecules of 2. Two such helices wrap around one another,
forming a double-helical structure. The two chains within the
same double helix run in the same direction, that is, the
pyridine→Zn bonds are oriented in the same direction, as
indicated by the two arrows in Figure 4a. On the other hand,
the other nonequivalent double helix (shown in reddish colors
in Figure 4c,d) runs in the opposite direction. The chlorophyll
molecules in one double helix make π−π stacking interactions
with molecules in the other oppositely running double helix,
with an intermacrocycle separation of ∼3.6 Å, apparently
mutually stabilizing the helices.
Figure 2. Chemical shift differences (δTHF‑d − δCDCl ) for zinc
complex 2.
8
3
other protons in CDCl3 are consistent with a self-assembled
structure in which the pyridine moiety of a molecule of 2
coordinates to the zinc center of another molecule of 2. These
upfield chemical shifts, including those for the α and β protons
of the pyridine moiety, showed little change over a temperature
range of 223−348 K [Figure S8 in the Supporting Information
(SI)]. Furthermore, these values were also almost independent
of concentration over a range of 0.1−10 mM (Figure S9). The
insensitivity of the chemical shifts to changes in temperature
and concentration over wide ranges, combined with the
appearance of a single set of proton signals for the molecular
structure, is inconsistent with the formation of linear oligomeric
structures in solution but instead points to the assembly of a
stable, well-defined discrete cyclic oligomer (or different-
membered cyclic oligomers) held together through pyridine−
zinc axial coordination.
Diffusion coefficients (D) of (6.37 0.20) × 10−10 and (3.43
0.05) × 10−10 m2 s−1 were obtained for free base 1 and zinc
complex 2, respectively, in CDCl3 (10 mM, 298 K) by means of
DOSY experiments (Figure S10). The hydrodynamic radii (r)
were then estimated using the Stokes−Einstein equation (eq
1),20
kBT
6πηD
r =
(1)
where kB, T, and η are the Boltzmann constant, absolute
temperature, and viscosity of the medium, respectively. The r
values obtained for 1 and 2 were 6.32 and 11.8 Å, respectively.
The radius for 1 is consistent with the dimensions of the
monomeric species (Figure 3), whereas the radius for 2 is about
twice that for 1, which is more or less in accord with the
dimensions of the cyclic tetramer.
The VPO data for 1 (M = 612 Da) and 2 (M = 689 Da) in
CHCl3 at 37 °C indicated the molar masses of the species in
Only a very limited number of crystal structures of
chlorophyll assemblies are known to date. Knapp and co-
workers reported a coordination polymer of a 31-oxime
derivative of zinc chlorophyll held together by axial
Figure 3. Molecular models of the (a) monomer and (b) cyclic
tetramer of zinc complex 2. The circles indicate the hydrodynamic
radii estimated from the DOSY measurements.
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Figure 4. Double-stranded helical structure of zinc complex 2. The colored arrows indicate the coordination direction (pyridine→Zn) of the
correspondingly colored helices. H atoms and solvent molecules have been omitted for clarity. A 3D animation for the pair of double helices can be
viewd in the SI. (a, b) One of the double helices. Zinc atoms are shown by space-filling models. (c, d) Two different helices packed with π−π
stacking interactions. Stacked chlorin rings are shown by space-filling models. (a) and (c) are views perpendicular to the c axis, while (b) and (d) are
views along the c axis.
coordination by the 131-carbonyl group.21 Very recently,
Tamiaki and co-workers reported another coordination
polymer of a zinc bacteriochlorophyll derivative held together
by coordination of the 17-propionyl carbonyl group to the zinc
ion.22 Both of them form staircaselike structures without any
helical turns. It is interesting to note that a tetraphenylporphyr-
in derivative functionalized with a vinylpyridine moiety at the β-
position also forms a staircase structure without any twist.23
The chirality of zinc complex 2 must play an important role in
the formation of the helical structure, but obviously chirality
alone is not a sufficient condition for achieving the helical
structure.
The double-stranded helical structure obtained in this work
has some implications for the design of artificial antennae for
efficient light harvesting. The axial coordination strategy via a
coordination site coplanar with the chlorophyll plane as
exemplified by 2 has an intrinsic weakness in the construction
of light-harvesting antennae because the chromophores organ-
ized in this coordination mode are arranged in mutually
perpendicular orientations. The perpendicular orientation is
strands alternatively in the double helix, even in the case that
intrastrand energy transfer is slow. This analysis demonstrates
that the double helices have a functional significance as a light-
harvesting antennae in addition to the aesthetic beauty. In this
particular crystal structure, inter-double-helix pathways should
be even more efficient because of the π−π overlap (Figure
4c,d) and parallel orientation.
For the double-helical structures reported herein, unlike
other staircase structures, isolation of each double helix may be
possible by peripheral modification of the molecular structure.
Such assemblies hold promise as light-harvesting antennae.2,25
Our work is directed toward revealing the structural require-
ments for the formation of such structures as well as
photophysical properties of these assemblies.
ASSOCIATED CONTENT
■
S
* Supporting Information
Preparation and characterization data for monomers and
assemblies of 1 and 2, crystallographic data (CIF), and a 3D
animation for 2 (QT). This material is available free of charge
via the Internet at http://pubs.acs.org.
unfavorable for Forster-type energy transfer, which relies on
̈
dipole−dipole interactions.2 Approximating the transition
dipole moments as lying in the direction of the diagonal line
connecting the nitrogen in pyrrole A bearing the pyridylvinyl
group and the nitrogen in pyrrole C,24 we calculated the factors
κ2/r6, where κ2 is the orientation factor and r is the
interchromophore center-to-center distance (Figure S18).
These factors are expected to be proportional to the energy
transfer rates among the chromophores in the double helices in
the crystal. As expected, energy transfer along the intrastrand
pathways is not efficient, with κ2/r6 values of 7−9 × 10−9 Å−6
between the nearest neighbors in the same strand due to
vanishingly small orientation factors (κ2 = 0.03−0.05).
However, the κ2/r6 factors are 2 orders of magnitude larger
(225 × 10−9 and 162 × 10−9 Å−6) between nearest neighbors
residing in complementary strands. Even the κ2/r6 factors
between next-nearest neighbors residing in complementary
strands are large (166 × 10−9 and 157 × 10−9 Å−6) because of
favorable orientations (κ2 = 1.42 and 1.51, respectively). Thus,
the double-helical architecture confers efficient, contiguous
interstrand energy transfer pathways along which energy
migrates among chromophores belonging to complementary
AUTHOR INFORMATION
■
Corresponding Author
otsuki.joe@nihon-u.ac.jp
Notes
The authors declare no competing financial interest.
ACKNOWLEDGMENTS
■
This work was partly supported by the Nanotechnology
Excellence, Nihon University “N.” Research Project and by a
Grant-in-Aid for Scientific Research (C) (24550163) from the
MEXT, Japan.
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