Phthalocyanine–Virus Nanofibers as Heterogeneous Catalysts for Continuous-Flow Photo-Oxidation Processes

Article abstract of DOI:10.1002/adma.201902582

The generation of highly reactive oxygen species (ROS) at room temperature for application in organic synthesis and wastewater treatment represents a great challenge of the current chemical industry. In fact, the development of biodegradable scaffolds to support ROS-generating active sites is an important prerequisite for the production of environmentally benign catalysts. Herein, the electrostatic cocrystallization of a cationic phthalocyanine (Pc) and negatively charged tobacco mosaic virus (TMV) is described, together with the capacity of the resulting crystals to photogenerate ROS. To this end, a novel peripherally crowded zinc Pc (1) is synthesized. With 16 positive charges, this photosensitizer shows no aqueous aggregation, and is able to act as a molecular glue in the unidimensional assembly of TMV. A step-wise decrease of ionic strength in mixtures of both components results in exceptionally long fibers, constituted by hexagonally bundled viruses thoroughly characterized by electron and confocal microscopy. The fibers are able to produce ROS in a proof-of-concept microfluidic device, where they are immobilized and irradiated in several cycles, showing a resilient performance. The bottom-up approach also enables the light-triggered disassembly of fibers after use. This work represents an important example of a biohybrid material with projected application in light-mediated heterogeneous catalysis.

Full text of DOI:10.1002/adma.201902582

CommuniCation
Heterogeneous Catalysts
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Phthalocyanine–Virus Nanofibers as Heterogeneous
Catalysts for Continuous-Flow Photo-Oxidation Processes
Eduardo Anaya-Plaza, Ana Aljarilla, Grégory Beaune, Nonappa, Jaakko V. I. Timonen,
Andrés de la Escosura, Tomás Torres,* and Mauri A. Kostiainen*
Visible-light-mediated oxidation is a fast-
The generation of highly reactive oxygen species (ROS) at room
developing field with applications in
organic synthesis[1] and wastewater treat-
ment.[2,3] In particular, molecular oxygen
as oxidation source has gained focused
attention, as it is considered as an envi-
ronmental-friendly approach.[4] In this
direction, organic chromophores such as
porphyrinoids have been employed to con-
vert nonreactive O2 into reactive oxygen
species (ROS) at room temperature, with
wide application in nanomedicine[5,6] and
catalysis.[7] Dye-containing heterogeneous
catalysts can be easily separated from the
reaction medium, offering advantages for
scale-up and continuous-flow processes.
Highly ordered structures, such as metal–
organic frameworks, have been exploited
in this direction as scaffolds to support
photoactive molecules in a biomimetic
approach.[7,8] However, even if the photo-
oxidation process itself is as environmen-
tally friendly as possible, a major drawback
of these catalysts active sites or structural
scaffolds rely on heavy metal atoms.[9–11]
These undesirable components represent
an environmental hazard and, therefore,
temperature for application in organic synthesis and wastewater treatment
represents a great challenge of the current chemical industry. In fact, the
development of biodegradable scaffolds to support ROS-generating active
sites is an important prerequisite for the production of environmentally
benign catalysts. Herein, the electrostatic cocrystallization of a cationic
phthalocyanine (Pc) and negatively charged tobacco mosaic virus (TMV)
is described, together with the capacity of the resulting crystals to
photogenerate ROS. To this end, a novel peripherally crowded zinc Pc (1)
is synthesized. With 16 positive charges, this photosensitizer shows
no aqueous aggregation, and is able to act as a molecular glue in the
unidimensional assembly of TMV. A step-wise decrease of ionic strength in
mixtures of both components results in exceptionally long fibers, constituted
by hexagonally bundled viruses thoroughly characterized by electron and
confocal microscopy. The fibers are able to produce ROS in a proof-of-
concept microfluidic device, where they are immobilized and irradiated in
several cycles, showing a resilient performance. The bottom-up approach
also enables the light-triggered disassembly of fibers after use. This work
represents an important example of a biohybrid material with projected
application in light-mediated heterogeneous catalysis.
development of biodegradable supported catalysts is of para-
mount importance.
Dr. E. Anaya-Plaza, Dr. Nonappa, Prof. M. A. Kostiainen
Department of Bioproducts and Biosystems
Aalto University
Proteins are one of the most functional and versatile bio-
macromolecules employed by nature in molecular recognition,
transport, and catalysis. Creating highly ordered structures via
bottom-up assembly of proteins and designed synthetic mate-
rials, can lead to fascinating functional biohybrids that combine
the best features of biological and synthetic matter.[12,13] Among
all the chemical assembly strategies employed,[14,15] electrostatic
interactions present important advantages. For example, they
enable the use of native proteins without genetic or chemical
modification and offer the possibility to design multistimuli
assembly/disassembly processes, capital in the design of
responsive materials.[16,17] The role that shape,[18] electrostatic
potential,[19–21] and specific nearest neighbor interactions of the
protein scaffold plays in the crystallization process is well-estab-
lished.[22,23] Importantly, strategies to control the interaction
between the protein and the cocrystallization agent by means
of pH and ionic strength of the aqueous media has enabled
fine tuning in the kinetics of the assembly process, leading to
high structural control. Recent examples of protein crystal scaf-
folds with catalytic activity indicate that biohybrids can function
Kemistintie 1, 02150 Espoo, Finland
E-mail: mauri.kostiainen@aalto.fi
Dr. A. Aljarilla, Dr. A. de la Escosura, Prof. T. Torres
Department of Organic Chemistry
Universidad Autónoma de Madrid (UAM)
Calle Francisco Tomás y Valiente, 7, 28049 Madrid, Spain
E-mail: tomas.torres@uam.es
Dr. G. Beaune, Dr. Nonappa, Prof. J. V. I. Timonen
Department of Applied Physics
Aalto University School of Science
Puumiehenkuja 2, FI-02150 Espoo, Finland
Dr. A. de la Escosura, Prof. T. Torres
Institute for Advanced Research in Chemical Sciences (IAdChem)
UAM
Campus de Cantoblanco, 28049 Madrid, Spain
Prof. T. Torres
IMDEA-Nanociencia
Campus de Cantoblanco, 28049 Madrid, Spain
The ORCID identification number(s) for the author(s) of this article
can be found under https://doi.org/10.1002/adma.201902582.
DOI: 10.1002/adma.201902582
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as efficient catalysts.[24–27] While protein cages such as (apo)
ferritin or cowpea chlorotic mottle virus have coped the most
recent developments in 3D electrostatic assemblies, other pro-
tein scaffolds such as tobacco mosaic virus (TMV) have been
recently explored, yielding unidimensional morphologies.[28]
Among the porphyrinoids available, phthalocyanines (Pc)
hold a prominent place due to their outstanding optical prop-
erties.[29–31] These non-natural photosensitizers consist of four
isoindole units linked through nitrogen atoms, which are
extendedly conjugated and yield intense absorption in the red/
near-infrared region of the visible spectrum. In particular, zinc
derivatives (ZnPc) present a characteristic sharp absorption
band between 670–700 nm, as well as moderate to high fluores-
cence quantum yields. Furthermore, ZnPc are reported to pro-
duce ROS, a compendium of highly reactive oxidation agents
such as superoxide, peroxides, and singlet oxygen, which can
be utilized in photodynamic therapy, diagnostic arrays, and
catalysis. We have previously reported spherical protein cage-
Pc cocrystal with maintained light-induced excited state prop-
erties.[32] Herein, we report the enhanced properties arising
from the cocrystallization between rod-like TMV and a highly
charged ZnPc via electrostatic interactions into highly ordered
fibers. Immobilization of the dye in fibers, in comparison with
the dye free in solution, yields a heterogeneous catalyst allowing
rapid purification by physical methods. Additionally, the high
aspect ratio of the fibers gives a high contact area with the
media. On the other hand, the use of responsive self-assembled
biohybrids allows us to dispose them with the adequate stimuli,
yielding exclusively biodegradable material. Such assemblies
can be used as aqueous media oxidizing agents with potential
application in green organic chemistry and water treatment.
The use of Pc in aqueous media is associated with several
challenges, such as lack of solubility, high hydrophobicity,
and aggregation, compromising their performance. In order
to circumvent these issues, we have designed and synthe-
sized a novel ZnPc bearing eight 2,6-bis-(3-methylpyridinium)
phenyloxy moieties (1) at the β position of the isoindole units
(Figure 1a). The challenging synthesis of this unique chromo-
phore was accomplished in four main steps (Scheme S1, Sup-
porting Information). Briefly, 2-benzyloxy-1,3-dibromobenzene
was coupled with pyridin-3-ylboronic acid via Suzuki–Miyaura
reaction which, after deprotection, yielded 2,6-(bis(pyridine-
3-yl))phenol. Second, nucleophilic aromatic substitution of
4,5-dichlorophthalonitrile with the previously synthesized
phenol led to the desired disubstituted phthalonitrile exclu-
sively under highly energetic microwave radiation. Otherwise,
thermal reaction in the same conditions yielded the mono-
substituted derivative due to the high steric hindrance of the
nucleophilic groups. The third step consisted on the cyclo-
tetramerization of the described phthalonitrile in the pres-
ence of Zn(OAc)2, resulting into the precursor phthalocyanine
bearing 16 pyridine groups (compound 8 in the Supporting
Information). Last, permethylation of 8 in presence of methyl
iodide resulted in the water soluble ZnPc 1. The substitution
pattern in this molecule renders a unique photosensitizer with
enhanced performance in aqueous media. Peripheral decora-
tion directs the 16 positively charged moieties out of the ZnPc
plane (Figure 1b), hindering the typical columnar aggrega-
tion through π–π stacking in aqueous environment, which is
Figure 1. a) Chemical structure of ZnPc 1. Iodide counterions are
omitted for clarity. b) 3D structure obtained by ab initio calculations
at semiempirical level (PM3). Pyridinium moieties shown as spheres.
c) Absorption and d) emission spectra of 1 at 0 and 200 × 10−3 m of NaCl.
known to quench excited-state properties such as fluorescence
and ROS production. This was clearly shown by the sharp
absorption band observed in a broad range of salt concentra-
tions (Figure 1c), as well as maintained emission when excited
at 615 nm (Figure 1d). On the other hand, other water soluble
ZnPc bearing eight N-methylpyridinium moieties (compound 9
in the Supporting Information) presented a strong aggregation
by increasing NaCl concentration, as shown by the band shift
from 675 to 635 nm as well as a complete emission quench
(Figure S1, Supporting Information).
TMV is a helical array of 2130 coat proteins of an approxi-
mate molecular weight of 17 kDa, wrapping the viral RNA. This
results in a 300 nm long, 18 nm diameter rod-like virus with
an estimate molecular weight of 39.4 MDa (Figure 2a,b). This
geometry, which renders a negatively charged helix on the outer
surface of the virus at pH above 4.5,[33] can function as a well-
defined scaffold for unidimensional ensembles. TMV has been
employed as drug delivery platform,[34–36] as well as building
block in different biohybrid arrays together with small func-
tional molecules,[37] or nanoparticles.[28,38,39]
In order to understand how 1 and TMV interact, the satu-
ration ratio (i.e., full coverage of TMV by photosensitizers)
between 1 and TMV was determined by dynamic light scat-
tering (DLS). TMV concentration was fixed at 0.1 mg mL−1 and,
assuming a molecular weight of 39.4 MDa, increasing ratios
between 0 and 25 000 equivalents of 1 were added. We observed
the decrease of the peak at 300 nm, which corresponds to the
unimeric TMV, while a new peak above 2000 nm arises, which
corresponds to aggregated TMV (Figure 2c). Monitoring the
derived count rate, we found the initial increase of the signal
above 1000 equivalents, establishing the starting point of
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and finally 0 × 10−3 m of NaCl, yielding the aforementioned
fibers. This electrostatically driven assembly is fully reversible
and the fibers show disassembly upon increasing the ionic
strength (Figure S2, Supporting Information).
The resulting complexes were structurally characterized by
different techniques (Figure 3). Optical microscopy images
show the fibrous morphology of the bundles, with thread
lengths in the hundreds of micrometers and thicknesses
between 1–2 µm (Figure 3a). Taking into account the TMV
dimensions (300 × 18 nm), this morphology is the conse-
quence of a spontaneous highly directional assembly process,
where TMV acts as self-assembling building block, providing a
protein-based scaffold that supports the photosensitizer. Small
angle X-ray scattering (SAXS, Figure 3b) measurements reveal
that the fibers present 2D hexagonal packing perpendicular
to the fiber vector. Three main diffraction peaks (q = 0.0354,
0.0632, and 0.0727 Å−1) were found, which correspond to the
reflections from (10), (11), and (20) planes, respectively. Linear
fitting of the squared diffraction peak indices as a function of
the measured q-values yields a lattice constant of a = 20.1 nm
(Figure 3c). This is in good agreement with the typical packing
of highly concentrated TMV,[42] or in presence of atomic cat-
ions[41,43] or small-size AuNPs.[28] The observed lattice para-
meter is slightly higher than the TMV diameter (i.e., 18 nm),
which is in close agreement with the proposed model. On the
other hand, direct combination of 1 and TMV capsids in acetate
buffer 10 × 10−3 m pH 5.5 in the absence of NaCl results in the
immediate sedimentation of a green-colored fibrous complex.
Observed under the optical microscope, the fibers are shorter
and thicker (Figure S3, Supporting Information). These quickly
assembled fibers do not show any scattering peaks in SAXS
analysis because of their amorphous structure.
Further structural insight of the highly ordered fibers was
obtained by ambient- and cryo-electron microscopy (Figure 3d–f).
High-magnification images of the fibers confirm the parallel
alignment and side-by-side packing of the individual viruses.
No periodic order along the fiber axis was observed, which sup-
ports the 2D structure obtained by SAXS. Additionally, cryo-TEM
(transmission electron microscopy) images show similar features
as observed in the macroscale, such as twists and bifurcations
(Figure 3f). The helical twists were 3D reconstructed, showing a
transfer of the chirality from the individual virus to the bundle.
As shown in Figure 3g, right-handed helicity was found, which
is in good agreement with previously reported TMV bundles.
As a consequence of the anisotropy inherent to 1D ordered
materials, the fibers present birefringence of polarized light
(Figure 4a). They show strong blue color when oriented 45°
respect the crosspolarizers, in opposition to other possible ori-
entations (Figure S4, Supporting Information). Otherwise, the
interaction with the virus does not affect the optical properties
of 1, as shown by the sharp absorption of the hybrid at 692 nm
(Figure 4b). This confirms the unaltered excited state proper-
ties of 1 even when packed with TMV. In fact, strong fluores-
cence of the fibers can be observed when irradiated at 633 nm.
This property opens up new characterization possibilities like
confocal microscopy, which offers better resolution than optical
microscopy. Hybrids shown in Figure 4c were characterized
with this technique and the images reinforce the hypothesis of
the hierarchical fiber ensemble of smaller threads.
Figure 2. a) Structure model and b) TEM image of TMV. c) DLS inten-
sity profiles of TMV (0.1 mg mL−1) in presence of 0, 15 000, and 25 000
equivalents of 1 (black, red, and blue dots, respectively). d) Derived count
rate of TMV (0.1 mg mL−1) in presence of increasing ratios of 1, showing
saturation above 15 000 equivalents. e) Schematic representation of the
step-wise approach to obtain crystalline hybrids, showing no interaction
at high ionic strength (150 × 10−3 m NaCl) and high-ordered materials at
low ionic strength (0 × 10−3 m NaCl).
assembly, while the saturation point was reached above 15 000
equivalents (Figure 2d). However, previously reported assembly
of TMV shows concentration dependence.[40,41] In fact, when
the concentration of the virus has risen to 10 mg mL−1, satu-
ration of the virus is reached above 10 000 equivalents, as we
observe the precipitate formation, while a deep-colored super-
natant remains. Therefore, unless stated otherwise, a ratio of
10 000 was employed in the following experiments.
Electrostatically assembled protein crystals are highly
dependent on the ionic strength of the media. Therefore, prep-
aration of high aspect-ratio fibers was achieved by step-wise
decrease of the NaCl concentration in the media (Figure 2e).
TMV and 1 were mixed in acetate buffer 10 × 10−3 m pH 5.5
containing 150 × 10−3 m of NaCl and no complex formation was
observed. The solution was dialyzed against the same buffer
containing 125 × 10−3, 100 × 10−3, 75 × 10−3, 50 × 10−3, 25 × 10−3,
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Figure 3. Structural characterization of the 1-TMV fibers. a) Optical microscopy image showing the fibers and their entanglement. b) SAXS measured
(line) of the hybrids. The simulated data (dots) were calculated assuming a = 20.1 nm. c) The squared diffraction peak indices plotted as a function of
the measured q-values. A linear fit yields a = 18.5 nm for a 2D hexagonal lattice. d) TEM image showing the 1-TMV fibers and e) their fine structure,
constituted by parallel alignment of individual TMV capsids. f) Cryo-EM image of the biohybrids, showing features of their higher order organization
in: 1) twists and 2) bundles to form bigger fibers. g) A cryo-ET density map of a twist, showing right-handed helicity.
Utilizing compound 1 as a molecular glue in the aforemen-
tioned biohybrids present several advantages, such as high
solvent-accessible surface, which yields an ideal platform for
heterogeneous photo-oxidation. In our approach, we hypoth-
esize that 1 maintains its ROS generation ability despite the
fact that it is immobilized within the biohybrid. In order to
demonstrate this, ROS photogeneration was monitored by the
well-known fluorescence indicator 2′,7′-dichlorodihydrofluo-
rescein (H2DCF) which oxidizes in presence of ROS to highly
fluorescent 2′,7′-dichlorofluorescein (DCF, Figure 5a). The
fibers were placed on a glass slide, covered with 750 × 10−6
m
H2DCF and then irradiated by excitation at 488 nm (green) and
633 nm (red). The former excites the sensor, while the latter
excites the 1-TMV fibers. Images were taken in a continuous
way (each being the average of four images, 1.96 s per frame).
We observed the DCF intensity increasing over the time exclu-
sively in the near proximity of the fiber bundles (Figure 5b), as
a consequence of the ROS photogeneration. On the other hand,
areas without fibers present no emission in neither wavelength,
serving as a negative control. Photo-oxidation dependence on
molecular oxygen present in the media as well as the ZnPc was
demonstrated in control experiments (Figures S5 and S6, Sup-
porting Information).
One challenge of photochemical oxidation in aqueous media
is to transfer this potential into continuous flow setups. How-
ever, our fiber-like morphology allowed to immobilize the bun-
dles inside a proof-of-concept device (Figure S7, Supporting
Information) consisting of a rectangular cross-section capil-
lary (0.2 × 2.0 × 50 mm). The capillary was fed with H2DCF
750 × 10−6 m in acetate buffer (10 × 10−3 m pH = 5.5), in order
to maintain the conditions as close as possible to the forma-
tion of the fibers. Controlling the inlet flow and irradiation
conditions allowed us to test the reproducibility of the ROS
Figure 4. a) Optical (left) and polarized light (right) microscopy images.
The latter was taken between crosspolarizers, aligned as shown in top-right
corner vectors. b) Normalized absorption spectra of the 1-TMV hybrid (red),
compared to the TMV (black) and 1 (blue) in acetate buffer (10 × 10−3
pH = 5.5). c) Confocal microscopy image of the hybrids (λexc = 633 nm).
m
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Figure 5. a) Schematic representation of the photoinduced oxidation process. Absorption of red light (λexc = 633 nm) by the chromophore induces the
excitation of molecular oxygen present in the media to ROS, which oxidizes the precursor (H2DCF, nonfluorescent) into DCF (λexc = 488 nm). Note that
the peripheral substituents of 1 have been omitted for clarity purposes. b) Time-lapse emission microscopy images of the bundled fibers (red) and in
situ photo-oxidized DCF (green). H2DCF is present at 750 × 10−6 m in acetate buffer (10 × 10−3 m pH = 5.5). c) Averaged and normalized increase of
DCF (black) and decrease of 1 (red) after 2 min irradiation (60 frames) per cycle. The error bars correspond to the standard deviation of three bundles.
Normalized data to the end value of the first cycle (DCF) and the initial emission 1. d) Emission (left) and bright field (right) microscopy images of
fibers before (top) and after (bottom) intense irradiation, showing the photobleaching of the ZnPc and, as consequence, loss of their structural stability.
photogeneration and stability of the fibers under irradiation.
In this setup, previously described irradiation conditions were
employed, obtaining similar results after 2 min of continuous
irradiation. Fluorescence intensity of DCF (green channel)
was measured as the average of three circular ROI within the
bundle and corrected with the average of three circular ROI
far from the bundle, which serves as background signal. In a
similar way, emission intensity of 1 was measured employing
the same ROI in order to measure the fiber photostability. Sub-
sequent washing with fresh H2DCF solution (≈6 µL s−1 over
15 s) washed-out the remaining DCF without detaching
the fibers, allowing us to repeat over 10 cycles. The average
obtained from three bundles was plotted (Figure 5c). First, we
observed remarkable stability of the fibers to the process: red
intensity decreases just above 10% after 10 cycles (20 min of
continuous irradiation). Additionally, no important intensity
loss is observed between cycles, which support the effective
immobilization of the fibers into the channel. Second, ROS
production is consistent and stable, with a slight decrease in
the final intensity due to the slight loss of photosensitizer.
One of the main advantages of supramolecularly assem-
bled materials is their ability to disassemble under given
stimuli. In our case, there is an opportunity to dispose the
active material once the desired photo-oxidation has been
achieved. To this end, the fibers were irradiated with laser
intensities 20 times higher than the one used in the previous
experiment. After a few seconds of irradiation, we observed
a fast decrease in the emission as a consequence of the
photobleaching of 1, which triggers the dissolution of the
samples as shown in the bright field images (Figure 5d). This
results in a green solution to the disposal of the active mate-
rials, in opposition to the nonsoluble inorganic materials typ-
ically used in catalysis.
In conclusion, we have designed, synthesized, and charac-
terized a new biohybrid material obtained by the electrostatic
interaction between the TMV capsid and a specifically designed
ZnPc, yielding a unique morphology with optical activity. The
chromophore presents 16 positive charges and resilient optical
properties in aqueous media of varying ionic strengths. The
cationic chromophore can act as molecular glue and direct
the assembly of the rod-like viruses into hexagonally packed
fibers. Additionally to their interesting structural features, the
resulting high aspect-ratio fibers maintain the optical properties
of the dye, namely, fluorescence and singlet oxygen production.
The first one allowed us to characterize the fibers by confocal
microscopy. The second enabled us to demonstrate that the
fibers are easily immobilized in capillaries, while their sin-
glet oxygen production remains stable after several oxidation/
flushing cycles. In addition, our self-assembly approach offers
the possibility to disassemble the fibers by laser irradiation.
This work represents a new approach to tackle continuous-flow
photo-oxidation processes in aqueous media.
Supporting Information
Supporting Information is available from the Wiley Online Library or
from the author.
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Keywords
heterogeneous catalysis, phthalocyanines, reactive oxygen species, self-
assembly, viral capsids
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D. Bochicchio, G. M. Pavan, O. Ikkala, R. H. A. Ras, M. A. Kostiainen,
ACS Nano 2018, 12, 8029.
Received: April 23, 2019
Revised: June 10, 2019
Published online:
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