(96e) Photo-Induced Polymerization and Reconfigurable Assembly of Multifunctional Ferrocene-Tyrosine

Self-assembly
inspired by nature has received tremendous attention owing to their unique
physicochemical and biological properties, which make them great candidates for
applications in many fields. Melanins are natural pigments that are widely present in plants, bacteria,
and animals, providing ultraviolet light protection and free radical
scavenging. Melanins are produced in melanocytes by the tyrosinase-catalyzed
oxidation of trypsine, followed by polymerization. Due to their broad band
adsorption, redox activity and chelating ability, considerable efforts have
been devoted to the self-assembly of melanin or melanin-like materials,
including eumelanin films and polydopamines with promising applications in
energy, environmental and biomedical fields.

Peptide
is a kind of versatile building blocks for the fabrication of highly ordered
materials due to their capability to form various intermolecular non-covalent
bonds (hydrogen bond, ¦Ð-¦Ð stacking, hydrophobic interactions, etc). The
chemical modifiability and biocompatibility of peptides make them excellent
candidates for the construction of highly ordered melanin-like materials via
simultaneous covalent and non-covalent self-assembly. Recently, Ulijn et al.
studied the use of tyrosine-containing tripeptides as tunable precursors and
tyrosinase as the catalyst to form polymeric pigments. These pioneering work
offers new insights into the rational design of melanin-inspired nanomaterials.
However, the wider applications of such biomaterials require us to develop molecular
building blocks with new functionalities.

The ferrocene (Fc) modified peptides have been attracting
increasing interests in recent years. Due to the unique molecular configuration
and redox activity, the ferrocene-peptides could self-assemble into diverse
nanostructures such as fibers, nanohelix, and nanoemulsions with intrinsic
redox activity and tunable chiroptics. Herein, we designed a simple
biomolecule: ferrocene-tyrosine (Fc-Y), a short conjugate that was designed to
couple the redox-active group (Fc) with a photosensitive amino acid (tyrosine).
The Fc-Y monomers could spontaneously self-assemble into nanospheres in water
driven by non-covalent interactions. Photoradiation was then used to induce the
oxidation and polymerization of the monomers within the nanospheres. In this
process, we observed a structural transition from solid nanosphere with a
smooth surface to hollow vesicle with a shell composed of lamellar stacking
architectures. The results indicated that the photoradiation could be used to
tune the self-assembly of molecules into diverse nanostructures with
reconfigurable architectures. Moreover, the melanin-like bioorganometallic nanostructures formed by non-covalent and
covalent interactions exhibited reducing property for in situ biomineralization of gold nanoparticles,
which could serve as enzyme mimics with tunable activity for the cascade
catalytic reactions. The nanoparticles also exhibited redox activity due to the
Fc and tyrosine moieties, which could serve as promising biomaterials for superior energy storage. The
results
provide a feasible strategy for the assembly of highly dynamic
and multifunctional materials
by integrating the merits of both bioorganometallic components and biomimetic
photopolymerization.

For the synthesis of the versatile nanospheres, the
ferrocene-tyrosine (Fc-Y) molecules were dissolved in water at 1 mg mL^-1,
and then self-assembled directly under different light conditions for 24 h.
After fully self-assembly, the supramolecular assemblies exhibited different
apparent morphology (Figure 1a).
Self-assembly under darkness gave a transparent yellow solution, while the
visible light treatment obtained a brown suspension, and the UV irradiation
yielded a dark brown suspension. Transmission electron microscopy (TEM) and
high-magnification scanning electron microscopy (SEM) were used to investigate
the microscopic morphology of the supramolecular nanostructures. The uniform
nanospheres with smooth surfaces were obtained by the darkness (Figure 1c and d) and the visible light
treatment (Figure 1c and e). Dynamic
light scattering (DLS) indicated that the nanospheres had average diameters of
480 nm and 663 nm, respectively, which were consistent with the statistics of
SEM analysis. Intriguingly, by UV irradiation, we yielded hollow vesicles with
a shell composed of the lamellar structures (Figure 1f-h), and the diameter was influenced by irradiation
wavelength. DLS results revealed that the average size of the vesicles was 142
nm for 365 nm UV, and 205 nm for 254 nm UV (Figure 1b), which was also in accordance with the statistics of SEM
analysis.

Figure 1. Self-assembly of Fc-Y under different
light irradiation. a) Photograph images showing the Fc-Y aqueous solutions
incubated for 24 h under various light conditions. From left to right, the
light condition is darkness, visible light, 365 nm UV, and 254 nm UV,
respectively. b) Size distribution of the prepared nanostructures derived from
the DLS analysis. 3D models c, f) and high-magnification TEM images of the nanospheres
and nanovesicles formed under d) darkness, e) visible light, g) 365 nm UV, and
h) 254 nm UV irradiation, respectively.

The great difference between the nanospheres and vesicles was
evident in secondary structures and morphologies. Inspired by melanin, we
studied the polymerization of Fc-Y molecules under UV irradiation. We
speculated that similar to the melanogenesis, under UV irradiation, the Fc-Y
first transformed into ortho-phenol (DOPA), and then oxidized to ortho-quinone.
Finally, the following UV irradiation would induce the oxidized Fc-Y molecules
to produce radicals, and two Fc-Y radicals would react, leading to the
formation of di-(Fc-Y). Through the proton-coupled electron transfer, the
di-(Fc-Y) radicals would be produced. Then the tri-(Fc-Y) was formed by the
further reaction of free tyrosine radicals with di-(Fc-Y) radicals, and leading
to the progress of the crosslinking reaction. So the tetra-(Fc-Y) was formed by
the reaction of free tyrosine radicals with tri-(Fc-Y) radicals or di-(Fc-Y)
radicals. In the whole photo-induced crosslinking process, the possible
resulting covalent crosslinks are DOPA, ortho-quinone, and polymers with
different polymerization degrees.

Combining with the TEM images and spectrum analysis, we
speculated that during the crosslinking reaction induced by UV, the Fc-Y
monomers first self-assembled rapidly into the uniform nanospheres, which was
kinetically controlled process (Figure
2b). Under the UV irradiation, the molecules located on the surface of the
nanospheres were oxidized to the ortho-quinone and polymerized into oligomers
(di-(Fc-Y), tri-(Fc-Y), and tetra-(Fc-Y)), which would nucleate and reassemble
into tiny pieces at the surface of the nanospheres (Figure 2a¢ñ). Furthermore, the continuous UV irradiation induced the
internal Fc-Y monomers within the nanospheres to migrate to the exterior
surface and be oxidized to the oligomers, resulting in the hollow nanovesicles
with a rough surface (Figure 2a¢ò, 2c-f).
This process was similar to that of the chemical etching, which was frequently
used for the fabrication of inorganic hollow nanostructures. Finally, when all
of the Fc-Y molecules converted to the crosslinking oligomers, the polymers
would reassemble into uniform nanovesicles composed of the lamellar structures
(Figure 2a¢ó, 2g). The results
indicated that the photo-induced covalent and non-covalent self-assembly was a
dynamic process, in which the morphology could be controlled by irradiation
wavelength, time, and strength, thus providing a feasible strategy for the
fabrication of reconfigurable materials with unique properties.

Figure
2. a) Schematic illustration of the
photo-induced reconfigurable
self-assembly of Fc-Y via simultaneous non-covalent and covalent polymerization. b-g)
Representative TEM images of the intermediate structures during the transition
of nanospheres into covalent crosslinked hollow vesicles under UV irradiation.

To
deal with the environment pollution and develop the low-carbon-emission
economy, tremendous efforts are being made to advance energy storage and
conversion, such as lithium-ion batteries (LIBs), and supercapacitors (SCs). The
prepared Fc-Y nanospheres and nanovesicles were configured to the cathodes in a
three-cathodes system (Figure 3a),
the discharge measurements were applied to investigate the energy storage
capacity. For all of the systems investigated, the potentials got more negative
during the discharge, indicating the disorder of the applied materials. By
using cathodes modified with different Fc-Y nanostructures, we could gain very
high specific capacities. It is worth noting that in the discharge
measurements, the nanospheres self-assembled under visible light irradiation
exhibited the highest specific capacity (Figure
3b,
c) of 31 mAh g^-1, which is over
twice of the maximum value reported so far by using peptide assemblies as
supercapacitors. The very high specific capacity of the non-crosslinking
nanospheres could be attributed to the largest amount of redox-active
substances (both ferrocene group and tyrosine. The results indicated that the
self-assembled ferrocene-tyrosine nanostructures could serve as promising
candidates for energy storage.

Figure
3.
a) Schematic illustration of the three-electrode system used for discharge measurements.
The nickel foam coated with self-assembled nanostructures was used as working
electrode, the platinum sheet was used as counter electrode, and the saturated
calomel electrode (SCE) was used as reference electrode. The electrolyte was
0.5 M KCl aqueous solution. b) Electrochemical potential and c) average
specific capacity of the self-assembled nanostructures formed under different
light irradiation.

In
summary, we reported the photo-induced non-covalent and covalent self-assembly
of a simple ferrocene-tyrosine (Fc-Y) conjugate. This allowed us to fabricate
reconfigurable nanostructures in water with controlled diameter and
hierarchical structures. The uniform nanospheres with smooth surface (400-700
nm in diameter) were prepared by the non-covalent self-assembly under visible
light irradiation and dark condition, while the dynamic nanovesicles composed
of stacked lamellar structures (100-300 nm in diameter) were obtained by
photo-crosslinking of the Fc-Y monomers. The melanin-like materials with
reducing property and redox
activity could be used as templates for the in
situ biomineralization of gold nanoparticles,
biomimetic catalysis, and as
biomaterials for superior energy storage. The results
offer great promise to
assemble
multifunctional
materials with potential
applications in various fields by integrating the merits of both bioorganometallic components and biomimetic photopolymerization.