Supramolecularly Assembled Nanocomposites as Biomimetic Chloroplasts for Enhancement of Photophosphorylation

Article abstract of DOI:10.1002/anie.201812582

Prototypes of natural biosystems provide opportunities for artificial biomimetic systems to break the limits of natural reactions and achieve output control. However, mimicking unique natural structures and ingenious functions remains a challenge. Now, multiple biochemical reactions were integrated into artificially designed compartments via molecular assembly. First, multicompartmental silica nanoparticles with hierarchical structures that mimic the chloroplasts were obtained by a templated synthesis. Then, photoacid generators and ATPase-liposomes were assembled inside and outside of silica compartments, respectively. Upon light illumination, protons produced by a photoacid generator in the confined space can drive the liposome-embedded enzyme ATPase towards ATP synthesis, which mimics the photophosphorylation process in vitro. The method enables fabrication of bioinspired nanoreactors for photobiocatalysis and provides insight for understanding sophisticated biochemical reactions.

Full text of DOI:10.1002/anie.201812582

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Accepted Article
Title: Supramolecularly Assembled Nanocomposites as Biomimetic
Chloroplasts for Enhancement of Photophosphorylation
Authors: Yue Li, Xiyun Feng, Anhe Wang, Yang Yang, Jinbo Fei,
Bingbing Sun, Yi Jia, and Junbai Li
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To be cited as: Angew. Chem. Int. Ed. 10.1002/anie.201812582
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Supramolecularly Assembled Nanocomposites as Biomimetic
Chloroplasts for Enhancement of Photophosphorylation
#
[a,b]
#[a,c]
#[a,d]
[b]
[a]
[a,e]
[a]
Yue Li,
Junbai Li*
Xiyun Feng,
Anhe Wang,
Yang Yang, Jinbo Fei, Bingbing Sun,
Yi Jia, and
[
a,e]
[
3]
Abstract: Prototypes of natural biosystems provide new opportunities
for artificial biomimetic systems to break the limits of natural reactions
and achieve output control. However, mimicking unique natural
structures and ingenious functions still remains a great challenge.
Here, we have integrated multiple biochemical reactions into
artificially designed compartments via molecular assembly. First,
multicompartmental silica nanoparticles with hierarchical structures
that mimic the chloroplasts were obtained by a templated synthesis.
Then, photoacid generators and ATPase-liposomes were assembled
inside and outside of silica compartments, respectively. Upon light
illumination, protons produced by a photoacid generator in the
confined space can drive the liposome-embedded enzyme ATPase
towards ATP synthesis, which mimics the photophosphorylation
process in vitro. The developed methodology enables fabrication of
bioinspired nanoreactors for photobiocatalysis and provides insight
for understanding sophisticated biochemical reactions.
harvesting or water splitting processes. Other than this, the final
solar-to-chemical energy conversion relies on the
photophosphorylation efficiency due to the crucial function of ATP
[
2c]
as an “energy currency”.
Notably, the rapid formation of a
proton gradient and a membrane potential across the thylakoid
membrane is the driving force for ATP production. Therefore,
constructing a controllable mimicking chloroplast employing this
strategy is of vital importance to enhance the final solar energy
conversion efficiency. However, it still remains a great challenge
to achieve large-scale production of ATP in vitro due to the
sophisticated biocomponents coupled in the cascade reaction
and the need for rapid formation of a proton gradient across the
[
4]
thylakoid membrane for enhanced ATP production.
Photophosphorylation reactions occurring in plant chloroplasts
play an important role in the usage of solar energy, which has
great potential as a clean, renewable and globally available
[
1]
energy source. Chloroplasts are typically hierarchical organelles
in which the light-harvesting pigments, electron transport chain,
and enzymes are supramolecularly organized in typical stacking
thylakoids, where light is captured then promote water splitting
into oxygen, electrons and protons, and the produced proton
gradients enable adenosine triphosphate (ATP) synthase to
rotate and catalyze the synthesis of ATP and biomass to
[
2]
accomplish further energy conversion (Scheme 1). However,
limited by the natural energy conversion efficiency and the weak
stability of natural photosystem complexes, many advanced
artificial systems have been developed to enhance light
[a]
Dr. Y. Li, Dr. X. Feng, Dr. A. Wang, Dr. J. Fei, Dr. B. Sun, Dr. Y. Jia,
Prof. Dr. J. Li
Beijing National Laboratory for Molecular Sciences (BNLMS), CAS
Key Lab of Colloid, Interface and Chemical Thermodynamics,
Institute of Chemistry, Chinese Academy of Sciences, Beijing,
Scheme 1. Natural chloroplast multicompartment structures and biochemical
reactions. A model of an artificially designed photophosphorylation system in
synthesized nanocomposites.
100190, China.
E-mail: jbli@iccas.ac.cn
As a spatially confined membrane protein, ATP synthase is
anchored predominantly outside of the obstructed proton gradient
in internal multicompartmental structures for efficient
[b]
Dr. Y. Li, Dr. Y. Yang
CAS Key Laboratory for Biomedical Effects of Nanomaterials and
Nanosafety, National Center for Nanoscience and Technology,
Beijing, 100190, China.
[
5]
photophosphorylation. Given the strong dependence on the
dominant structure of multicompartment thylakoids, it’s an urgent
requirement to employ efficient light-sensitive pH-jump reagents
[
c]
d]
Dr. X. Feng
Yunnan Normal University, Faculty of Chemistry and Chemical
Engineering, Kunming, 650050, China.
Dr. A. Wang
[
6]
[
as proton source and integrate it with the protein motor with a
mimicking strategy, through more elegant method,
supramolecular assembly. Based on assembly, well-ordered
State Key Laboratory of Biochemical Engineering, Institute of
Process Engineering, Chinese Academy of Sciences, Beijing,
a
[7]
100190, China.
[
8]
and morphology-tunable reactors can be synthesized,
[
e]
#]
Dr. B. Sun, Prof. Dr. J. Li
[
9]
University of Chinese Academic of Sciences, Beijing 100049, China.
These authors contributed equally to this work.
especially for biomimetic systems. Among assembled systems,
reactors at the nano and micro scales have attracted much
attention because of their potential advantages for mass
[
Supporting information for this article is given via a link at the end of
the document.
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Angewandte Chemie International Edition
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COMMUNICATION
[
10]
Figure 1. (a) The illustration of the biochemical reaction mechanism and the
fabrication process: HPTS can be assembled into the multiple compartments of
production in vitro.
constructed
As an extension, we have successfully
spatially confined photophosphorylation
a
SiO
2
nanosponges by electrostatic interaction. With the coassembly of
nanoreactor through supramolecular assembly to mimic both the
structures and the functions of natural chloroplasts. In detail,
massive proton formation is achieved by photoacid being
absorbed in the multicompartmental reaction room, and this
approach is based on short laser pulses as optical “switches”
introducing an instantaneous change in the pH value for the
activation of protein function. Then, ATP synthase is reconstituted
with liposomes and further stabilized on the surface of a silica
liposome-ATP synthase, light-mediated protons are generated and stored to
form a proton gradient across the multicompartmental SiO nanosponge for ATP
2
production. (b,c) SEM images of hierarchical silica nanosponges. (d,e) TEM
2
images of hierarchical silica nanosponges. (f,g) TEM images of SiO -
HPTS@liposome-ATP synthase particles. (h,i) Fluorescence images of HPTS
entrapped silica nanoparticles covered with Texas red-labeled liposome excited
at 488 nm (green signal) and 561 nm (red signal), respectively. Insets are the
green and red fluorescence signal distribution of two chosen particles in h and
i, respectively. (j) EDX mapping of the individual SiO
synthase particle.
2
-HPTS@liposome-ATP
nanoparticle. Hence, using mesoporous silica as
a three-
dimensional proton ‘cage’ and a lipid bilayer shell as a ‘proton
barrier’, spatial control of the proton concentration in nanoscale is
obtained, and the photostimulated photoacid generator produces
a rapid pH jump and triggers rotation of ATP synthase to produce
ATP (Scheme 1). By this procedure, the large-scale
Assembled nanocomposites enable specific biochemistry
reactions to be carried out in a confined space. In this case, the
proton source is crucial for the integrated system. Photoacid
generators are a class of proton-bearing small molecules that
become acidic, lowering the pH value by several orders of
photophosphorylation
reaction
was
achieved
through
construction of quantity controlled, spatially defined nanoreactors
using a simple supramolecular assembly method.
[13]
magnitude, in the excited state and release their protons. They
have been used in several applications, including studies of
chemical kinetics, where creating a rapid optical pH jump to
The fabrication process of the nanoreactor is shown in Fig. 1a.
Hierarchical silica nanoparticles, as both photoacid repositories
and liposome upholders, were obtained through a templating
[
14]
initiate a proton-requiring process is desired.
HPTS was first
Its fluorescence in
bulk water shows two distinct excitation bands corresponding to
[
15]
used as a fluorescence pH indicator dye.
[
11]
method.
templates allowing SiO
b,c). After removing the template, multi-compartmental SiO
In brief, CaCO
3
nanoparticles were prepared as
-
to duplicate the hierarchical structure (Fig. protonated (ROH) and deprotonated (RO ) forms. When the pH in
2
1
2
the bulk solution (pHbulk) changed from 9.0 to 4.6, the intensities
of the characteristic excitation bands at approximately 405 nm
(ascribed to ROH) increased, and the band at approximately 458
nanoparticles were fabricated, yielding a packed array of globular
pores of tens of nanometers in diameter and 10-15 nm in wall
thickness (Fig. 1d,e). Then, poly(allylamine hydrochloride) (PAH),
-
nm (ascribed to RO ) decreased (Fig. 2a), which is in good
[
16]
(
8-hydroxypyrene-1,3,6-trisulfonate trisodium salt) (HPTS) and
agreement with a previous report. In dark, the pH value can be
calculated by substituting the ratio I405/I458 into the equation (inset
reconstituted ATP synthase-liposome were assembled
successively through electrostatic interaction, and a carrier for
[
16]
of Fig. 2a).
[
12]
proton gradient building was formed.
proteoliposome was successfully assembled onto the HPTS-
incorporated SiO nanoparticles(Fig. f-i). Additional data from
As a result, the
Other than its use as a fluorescence pH indicator, HPTS is
[6b]
also a well-known photoacid generator. It has a nearly neutral
2
pKa (7.4) in its ground state, and this can be changed to a much
energy-dispersive X-ray spectroscopy (EDX) mapping (Fig. 1j)
were collected to investigate the location of the key elements Si,
[17]
lower value (pKa* 0.5) after photoexcitation.
In aqueous
solution with a pH value larger than the pKa*, deprotonation of the
photoacid occurs rapidly, and HPTS is converted into a strong
N, Na, and P, mainly originating from SiO
liposome-ATP synthase, respectively.
2
, PAH, HPTS and
-
+
acid by photolysis release of protons (ROHàRO *+H ) (Fig.
[
6b]
2
b).
Against this background, HPTS assembled in the
nanocomposite was employed as a photoinduced proton source.
However, when it is employed as a photoacid generator, the pH
value cannot be calculated by a simple equation. The intensity
-
peak has a slight blue shift, and the intensity of RO at 455 nm
decreased with irradiation. After 18 min an excitation peak at 403
-
nm appeared (Fig. 2b). The disappearance of RO was due to the
-
equilibrium between ROH and RO and the accumulated acidity
-
was caused by the ROH-to-RO * transformation. After irradiation
for a long period, it seems that the pH change is irreversible, and
the jump of the pH value strongly depends on the time of
stimulation. A large number of protons was then generated in the
confined space of the nanoreactor (Fig. 2c).
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protons generate a proton gradient that significantly affects the
biochemical activity of transmembrane proteins. This cascade
biocatalytic process can be clearly observed via the ATP synthase
membrane channels converting the pH gradient into chemical
[
16]
energy, that is, ATP generation.
Under light illumination, the outward pumping of protons
generated by HPTS provides a driving force for ATP synthase
rotary catalysis, synthesizing ATP detected by luciferin-luciferase
[
12b,16]
bioluminescence assay.
It is clearly seen that the ATP
production continuously increased with increasing irradiation time
within the first 70 min under illumination and reached a plateau
after 70 min (Fig. 3a,b). Remarkably, the ATP production and the
degree of pH decrease both occurred in response to the
illumination intensity and HPTS amount. In the optical situation
depicted in Fig. 3a,b, the samples containing 0.16 mM HPTS
-
2
under 100 mW cm light power could generate over 6 μmol ATP
per mg ATP synthase within 122 min. In this case, during the first
1
0 s, the ATP production increased to 0.06586 μmol per mg ATP
-
1
synthase s . During this time, the average rate was 37.5402 ATP
-
1
-1
s
o 1
ATP synthase (Fig. 3c left), which represents the CF F -
ATPase turnover frequency (TOF), and can be compared with the
existing ATP production systems (Table S1). Moreover, the
maximum rate (initial 10 s) of ATP production is associated with
the light power and HPTS concentration, indicating that the
generation rate can be precisely controlled (Fig. 3c). It is worth
mentioning that higher values could be obtained if more particles
were employed. In addition, Fig. 3f demonstrates that ATP
synthesis could be simply triggered by light. These results further
demonstrate that it is the light-induced local acidification that
leads to activation of ATP synthase and delivers the
chemiosmotic energy. Under illumination, the proton
concentration gradient is built up, and the embedded ATP
synthase can be switched on.
Figure 2. (a) Fluorescence excitation spectra (λem=513 nm) of HPTS in silica
nanoparticles as a function of pHbulk, and the inset is the pH-dependent value of
Ex458/Ex405. The pH of the solution in a, b and c was adjusted using HCl and
2
NaOH. (b) Time-dependent excitation spectra of SiO -HPTS in solution under
white illumination, and the inset is the time-dependent value of Ex455/Ex403 under
illumination. To maintain the appropriate ionic strength, 100 mM NaCl was used.
(
2
c) Graphic illustration of spatially confined SiO -HPTS.
ATP synthase was isolated, reconstituted into liposome to
form liposome-ATP synthase through a published procedure with
[
12b,16]
minor modifications,
of SiO -HPTS nanoparticle (Fig. 1f-j). To detect the
proton gradient within the assembled nanoreactor,
three different particles, SiO -HPTS, SiO
HPTS@liposome, and SiO -HPTS@liposome-ATP
then located on the surface
2
2
2
-
2
synthase, were investigated in the test solution. As a
result, the pHbulk rapidly decreased without liposome
cover (dotted line), indicating that the protons freely
diffused in the aqueous solution without the protection
2
of liposomes (Fig. 3d). For SiO -HPTS@liposome the
pHbulk decreased much more slowly during the initial 30
min due to the protection of liposomes (solid line).
However, the pHbulk distinctly decreased with increasing
time of light irradiation after 30 min, indicating leakage
of protons. Furthermore, SiO
synthase was introduced to prove the function of the
proton pump for comparison. It is obvious that SiO
HPTS@liposome-ATP synthase (dashed line)
exhibited a higher proton throughput ability than did
SiO -HPTS@liposome. The different values are shown
2
-HPTS@liposome-ATP
2
-
2
in Fig. 3d (below). It was concluded that ATP synthase
acted as a proton pump in the system mainly during the
initial 30 min. Compared with the outside bulk solution,
the localized acidification inside the core undergoes a
significant pH change upon irradiation. The obtained
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Figure 3. (a) Effect of different light power on ATP production and pHbulk
changes. (b) Effect of different HPTS concentrations on ATP production (μM)
and pHbulk changes. (c) Plots of maximum rate of ATP production vs. light power
or HPTS concentration. (d,e) Light-dependent pHbulk changes of different
solutions containing HPTS (dotted line), HPTS-liposome (solid line) or HPTS-
liposome-ATP synthase (dashed line) under illumination, and changes of the
value of the solid line and the dashed line during time of illumination (below). (f)
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mimic chloroplasts at the structural and functional levels in a
nanocomposite system that involves photophosphorylation,
mimicking the massive ATP production in vitro. In particular, a
light switch and a pH jump trigger are combined in a coupling
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Keywords: supramolecular assembly • nanocomposite •
photophosphorylation • organic-inorganic hybrid composites •
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COMMUNICATION
COMMUNICATION
#
#
#
Yue Li , Xiyun Feng , Anhe Wang ,
Yang Yang, Jinbo Fei, Bingbing Sun, Yi
Jia, Junbai Li*
Page No. – Page No.
Supramolecularly Assembled
Nanocomposites as Biomimetic
Chloroplasts for Enhancement of
Photophosphorylation
Table of Content:
Inspired by natural chloroplast compartment structures, hierarchical SiO
2
nanosponges are artificially designed, co-assembled with
photoacid molecules and liposome-ATP synthase to form organic-inorganic hybrid nanocomposites for photophosphorylation output
control achievement.
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