Mimicking Photosystem I with a Transmembrane Light Harvester and Energy Transfer-Induced Photoreduction in Phospholipid Bilayers

Article abstract of DOI:10.1002/chem.202003391

Photosystem I (PS I) is a transmembrane protein that assembles perpendicular to the membrane, and performs light harvesting, energy transfer, and electron transfer to a final, water-soluble electron acceptor. We present here a supramolecular model of it formed by a bicationic oligofluorene 1²⁺ bound to the bisanionic photoredox catalyst eosin Y (EY^2?) in phospholipid bilayers. According to confocal microscopy, molecular modeling, and time dependent density functional theory calculations, 1²⁺ prefers to align perpendicularly to the lipid bilayer. In presence of EY^2?, a strong complex is formed (K_a=2.1±0.1×10⁶ m^?1), which upon excitation of 1²⁺ leads to efficient energy transfer to EY^2?. Follow-up electron transfer from the excited state of EY^2? to the water-soluble electron donor EDTA was shown via UV–Vis absorption spectroscopy. Overall, controlled self-assembly and photochemistry within the membrane provides an unprecedented yet simple synthetic functional mimic of PS I.

Full text of DOI:10.1002/chem.202003391

Accepted Article
Accepted Article
Title: Mimicking Photosystem I with a Transmembrane Light Harvester
and Energy Transfer-Induced Photoreduction in Phospholipid
Bilayers
Authors: Andrea Pannwitz, Holden Saaring, Nataliia Beztsinna,
Xinmeng Li, Maxime A. Siegler, and Sylvestre Bonnet
This manuscript has been accepted after peer review and appears as an
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of the final Version of Record (VoR). This work is currently citable by
using the Digital Object Identifier (DOI) given below. The VoR will be
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To be cited as: Chem. Eur. J. 10.1002/chem.202003391
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1/2020

Chemistry - A European Journal
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RESEARCH ARTICLE
Mimicking Photosystem I with a Transmembrane Light Harvester
and Energy Transfer-Induced Photoreduction in Phospholipid
Bilayers
Andrea Pannwitz,* [a] Holden Saaring, Nataliia Beztsinna, Xinmeng Li, Maxime A. Siegler,[b]
[a]
[a]
[a]
Sylvestre Bonnet*[a]
Abstract: Photosystem I (PS I) is a transmembrane protein that
assembles perpendicular to the membrane, and performs light
harvesting, energy transfer, and electron transfer to a final, water-
soluble electron acceptor. We present here a supramolecular model
electron acceptor.[1–5] Synthetic self-assemblies are aimed at
mimicking functions of cells and photosynthesis.[6–8] In particular,
phospholipid membranes and vesicles (e.g. liposomes) can serve
[9–11]
as a scaffold for mimicking cellular compartmentalization,
2+
[12]
[13,14]
of it formed by a bicationic oligofluorene 1 bound to the bisanionic
light harvesting,
membrane interactions,
transmembrane
2-
[15–20]
photoredox catalyst eosin Y (EY ) in phospholipid bilayers. According
to confocal microscopy, molecular modeling, and time dependent
electron transfer,
and co-assembly of photosensitizers with
electron relays and catalysts.[
21–24]
In very rare cases the
2
+
density functional theory calculations,
1
prefers to align
assembly of chromophores at phospholipid membranes enabled
2-
[25]
perpendicularly to the lipid bilayer. In presence of EY , a strong
for light-induced energy and electron transfer. Self-assembled
6
-1
complex is formed (K
a
= 2.1 ± 0.1 · 10 M ), which upon excitation of
transmembrane molecular wires were able to achieve electron
transfer across artificial and natural phospholipid membranes,
though in the absence of light.[26–29] Liposomes doped with
transmembrane electron transferring chromophores coupled to
proton and ion transfer lead to pH and concentration gradients
across membranes.[27–29] One common design principle for
membrane-spanning molecules it that they shall comprise both a
central hydrophobic and one or two terminal hydrophilic groups.
With two end-groups, the distance between these hydrophilic
groups should match the thickness of the lipid bilayer, as distance
mismatch tends to lower membrane stability.[30–34]
2+
2-
1
leads to efficient energy transfer to EY . Follow-up electron
2-
transfer from the excited state of EY to the water-soluble electron
donor EDTA was shown via UV-vis absorption spectroscopy. Overall,
controlled self-assembly and photochemistry within the membrane
provides an unprecedented yet simple synthetic functional mimic of
PS I.
Introduction
In nature, photosynthetic organisms absorb sunlight to convert it
into high-energy chemicals used as bioenergy carriers. In order to
do so, they arrange several protein super complexes with
precisely oriented chromophores in phospholipid membranes.[1–3]
One example is photosystem I (PS I) which is surrounded by
multiple units of the protein light harvesting complexes I (LHC I)
to harvest sunlight in the UV and visible range of the solar
spectrum to funnel the photon energy to the reaction center in
photosystem I (PS I).[1] Light energy transfer within the membrane
is enabled by orientation control of numerous light harvesting
chromophores within the membrane and with respect to the
energy accepting reaction center.[1] The reaction center itself is a
red light-absorbing chlorophyll dimer which triggers multistep
electron transfer reactions in the phospholipid membrane to a final
[
a]
Dr. A. Pannwitz, H. Saaring, Dr. N. Beztsinna, Dr. Xinmeng Li, Dr. S.
Bonnet
Leiden University
2
+
Scheme 1. Light absorption by 1 is followed by energy transfer to eosin Y
2-
4-
(
EY , in red) and subsequent electron transfer from the electron donor EDTA
2-
to the excited EY .
Leiden Institute of Chemistry
Einsteinweg 55, 2333 CC Leiden, The Netherlands
E-mail: a.pannwitz@lic.leidenuniv.nl, andrea.pannwitz@uni-ulm.de,
bonnet@chem.leidenuniv.nl
[
b]
Dr. M. A. Siegler
Johns Hopkins University
Department of Chemistry
Maryland 21218, Baltimore, USA
Supporting information for this article is given via a link at the end of
the document.
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Chemistry - A European Journal
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RESEARCH ARTICLE
Figure 1. a) Molecular dynamics model of 12+ in a transmembrane geometry in a phospholipid bilayer. Color-code: 12+: turquoise, space filling model; lipid bilayer
and water: stick model, red: oxygen, yellow: phosphorous, blue: nitrogen, grey: carbon, green: chloride. Hydrogen atoms are omitted for clarity. c) Confocal
2+
luminescence microscopy images of giant DMPC vesicles doped with 1 mol-% 1 at pH 7.8, laser excitation at λex = 405 nm, detection in the range: 420 – 514 nm.
2+
T
c) Schematized interaction of the transition dipole µ of 1 with the incident (polarized) laser light exciting the sample from top. d) HOMO, LUMO, and transition
dipole moment, of 12+ calculated by TDDFT at the CAM-B3LYP/TZP level.
In this study, we constructed an artificial, biomimetic analogue of
photosystem I based on a rigid, oligofluorene chromophore that
precisely self-assembles perpendicularly to phospholipid bilayers.
We chose here a rigid, symmetrical oligofluorene core composed
of eight conjugated aromatic rings, directly connected to two
terminal, hydrophilic trimethylammonium anchoring groups. The
designed oligo-fluorene 12+ is depicted in Scheme 1. The
ammonium groups are separated by a distance of 3.5 nm, which
fits best with typical thicknesses of phospholipid bilayers (vide
infra).[34] Upon light absorption, this oligofluorene funnels the
photon energy into an energy acceptor finally capable of
transferring electrons at the water-membrane interface.
membranes as compared to organic solvent, which differs from
other oligovinylene chromophores.[26,37]
Modeling the absorption spectra with time-dependent density
functional theory (TD-DFT) yielded the lowest energy absorption
bands at 352 nm for 12 and 353 nm for 2 respectively, which is
reasonably similar to the experimental values (Table 1). The
CAMB3LYP functional was chosen for 12+ to take into account the
charge transfer (CT) character found for its lowest excited states:
As shown in Figure 1d, the calculated HOMO and LUMO of the
ground state of 12+ are located in the middle and at the extremities
+
2
+
of the oligofluorene 1 , respectively. By contrast, the HOMO and
LUMO of 2 (Figure S9) are both located at the center of the
trifluorene molecule, lowest energy transition is a more classical
π - π* character (Figure S9).
Results and Discussion
The synthesis of 1(PF
in the Supporting information. A molecular dynamics model of 1
6 2
) was performed in four steps described
2+
in a phospholipid bilayer (Figure 1a) confirmed that the 3.5 nm
distance between the ammonium groups fits ideally with the 1,2-
dimyristoyl-sn-glycero-3-phosphocholine (DMPC) and 1,2-
dipalmitoyl-sn-glycero-3-phosphocholine (DPPC) membrane
thickness of 3.1-3.4 and 3.4-3.7 nm, respectively.[35,36]
6 2
In organic solvent, 1(PF ) absorbs at 358 nm in methanol, and its
hydrophobic core molecule 2 (Scheme 2) absorbs at slightly
higher energy in chloroform (349 nm, see Table 1). In spite of their
similar emission maxima (~400 nm) and stokes shifts (48 vs. 44
nm, respectively), the molar absorption coefficient (ε) of 12+ in
methanol was found significantly higher than that of 2 in
chloroform (16·104 M-1 cm-1 vs. 6.8·104 M-1 cm ) suggesting
different types of excited states. Upon incorporation into
Scheme 2. Chemical structures of the chromophores and lipids (DMPC and
DPPC) used in this work
-1
2
+
liposomes neither 1 nor 2 experienced significant spectroscopic
changes compared to organic solvents. Very small shifts of their
absorbance maxima might result from Tyndall scattering of the
liposomes suspension (Figure S8), while the shift in luminescence
upon incorporation into liposomes was hardly measurable (~2
nm). Such minor spectroscopic variations suggest negligible
solvent effects and minor aggregation of 12+ and 2 in phospholipid
In order to see whether 12+ aligns indeed perpendicularly to lipid
membranes, confocal microscopy was performed on giant
multilamellar vesicles using laser excitation at 405 nm and
detection in the region 420 – 514 nm (Figure 1b). The
luminecence images were superimposable with the simultaneusly
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Chemistry - A European Journal
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RESEARCH ARTICLE
of 1(PF
6
)
2
in water was modelled for 200 ns, as described in the
Table 1. Spectroscopic and properties of the investigated compounds
Supplementary Information. In all cases spontaneous bilayer
formation was observed, and in four cases out of six 12+ indeed
ended up in a transmembrane fashion (see supplementary movie
Movie1.mpg), while two simulations ended up in a parallel
configuration. This result suggested a preference of 12+ for a
transmembrane self-assembly, but it would not be affordable to
quantify this preference using this computationally intensive
method. Thus, in two of these simulations we computed the
binding free energy of 12+ to the membrane, ΔGbind either in the
transmembrane or in the parallel configuration (see details in the
Supporting Information). The averaged ΔGbind for the
perpendicular (transmembrane) and parallel configuration were -
Conditions
λ
abs (nm)
λem (nm)
4
-1
(ε (10 M
-
1
cm ))
Methanol
358 (16)
362
404; 422
DMPC vesicles[a]
404; 425
-
12+
TD-DFT
352
(CAMB3LYP)
CHCl
3
349 (6.8)
350
393; 414
393; 413
-
2
DMPC vesicles[a]
TD-DFT (PB0)
Water, pH 7.8[b]
DPPC vesicles[a,c]
Methanol
1
65.5 kJ/mol and -22.4 kJ/mol, respectively, which further
2
+
confirmed the preference of
1
for the transmembrane
353
configuration. Overall, these modeling studies supported our
design hypothesis, that the half-moon effect observed in confocal
517
538
EY2-
2+
images of giant vesicles containing 1 , is due to a preference for
517 – 528
531
545
a transmembrane configuration of this linear molecule.
556
C16EY-
DPPC vesicles[a]
545
574
[
a] DMPC or DPPC, 1 % chromophore and 1 - 4 % NaDSPE-PEG2K in
phosphate buffer, pH 7.8, [b] phosphate buffer [c] dependent on
concentration, in line with ref.[
39,40]
.
recorded transmission image (Figure S16), which demonstrates
2+
that 1 is selectiveley taken up in the lipid bilayer.
For the reference compound 2 no selective staining of the bilayer
was observed for 2 under comparable experimental conditions
(
see Figure S17), which we attribute to preferred π-stacking of 2
over its solublity in the lipid bilayer structure.
Furthermore, for vesicles with 12+ a double half-moon shaped
emission profile was observed in all vesicles in the microscopic
image (Figure 1b), which is typical for molecules forming a circle
in the observation plane.[26]
The interaction of each chromophore molecule with the laser
beam depends on the orientation of their transition dipole moment
with respect to the direction of propagation of the light beam. As
the incident laser light is polarized, all molecules with a transition
T
dipole moment (µ ) parallel to the polarization plane of the laser,
absorb more light and therefore exhibit brighter luminecence,
which explains the bright regions on the thick parts of both half-
moons. In the thin regions of the image the transition dipole
moment of 12+ is orthogonal to the polarization plane, therefore
the absorption of the light beam, and hence the luminescence
image are weaker. The transition dipole moment of the lowest
electronic transition of 1 , is parallel to the long axis of the
molecule (Figure 1d) and has 6.32 Debye according to TD-DFT
calculation at the CAM-B3LYP/TZP level. Hence, spherically
assembled transition dipole moments correspond to spherically
assembled molecules.
In principle, one could argue that the half-moon effect might be
due to either a parallel, or a perpendicular (transmembrane)
alignment of 12+ with respect to the lipid bilayer. We performed
molecular dynamics simulations using Gromacs 2018 software[38]
in order to check that. First, the self-assembly of 6 independent
random distributions of 128 DMPC molecules and one molecule
Figure 2. a) Scheme of energy transfer within the phospholipid bilayer. b)
Luminescence spectra upon excitation of 1.25 mM liposomes DPPC:12+:EY at
2-
2
+
374 nm at pH 7.8. The liposomes contained 0.3 % NaDSPE-PEG2K, 1.3 % 1
and various concentrations of EY2 added to the lipid mixture during liposome
preparation. The asterisk (*) marks the scattered excitation light. c) Confocal
images (excitation at 405 nm) of DMPC:12+ in presence of 10 µM EY added to
the solution after vesicle formation at pH 7.8.
-
2
+
2-
In nature, photosystem I transfers the excitation energy of the
transmembrane molecular light harvester to a second dye in the
membrane, to finally induce charge transfer. To mimic this system
2-
eosin Y (EY ) was chosen as a co-dopant in lipid membranes,
because this dye has been widely used in photoelectron
transfer[41] and photocatalytic proton and CO
2
reduction studies
on lipid bilayers and cell membranes.[23,41,42] Therefore, 12+ and
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RESEARCH ARTICLE
H
2
EY were added in different ratios into the lipid bilayer of DPPC
vesicles, while the luminescence of EY2- in the red region of the
spectrum was switched on (Figure 2c). Interestingly, this
liposomes during lipid film preparation. Deprotonation of H EY to
EY occurred upon hydration of the lipid films with a phosphate
buffer at pH 7.8, as demonstrated by the characteristic absorption
maximum at 544 nm for DPPC:1 :EY liposomes (1000:13:10
n/n/n ratio). Interestingly, this band is significantly red-shifted
compared to homogeneous solution (λmax = 517 nm in water[43–45]).
The absorbance of 12+ was slightly blue-shifted in presence of
EY2- in the membrane, from 356 nm in DPPC:1 liposomes
2
2
-
2+
phenomenon was not observed for apparently similar DPPC:1
vesicles. Upon addition of 10 µM EY2- to the outer aqueous phase
of these vesicles at room temperature, the luminescence of 12+
was only partly quenched lighting up only parts of the EY2-
luminescence. This could be explained by the fact that only the
2+
2-
2-
outer shells of the multi-lamellar vesicles are interacting with EY .
2+
According to the leakage test with DPPC:12+ (Supporting
Information, p. S32), lipid bilayers are impermeable to water-
soluble species. Therefore, inner lamellas of multilammelar
vesicles are not affected by quenching via energy transfer. By
contrast, DMPC vesicles are inherently leaky and more fluid at
2
+
2-
(
(
1000:13 n/n ratio) to 351 nm in DPPC:1 :EY liposomes
1000:13:10 n/n/n ratio). Both shifts are indicative of
supramolecular interaction within the membrane between EY2
and 12+ (in the ground state).[43] These interactions were
confirmed by molecular dynamics simulations of one molecule of
-
room temperature, because their phase transition temperature
2
+
2-
[48,49]
1
3
and one molecule of EY in a DMPC lipid bilayer model. Within
0 ns simulation both dyes showed close contact interactions,
coincides with room temperature.
Nevertheless, these data
2
+
2-
underline that the supramolecular complex [1 :EY ] forms within
the phospholipid bilayer and provides an efficient scaffold for
energy transfer from the transmembrane blue-light harvesting
characterized by a distance of less than 1 nm between the two
oppositely charged species. Respective graphical presentations
of this model can be found in Figure S6 and Figure S7.
The formation of a supramolecular complex between 12+ and EY
in liposomes was confirmed by efficient energy transfer from 12
to EY2- observed upon selective photoexcitation of 1 (at 374 nm)
oligofluorene 12 to the photoredox catalyst EY .
+
2-
2-
+
2+
2
-
lighting up the emission band of EY (Figure 2b). The steady-state
2
+
2-
emission spectrum of such DPPC:1 :EY liposomes showed
gradual quenching of the emission of 12+ at 404 nm upon adding
increasing concentrations of EY2- into the membrane, while
increasing emission of EY2- was observed (Figure 2b). Plotting the
inverse of the luminescence intensity vs. acceptor concentration
in a Stern-Volmer plot indicated combined static and dynamic
quenching (Supporting Information, Figure S15). Eq. 1 was used
-1
to obtain the association constant (K
shown in Eq. 2:[46]
a
in M ) for the equilibrium
I0
2
-
=
(1 + K
a
· [EY ]) · (1 + KSV · [EY2-])
(Eq. 1)
(Eq. 2)
I
DPPC:12+ + EY2- ⇌ DPPC:1 :EY
2+
2-
2
+
In Eq. 1, I
0
and I represent the emission intensity of 1 in absence
2
-
and in presence of the quencher [EY ], and KSV the Stern-Volmer
-1
constant (in M ) for the dynamic quenching of the emissive S
1
excited state of 12+ by EY . In absence of EY DPPC:12+
2-
2-
liposomes had a luminescence lifetime of 1.4 ns. In the lower
concentration regime of EY2- ([EY ] < 0.5 · [1 ]) the dynamic
2-
2+
quenching takes place with a Stern-Volmer constant KSV = 5.3 ·
5
-1
1
0 M while the association constant (K
a
) for its static component
6
-1
is K
a
= (2.1 ± 0.1) · 10 M . This association constant is 3 orders
Figure 3 a) Evolution of the UV-vis absorption spectrum of DPPC:1 :EY2-
2+
2
-
of magnitude stronger than the reported association of EY to
bare DPPC vesicles at pH 7 (K
2+
liposomes containing 0.3 % NaDSPE-PEG2K and 1.3 % (13 µM) 1 at 1 mM
= (1.0 ± 0.1) · 103 M ) which
-1 [40]
a
DPPC and 10 µM EY overall ratio of 12+/EY is 1:0.8 (n/n) upon irradiation with
2-
2-
highlights the strong attracting effect of the positively charged
membrane-doping agent 1 . At higher concentration of EY (0.5
375 nm LED light. Inset: Temporal evolution of the absorbance at 544 nm b)
2+
2-
Thermochemistry of energy transfer from photo excited 12+ to EY2- followed by
2-
2
-
2+
electron transfer from excited state EY to the water-soluble electron acceptor
<
[EY ]/[1 ] < 1) the quenching behavior does not follow the trend
4
-
EDTA .
of eq. 1 anymore, which might be due to dimerization of EY2- at
the membrane interface.[47]
Luminescence quenching was also observed by confocal
luminescence microscopy of micrometer sized multi-lamellar
giant vesicles. The blue luminescence observed with DMPC
vesicles containing 12+ was quenched almost completely upon
addition of 10 µM EY2- to the outer aqueous phase of the giant
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Chemistry - A European Journal
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RESEARCH ARTICLE
Table 2. Excited state energy (E0-0) and electrochemical properties of the
investigated compounds.
functionalization of the acid side group with a long (C16) aliphatic
chain (Scheme 2). DPPC liposomes doped with 1 mol% of
-
2-
C16EY showed an absorption band similar to EY at pH 7.8 in
water, but red-shifted to 545 nm. This is in line with the integration
of the eosin dye into a hydrophobic environment such as a lipid
bilayer.[40,43] Irradiating DPPC:C16EY liposomes with neither 375
E
0-0 (eV)
E
ox
E
red
Ref.
(
V vs.
(V vs.
SCE)
SCE)
-
-
2.13
This study.
This study
4-
nm nor 530 nm light in the presence of EDTA (42 mM) did not
1
6 2
(PF ) in MeCN
1.15
(irrev.)
yield any spectroscopic changes. Therefore, no light-induced
electron transfer occurred between the strongly membrane bound
2
in MeCN
1.17
2.03
-2.72
0.48
-state)[
50]
and
[50]
-
4-
*
2 in MeCN
3.2 (S
1
excited state of C16EY and EDTA in the aqueous phase.
~
2.3 (T
1
-state)[50]
2-
Secondly, free eosin EY (6.7 µM) was quickly photoreduced in
[
[
41]
52]
the presence of EDTA4- (42 mM) in homogeneous, liposome-free
buffer at pH 7.8 upon irradiation with 375 nm LED light (0.5 mW),
as seen by the disappearance of the absorption band at 517 nm
EY2
-
0.78
-1.1
-1.06
0.8
1
1.9 (T -state)
2-
*
EY
EDTA4- in water
0.6
-1
with a rate constant of 1.15 ± 0.1 min . The evolution of the
spectra is shown in Figure S19. This photoreaction rate is
significantly faster than that observed with DPPC:C16EY-
2
-
To test the reactivity of the energy transferred on EY for further
2
+
2-
2
+
2-
liposomes and DPPC:1 :EY liposomes, which is most probably
due to a combination of several effects. First, in absence of 12+
there is no filter effect by this strongly UV-absorbing molecule, so
redox reactions, DPPC:1 :EY liposomes (1000:13:10 n/n/n at 1
mM DPPC) were irradiated at 375 nm (0.5 mW) in the presence
of an isotonic buffer containing 83 mM EDTA4- at pH 7.8. During
irradiation the absorption band at 544 nm characteristic for EY
vanished with a rate constant of 18 min , while simultaneously
the absorption band of 12+ was shifted from 351 nm to 354 nm.
Figure 3a). Based on the excited state energies and redox
potentials of all membrane-embedded components or their
reference compound (Table 2) the reaction sequence shown in
Scheme 1 and Figure 3 is proposed. Upon photoexcitation of 1 ,
energy transfer (ET) takes place from an excited state of 1 to
EY . This step has an overall driving force of 1.3 eV, either from
the S
state of 12+ at ~3.2 eV to the S state of EY2- (2.3 eV)
followed by intersystem crossing to the T
state of EY2- at ~1.9
eV. , or via inter system crossing of 12+ to the T
2
-
2-
all available light is absorbed by EY and can lead to excited state
2
+
2-
2+
-1
formation. For DPPC:1 :EY liposomes, 1 absorbs most light,
2
-
preventing direct absorption by EY . Second, diffusion rates are
higher in homogeneous solution than with molecules embedded
in membranes, which may improve electron transfer rate in
liposome-free conditions. Finally, in DPPC:1 :EY liposomes the
strong association of EY2- to 1 leads to a very low bulk
concentration of EY2- in the water phase, which slows down direct
(
2
+
2-
2+
2
+
2
+
2
-
4-
2
-
electron transfer from the excited states of EY , to EDTA .
1
1
1
[
41]
50]
1
state at ~2.3 Conclusion
[
eV,
followed by triplet-triplet energy transfer to the triplet
excited state of EY2- at ~1.9 eV.[41] From its T state EY2- accepts
1
Overall, our experimental and theoretical data are consistent with
an electron and two protons from the electron donor EDTA4- with
2+
the following picture. First, the transmembrane oligofluorene 1
a driving force ΔGeT = -0.2 eV, providing the almost colorless
EYH .
2
is acting as a light-harvesting chromophore that self-assembles
perpendicular to the membrane, and transfers photochemical
energy to EY2- within a membrane-embedded supramolecular
complex. We propose that following energy transfer, the triplet
excited state of EY2- is reduced at the membrane-water interface
2
- [51]
The slow electron transfer kinetics on the minute time scale can
be explained by the strong association of the relatively
2
-
hydrophobic EY dyes to the membrane, as supported by the
strong association constant with 12+ and the close contact
observed in molecular dynamics simulation (Supporting Info page
S22-S23). By contrast, the strongly charged and poorly
4-
by the reductant EDTA , to a colorless form. To the best of our
knowledge, the combination of light absorption, energy transfer,
and electron transfer using a transmembrane chromophore
represents an unprecedented functional mimic of PS I using
simple organic chromophores.
4
-
hydrophobic species EDTA is anticipated to remain in the
aqueous phase. Still, the positive charge of the antenna 12 might
play a role in attracting the anionic EDTA4- electron donor near
the membrane-water interface, thereby promoting electron
+
2
-
transfer from the excited state of EY . As an alternative, it may
Experimental Section
2
+
2-
2-
also be possible that in DPPC:1 :EY liposomes EY diffuses
temporarily away from the membrane into the solution, to absorb
photons by itself and directly photoreact with the sacrificial donor
EDTA4- in the aqueous phase, before stochastically coming back
to the membrane.
Experimental details including synthetic procedures can be found in the
Supporting Information. The structure of the brominated intermediate
obtained during the synthesis of 12+ is reported via CCDC1970033.
To investigate if the observed photoreduction may have occurred
2
-
via direct photoexcitation of EY by the 375 nm exciting light
(
Acknowledgements
4
-1
-1
4-
0.1·10 M cm ) and subsequent photoreduction by EDTA , we
realized two control experiments. First, a strongly membrane-
bound eosin
dye C16EY- was prepared by covalent
A. P. wants to thank the Swiss National Science Foundation who
supported this project through grant number P2BSP2-175003.
Y
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Chemistry - A European Journal
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RESEARCH ARTICLE
We kindly thank the Institute for Biology at Leiden University and
Gerda Lamers for technical support and access to the confocal
microscope. Molecular dynamics simulations with Gromacs were
carried out on the Dutch national e-infrastructure with the support
of SURF Cooperative. The LACDR at Leiden University is
thanked for providing access to the time-resolved luminescence
fluorimeter and SBC for access to the DLS. Elisabeth Bouwman
and Agur Sevink are thanked for their support and scientific
discussion.
[24]
[25]
B. Limburg, J. Wermink, S. S. Van Nielen, R. Kortlever, M. T. M.
Koper, E. Bouwman, S. Bonnet, ACS Catal. 2016, 6, 5968–5977.
K. Börjesson, J. Tumpane, T. Ljungdahl, L. Marcus Wilhelmsson, B.
Nordén, T. Brown, J. Mårtensson, B. Albinsson, J. Am. Chem. Soc.
2009, 131, 2831–2839.
[
[
[
[
[
26]
27]
28]
29]
30]
L. E. Garner, J. Park, S. M. Dyar, A. Chworos, J. J. Sumner, G. C.
Bazan, J. Am. Chem. Soc. 2010, 132, 10042–10052.
N. Sakai, N. Majumdar, S. Matile, J. Am. Chem. Soc. 1999, 121,
4294–4295.
V. Gorteau, G. Bollot, J. Mareda, A. Perez-Velasco, S. Matile, J.
Am. Chem. Soc. 2006, 128, 14788–14789.
Keywords: vesicles • energy transfer • electron transfer
N. Sakai, P. Charbonnaz, S. Ward, S. Matile, J. Am. Chem. Soc.
[
[
[
1]
2]
3]
A. Ben-Shem, F. Frolow, N. Nelson, Nature 2003, 426, 630–635.
N. Nelson, C. F. Yocum, Annu. Rev. Plant Biol. 2006, 57, 521–565.
J. P. Dekker, E. J. Boekema, Biochim. Biophys. Acta - Bioenerg.
2014, 136, 5575–5578.
C. Zhou, G. W. N. Chia, J. C. S. Ho, T. Seviour, T. Sailov, B.
Liedberg, S. Kjelleberg, J. Hinks, G. C. Bazan, Angew. Chemie Int.
Ed. 2018, 57, 8069–8072.
2005, 1706, 12–39.
[
[
4]
5]
R. E. Blankenship, Molecular Mechanisms of Photosynthesis, Wiley
Blackwell, 2014.
[
[
31]
32]
J. Hinks, Y. Wang, W. H. Poh, B. C. Donose, A. W. Thomas, S.
Wuertz, S. C. J. Loo, G. C. Bazan, S. Kjelleberg, Y. Mu, T. Seviour,
Langmuir 2014, 30, 2429–2440.
P. Jordan, P. Fromme, H. T. Witt, O. Klukas, W. Saenger, N. Krauß,
Nature 2001, 411, 909–917.
C. Zhou, G. W. N. Chia, J. C. S. Ho, A. S. Moreland, T. Seviour, B.
Liedberg, A. N. Parikh, S. Kjelleberg, J. Hinks, G. C. Bazan, Adv.
Mater. 2019, 1808021.
[
[
[
6]
7]
8]
G. M. Whitesides, Science 2002, 295, 2418–2421.
M. R. Wasielewski, Acc. Chem. Res. 2009, 42, 1910–1921.
M. Hansen, S. Troppmann, B. König, Chem. - A Eur. J. 2016, 22,
[
[
33]
34]
J. Limwongyut, Y. Liu, G. S. Chilambi, T. Seviour, J. Hinks, Y. Mu,
G. C. Bazan, RSC Adv. 2018, 8, 39849–39853.
58–72.
[
9]
R. Watanabe, N. Soga, D. Fujita, K. V. Tabata, L. Yamauchi, S.
Hyeon Kim, D. Asanuma, M. Kamiya, Y. Urano, H. Suga, H. Noji,
Nat. Commun. 2014, 5, 4519.
J. A. Killian, G. von Heijne, Trends Biochem. Sci. 2000, 25, 429–
4
34.
B. A. Lewis, D. M. Engelman, J. Mol. Biol. 1983, 166, 211–217.
N. Kučerka, D. Uhrıková, J. Teixeira, P. Balgavý, Phys. B Condens.
[
[
35]
36]
[
[
10]
11]
L. Hammarström, M. Almgren, J. Phys. Chem. 1995, 99, 11959–
́
11966.
Matter 2004, 350, E639–E642.
A. Stikane, E. T. Hwang, E. V. Ainsworth, S. E. H. Piper, K.
[
[
[
37]
38]
39]
H. Y. Woo, B. Liu, B. Kohler, D. Korystov, A. Mikhailovsky, G. C.
Bazan, J. Am. Chem. Soc. 2005, 127, 14721–14729.
M. J. Abraham, T. Murtola, R. Schulz, S. Páll, J. C. Smith, B. Hess,
E. Lindahl, SoftwareX 2015, 1–2, 19–25.
Critchley, J. N. Butt, E. Reisner, L. J. C. Jeuken, Faraday Discuss.
2019, 215, 26–38.
[
[
12]
13]
A. M. Hancock, S. A. Meredith, S. D. Connell, L. J. C. Jeuken, P. G.
Adams, Nanoscale 2019, 11, 16284–16292.
D. A. Poletaeva, R. A. Kotel’nikova, D. V. Mischenko, A. Y. Rybkin,
A. V. Smolina, I. I. Faingol’d, P. A. Troshin, A. B. Kornev, E. A.
Khakina, A. I. Kotel’nikov, Nanotechnologies Russ. 2012, 7, 302–
A. De La Cadena, T. Pascher, D. Davydova, D. Akimov, F.
Herrmann, M. Presselt, M. Wächtler, B. Dietzek, Chem. Phys. Lett.
2016, 644, 56–61.
307.
[
[
[
[
[
[
[
[
14]
15]
16]
17]
18]
19]
20]
21]
A. Bahreman, M. Rabe, A. Kros, G. Bruylants, S. Bonnet, Chem. - A
Eur. J. 2014, 20, 7429–7438.
[
40]
I. R. Calori, D. S. Pellosi, D. Vanzin, G. B. Cesar, P. C. S. Pereira,
M. J. Politi, N. Hioka, W. Caetano, I. R. Calori, D. S. Pellosi, D.
Vanzin, G. B. Cesar, P. C. S. Pereira, M. J. Politi, N. Hioka, W.
Caetano, J. Braz. Chem. Soc. 2016, 27, 1938–1948.
D. P. Hari, B. König, Chem. Commun. 2014, 50, 6688–6699.
S. F. Rowe, G. Le Gall, E. V. Ainsworth, J. A. Davies, C. W. J.
Lockwood, L. Shi, A. Elliston, I. N. Roberts, K. W. Waldron, D. J.
Richardson, T. A. Clarke, L. J. C. Jeuken, E. Reisner, J. N. Butt,
ACS Catal. 2017, 7, 7558–7566.
L. Hammarström, M. Almgren, J. Phys. Chem. 1995, 99, 11959–
1
1966.
B. Limburg, E. Bouwman, S. Bonnet, Chem. Commun. 2015, 51,
7128–17131.
[
[
41]
42]
1
M. Li, S. Khan, H. Rong, R. Tuma, N. S. Hatzakis, L. J. C. Jeuken,
Biochim. Biophys. Acta - Bioenerg. 2017, 1858, 763–770.
G. R. Heath, M. Li, H. Rong, V. Radu, S. Frielingsdorf, O. Lenz, J.
N. Butt, L. J. C. Jeuken, Adv. Funct. Mater. 2017, 27, 1606265.
T. Laftsoglou, L. J. C. Jeuken, Chem. Commun. 2017, 53, 3801–
[
[
43]
44]
M. Chakraborty, A. K. Panda, Spectrochim. Acta Part A Mol. Biomol.
Spectrosc. 2011, 81, 458–465.
3
809.
N. N. Daskalakis, S. D. Evans, L. J. C. Jeuken, Electrochim. Acta
011, 56, 10398–10405.
B. Limburg, G. Laisné, E. Bouwman, S. Bonnet, Chem. - A Eur. J.
014, 20, 8965–72.
V. R. Batistela, D. S. Pellosi, F. D. de Souza, W. F. da Costa, S. M.
de Oliveira Santin, V. R. de Souza, W. Caetano, H. P. M. de
Oliveira, I. S. Scarminio, N. Hioka, Spectrochim. Acta Part A Mol.
Biomol. Spectrosc. 2011, 79, 889–897.
2
2
[
[
45]
46]
E. A. Slyusareva, M. A. Gerasimova, Russ. Phys. J. 2014, 56,
[
[
22]
23]
M. Hansen, F. Li, L. Sun, B. König, Chem. Sci. 2014, 5, 2683.
1370–1377.
S. Troppmann, B. König, Chem. - A Eur. J. 2014, 20, 14570–14574.
V. Balzani, P. Ceroni, A. Juris, Photochemistry and Photophysics,
This article is protected by copyright. All rights reserved.

Chemistry - A European Journal
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RESEARCH ARTICLE
Wiley-VCH Verlag, Weinheim, Germany, 2014.
[
[
[
47]
48]
49]
M. Enoki, R. Katoh, Photochem. Photobiol. Sci. 2018, 17, 793–799.
D. Marsh, Handbook of Lipid Bilayers, CRC Press, 2013.
L. M. Hays, J. H. Crowe, W. Wolkers, S. Rudenko, Cryobiology
2001, 42, 88–102.
[
[
[
50]
51]
52]
M. Sudhakar, P. I. Djurovich, T. E. Hogen-Esch, M. E. Thompson, J.
Am. Chem. Soc. 2003, 125, 7796–7797.
A. Aguirre-soto, K. Kaastrup, S. Kim, K. Ugo-beke, H. D. Sikes, ACS
Catal. 2018, 8, 6394–6400.
Y. Pellegrin, F. Odobel, Comptes Rendus Chim. 2016, 20, 283–295.
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Chemistry - A European Journal
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RESEARCH ARTICLE
Entry for the Table of Contents
Layout 1:
RESEARCH ARTICLE
Light absorption, energy transfer and
electron transfer were obtained in a
supramolecular mimic of photosystem
I.
Andrea Pannwitz,* Holden Saaring,
Nataliia Beztsinna, Xinmeng Li, Maxime
A. Siegler, Sylvestre Bonnet*
Page No. – Page No.
Mimicking photosystem I with a
transmembrane light harvester and
energy transfer-induced
photoreduction in phospholipid
bilayers
This article is protected by copyright. All rights reserved.