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Spin-Controlled Photoluminescence in Hybrid
Nanoparticles Purple Membrane System
Partha Roy,†,§ Nirit Kantor-Uriel,†,§ Debabrata Mishra,† Sansa Dutta,‡ Noga Friedman,‡
Mordechai Sheves,‡ and Ron Naaman*,†
†
Department of Chemical Physics and ‡Department of Organic Chemistry, Weizmann Institute, Rehovot 76100, Israel
S Supporting Information
*
ABSTRACT: Spin-dependent photoluminescence (PL) quenching of
CdSe nanoparticles (NPs) has been explored in the hybrid system of
CdSe NP purple membrane, wild-type bacteriorhodopsin (bR) thin film
on a ferromagnetic (Ni-alloy) substrate. A significant change in the PL
intensity from the CdSe NPs has been observed when spin-specific charge
transfer occurs between the retinal and the magnetic substrate. This
feature completely disappears in a bR apo membrane (wild-type
bacteriorhodopsin in which the retinal protein covalent bond was
cleaved), a bacteriorhodopsin mutant (D96N), and a bacteriorhodopsin
bearing a locked retinal chromophore (isomerization of the crucial C13
C14 retinal double bond was prevented by inserting a ring spanning this
bond). The extent of spin-dependent PL quenching of the CdSe NPs
depends on the absorption of the retinal, embedded in wild-type
bacteriorhodopsin. Our result suggests that spin-dependent charge
transfer between the retinal and the substrate controls the PL intensity from the NPs.
KEYWORDS: spin filtering, bacteriorhodopsin, photoluminescence, energy transfer, charge transfer
I
biomolecules including bR and green fluorescent protein
(GFp) were observed before.1,2 This phenomenon is associated
either with fluorescence quenching, fluorescence enhancement,
or nonradiative energy transfer from NPs (donor) to the retinal
(acceptor) and is commonly related to the Förster resonance
energy-transfer (FRET) process.3 This process is sensitive to
the distance between donor and acceptor and can be modulated
by the size of the NPs,11 irradiation intensity, structure, and
morphology of the biosystem.12 Besides these extrinsic
parameters, properties inherent to the NP-Bio system such as
dipole−dipole interactions13 and chirality14,15 play a significant
role in the overall photoluminescent (PL) behavior of such a
hybrid system. It is also known that pure sources of spinpolarized electrons contribute to the spin-dependent PL in
semiconductor16 and spin-dependent exciton formation in a πconjugated system.
Recently, spin-dependent electron transport through wildtype (WT) bacteriorhodopsin (WT bR) was reported.17 This
phenomenon has been attributed to the chirality of the protein
and is another manifestation of the chirality-induced spin
selectivity effect.18,19 In a sequential work it was also
n the last few decades, the combination of biosystems and
nanostructures has been applied to produce new photonic
and electronic devices.1−3 Owing to the special properties
of the biosystems, like structure recognition, self-assembly
abilities, and complex responses to light, new hybrid biodevices
may be used to express novel functions, those that are not
available in the common solid-state photonic/electronic
devices. Purple membrane, which includes bacteriorhodopsin
(bR), is perhaps one of the most promising biosystems that has
been explored for photo/electronic applications.4−6 The
present work focuses on the optical and spintronic properties
of bR, an integral membrane protein in the purple membrane
(PM) of Halobacterium salinarum, which is usually found as
two-dimensional crystalline patches. The retinal, imbedded
inside bR, absorbs light (at about 570 nm), which triggers a
photocycle including several intermediates, which leads to
pumping of protons across the membrane from the internal
cytoplasm to the external medium. As a result, a proton
gradient is generated that is used for ATP synthesis in the
cell.7,8 The proton transfer within PM is accomplished by
charge separation followed by de- and reprotonation of the
retinal.9 Note that the retinal is located at the center of the PM,
i.e., 2.5 nm from both sides of the PM surfaces.1 Relevant to this
work is the realization that this distance is smaller than the
typical Förster radius (5 nm) in energy-transfer processes.10
Excitonic interactions in nanobiohybrid structures based on
semiconductors, nanoparticles (NPs), and photochromic
© 2016 American Chemical Society
Received: January 15, 2016
Accepted: March 27, 2016
Published: March 27, 2016
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was cleaved, and therefore it can be used for the control
experiment (see SI Figure S1). In order to confirm the surface
coverage, atomic force microscopic measurements were carried
on drop-casted WT-bR and APO-bR. The results show that the
surface coverage is almost 100%, and the data confirm that
these drop-casted bR on the surface always form multilayer (see
SI, Figure S2). The orientation of bR membrane on the
substrate was studied in our previous work, and it was found
that the membrane is deposited such that the more negative
side is facing the substrate.20
To elucidate the effect of spin-dependent fluorescent, we
recorded the PL spectra with the magnetic field applied normal
to the Ni-alloy surface in two opposite directions. Figure 2
demonstrated that the degree of spin polarization can be
controlled by light.20
In the present work, we investigated the PL from CdSe NPs
that are adsorbed on a PM that contains bR.1 The hybrid
system, NPs, and the PM are deposited on ferromagnetic Nialloy (see the Supporting Information (SI)). We demonstrate
that the PL intensity strongly depends on the direction of
magnetization of the ferromagnetic substrate. By investigating
the system with modified bR, we are able to conclude that the
alternation in the PL intensity is controlled by spin-specific
electron transfer from the substrate to the retinal, which
consequently affects the efficiency of energy transfer between
the NPs and the retinal.
RESULTS AND DISCUSSION
Figure 1 schematically presents the experimental system in
which a PM that includes bR is adsorbed on a ferromagnetic
Figure 2. PL spectra of CdSe NPs on WT-bR with two different
magnetic field directions (H ∼ 0.5T). Inset shows the maximum
effect obtained for WT-bR.
Figure 1. Schematic diagram of an experimental setup for
measuring PL. A hybrid structure containing semiconductor
nanoparticles (CdSe) of ∼6−7 nm diameter, which are adsorbed
to the bacteriorhodopsin (either WT, APO, mutant, locked retinal,
or reconstitute), imbedded in a PM which is deposited on a Nialloy surface. Magnetic field (field strength ∼0.5T) is applied
normal to the surface of the sample while measuring the PL spectra.
shows the PL spectra from hybrid NPs-bR (WT) recorded with
the magnetic field applied up (↑H) and down (↓H). A clear
change was observed with an average peak-to-peak ratio of the
PL spectra for two directions of the magnetic field of
1.4(±0.1):1 (down:up). The results represent the average
over five different sets of samples, when the maximum ratio
observed was 2.5:1 (inset in Figure 2).
In principle, the magnetic field-induced change in the PL
intensity may result either from variation in the rates of the
energy transfer or the charge transfer. In order to verify the
contribution of the charge transfer, we performed contact
potential difference (CPD) measurements that are sensitive to
the work function (Φ) of the sample. When the sample is
illuminated and charge transfer occurs, a surface photovoltage
(SPV) is developed with a shift in the work function of the
material. Details of the measurements and instrumentation are
given in ref 21.
Figure 3 presents the SPV signal observed for a PM
containing WT bR, with and without NPs. The two columns on
the left show the SPV signal (the change in the CPD signal
upon illumination) when the sample was illuminated at 532 nm
(green light). The amount of charge transferred as a result of
the illumination is almost constant with and without CdSe NPs,
i.e., the amount of charge transfer from NPs is negligible, and
most of the charge transfer occurs between the WT-bR and the
surface. The positive sign of the signal indicates hole transfer
from the retinal to the substrate. In order to confirm this
conclusion, SPV measurements were performed with illumination at 630 nm (red light). The purpose of using red light was
to monitor the charge transfer with negligible retinal excitation
substrate (Ni- alloy) and CdSe NPs are adsorbed to bR on top
of the membrane (see SI). The CdSe NPs’ absorption peak is at
630 nm. Circular dichroism (CD) spectroscopy performed on
the adsorbed membrane confirms that the helical structure of
the proteins in bR is retained when the membrane is adsorbed
on the Ni-alloy surface and that the CD spectra are identical to
those observed in our former studies.17 A well-defined
absorption band centered at ∼570 nm confirms that retinal is
covalently attached to the WT bR and its mutant (D96N) (see
the SI, Figure S1). This observation is consistent with the
proteins not being significantly altered. Emission spectra of the
adsorbed bR were also measured and confirm the intact
structure. In order to adsorb the NPs to bR, CdSe NPs were
dissolved in toluene, and the samples containing bR were
immersed in this solution for 3.5 h. Afterward, the samples were
sonicated for 20 s to remove the excess and weakly bound NPs.
To confirm that the structure was not disturbed, we compared
the emission spectra of bR on Ni-alloy before and after it was
suspended in toluene for 3.5 h (see SI Figure S5). In addition,
the absorption band at 570 nm indicates that immersing the bR
multilayer in toluene does not disturb the bR structure. The
disappearance of the absorption band at 570 nm for apo
membrane bR indicates that the retinal−protein covalent bond
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cannot depend on the sign of the magnetic field, we assume
that there is a cooperative effect leading to the magnetic fielddependent PL. Namely, there is a charge-transfer process
between the retinal and the magnetic substrate, which is
magnetic field dependent. The charge transfer affects the
efficiency of energy transfer between the NPs and the retinal;
hence it affects the PL. Therefore, the magnetization of the
substrate “gates” the energy transfer from NPs to the retinal by
controlling the charge transfer from the retinal to the substrate.
The validity of the proposed model will further be strengthened
by the results described below.
To pinpoint the role of the retinal chromophore as the
intermediate in the process, we have modified the WT bR
structure by site-directed mutagenesis to form the D96N
mutant. Details on the modifications were published elsewhere.15 Experiments similar to those that led to the results in
Figure 2 were repeated for a CdSe NPs-bR (D96N) hybrid
structure and no effect of the magnetic field could be observed
(Figure 4A). Moreover the PL signal is stronger than in the
case of WT bR, indicating that there is no efficient energy
transfer.
The lack of a magnetic field effect, in the case of the mutant,
is accompanied by an inefficient charge-transfer process, as
observed in the SPV experiment (Figure 5). The SPV signal is
about −50 mV vs about −30 mV obtained with the bare
substrate. Here we observed negative values which indicate
electron transfer from the NPs and not positive values (hole
transfer), as was observed in the WT bR. Since in the mutant
Figure 3. SPV (ΔCPD) of WT bR deposited on Ni-alloy surfaces
with and without CdSe nanoparticles illuminated in two different
wavelengths and the control for the bare Ni-alloy substrate.
(630 nm should mostly excite the CdSe NPs). Indeed, when
the experiment is performed with red light, there is almost no
response to the light (i.e., when the SPV signal is low, charge
transfer between the NPs and the surface is negligible, as shown
in Figure 3). Therefore, this result suggests that the PL
intensity from the NPs is mainly affected by the energy-transfer
rate, and variation in the energy-transfer efficiency should
account for the observed magnetic field. Since the energytransfer rate itself should not be spin dependent and therefore
Figure 4. PL from CdSe NPs for substrates that are magnetized normal or antinormal to the surface for various mutations of the retinal. (A)
Mutant (D96N), (B) APO bR, (C) locked retinal, (D) reconstituted bR.
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WT bR. Hence, the retinal should not be able to accept any
energy transferred from the NPs. Indeed, Figure 4B shows no
change in PL intensity upon changing the direction of the
magnetic field. This observation proves that the excited retinal
plays an important role in the observed effect. In this context,
SPV data for an apo bR-modified surface with and without
CdSe NPs (Figures 5) show an inefficient charge transfer both
between the CdSe NPs and the surface and between the retinal
and the surface (the low response that was observed may come
from a small portion of bR in which the retinal is still bonded to
the protein).
For additional verification of the role of the retinal in the
magnetic field-controlled PL, the external magnetic fielddependent PL process was studied with two other modified
bR forms. The first is an artificial pigment derived from a
synthetic “locked retinal” in which the retinal has been modified
such that isomerization around the crucial C13C14 double
bond is prevented (see Methods). The second is a
reconstituted bR to evaluate the effect of mere bleaching and
retinal reconstitution processes. In the first case, no change in
the PL intensity was observed, as a function of the direction of
the magnetization of the substrate (Figure 4C), whereas for the
reconstituted bR, a clear difference in PL intensity was found
(Figure 4D). However, the intensity ratio (up:down = 1.2:1) is
Figure 5. SPV (ΔCPD) of mutant and APO bR deposited on Nialloy surfaces illuminated at 533 nm.
the M photochemically induced intermediate is accumulated,
the retinal in the bR mutant dark state cannot be excited, and
the lack of a magnetic field effect suggests that retinal excitation
is essential for quenching the fluorescence of the NPs.
As another control, magnetic field-dependent studies were
performed on apo bR, which lacks the retinal−protein covalent
bond, leading to absorption at 360 nm instead of 570 nm in the
Scheme 1. Process Leading to Magnetically Controlled PL from the CdSe NPsa
a
(A) The system consists of a ferromagnetic substrate (gray on the right) on top of which a PM that includes bacteriorhodopsin (bR) is deposited.
CdSe NPs are adsorbed to the bR. Commonly upon excitation of bR with green light, a photocycle is initiated by isomerization of the retinal
chromophore. (B) In the system studied, the same light also excites the NPs. (C) If the ferromagnetic substrate is magnetized so that spins can be
injected from it into the chiral bR, following photoexcitation of the bR, an electron will be transferred to the hole in the excited bR, the retinal will be
quenched to its ground state so that it can absorb a photon again and form the excited state to which energy transfer can occur, and the PL signal will
be reduced. (D) In the case that the magnetic substrate is magnetized so that the spin transfer to the excited retinal is slower, the retinal excited state
will complete its lifetime, and the regular photocycle will take place, reducing the probability for multiple retinal excitation and therefore reducing the
probability for energy transfer from the NPs to the retinal.
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by the slow electron transfer from the substrate, when it is
magnetized in the “wrong” direction.
The proposed model is based on two photons that must be
absorbed by the system simultaneously. Figure 6 indeed
indicates that this effect depends on the intensity square.
smaller than for WT bR, and the sign of the magnetic field
effect is reversed.
The existence of the effect in the reconstituted bR indicates
that the absence of the effect in the locked artificial pigment is a
property of the pigment itself and does not originate from the
reconstitution process. The switch in the sign of the signal may
result from some structural changes in the reconstituted bR
versus the WT. In recent studies it was found that structural
changes may affect the sign of the spin preferred in the electron
transfer.22 Finally, the effect of the direction of the magnetic
field on the PL was monitored on a sample containing only WT
bR without NPs (see SI, Figure S3). No effect of the magnetic
field was found.
To probe the importance of simultaneously exciting the NPs
and the retinal, we conducted the experiments on WT bR with
NPs using 488 nm light. At this wavelength, the absorption of
the NPs is higher than at 514 nm; however, the retinal
absorption is much weaker. A significant change in the PL
intensity was found (see SI, Figure S4); however, the intensity
ratio (down:up = 1.15:1) is smaller than in the case of
illumination at 514 nm. This observation can be explained only
if the effect involves a cooperative mechanism and it cannot be
explained by simple spin-dependent charge transfer between
the NPs and the surface.
Based on extensive experimental work with several modified
forms of bR, we propose the following mechanism (see Scheme
1) for the observed magnetic field-controlled PL. It assumes
that after irradiation at 514 nm, both CdSe NPs and the retinal
are excited, and subsequently energy is transferred from the
excited CdSe NPs to the excited retinal. Furthermore, it is
assumed that energy transferred does not occur from the
excited CdSe NPs to the retinal ground state. If the excitation
of the retinal is followed by the photocycle, no energy transfer
can occur from the NP to the retinal all through the photocycle
time. A competitive process involves electron transfer from the
magnetic substrate to the excited retinal. This process prevents
the retinal excited state to isomerize and to initiate the regular
bR photocycle. In our previous work, we found that electron
transmission through WT bR is spin specific.20
Since the electron transfer between the substrate and the
retinal is spin selective, the direction of magnetization of the
substrate defines its rate. If the substrate is magnetized so that it
has a substantial density of populated states of the correct spin,
namely, the spin that can be transferred from the substrate to
the excited retinal through the chiral protein, then the electron
transfer from the surface to the retinal is efficient, and the
retinal is quenched to its ground state so that it can absorb a
photon again and form the excited state to which energy
transfer can occur. On the other hand, if the substrate is
magnetized in the opposite direction, the electron transfer from
the substrate to the retinal is blocked, due to the very low
density of the populated states having the correct spin, and the
retinal excited state continues to its regular photocycle.
Consequently the time it takes for the retinal to return to its
ground state is longer, reducing the probability for multiple
retinal excitation and therefore reducing the probability for
energy transfer from the NPs to the retinal.
In short, the mechanism we propose assumes that for
observing efficient energy transfer from the NP to the excited
retinal, the excited retinal has to be quenched fast so as to be
ready for reabsorption of photon. The return of the retinal to
its ground state can be hindered by the photocycle process or
Figure 6. Difference in the fluorescence intensity for a magnetic
field of the substrate pointing up versus down, as a function of the
laser intensity. The results are fitted to the intensity square with R =
0.95.
The strong effect of the magnetic field observed can be
rationalized by the short lifetime of the excited retinal (about
0.5 ps) versus that of the excited NPs (ns). Hence, the retinal
can be excited many times within the lifetime of the NP, and
therefore the probability for energy transfer from the NPs to
the retinal is enhanced by up to a factor of 2000.
The model presented above is confirmed by studying the
systems that contain bR with various modifications. In the
D96N mutant, the M intermediate is accumulated, following
photoexcitation, and therefore there is no retinal in the excited
state that can accept energy from the NPs, and the retinal does
not return to its ground state. The same holds for the apo
system. The lack of an effect in the “locked” system also
indicates that the effect is associated with the lifetime of the
retinal excited state. Since retinal isomerization is prevented in
the locked pigment, its excited lifetime is prolonged from 0.5 ps
(WT) to 20 ps,23,24 and therefore the probability of the retinal
to return to its ground state increases, and it can be excited
multiple times so that efficient energy transfer from the NPs to
the retinal can occur at both directions of the magnetic field.
CONCLUSION
Our results indicate a system in which spintronic properties
control PL. In the hybrid NP-bR structure, the chirality of the
protein induces spin-dependent electron transfer from a
magnetic substrate to the retinal moiety, inside the bR. This
electron transfer depends on the direction of the substrate’s
magnetization. The electron-transfer process “gates” the energy
transfer from the excited NPs to the excited retinal.
METHODS
Figure 7 presents the structure of the retinal and of the “locked retinal”
used in the current study.
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Figure 7. Structure of the retinal (on the left) and the “locked retinal” (on the right). In the latter no isomerization can occur upon
photoexcitation.
Absorption Spectra. The absorbance spectra were measured on a
HP 8453 UV−vis spectrometer, and the CD spectra of bR films were
measured on a Chirascan spectrometer, Applied Photo Physics,
England.
Surface Photovoltage (SPV) Measurements. SPV measurements were used to quantify the amount of photo-induced charge
transfer in these assemblies. CPD measurements provide the work
function (Φ) of the sample by measuring the electric potential
between the sample and a reference plate. When the sample is
illuminated and charge transfer occurs, a SPV is created; i.e., a work
function shift occurs. Based on the SPV measurements, it is possible to
determine the direction and the extent of the electron transfer (for a
given illumination intensity) between the NPs and the substrate. If an
electron is transferred from the NP layer to the substrate, the surface’s
work function decreases, whereas the work function increases if
electrons are transferred in the opposite direction. Thus, the sign of
the SPV signal provides the direction of electron transfer, and its
magnitude is proportional to the change in the work function resulting
from the light-induced dipole moment that arises from charge transfer
between the NPs and the substrate.
Photoluminescence (PL) Measurement. The PL measurements
were carried out by using a LabRam HR800-PL spectrofluorimeter
microscope (Horiba Jobin-Yivon). Typically, 514 nm laser light
(argon-ion CW laser at ∼15 mW/cm2) has been used for excitation of
CdSe NPs. The incident light was impinged on the surface at an angle
90° to the sample surface. Prior to collecting the PL spectra, an area
(typically, 20 au × 20 au) and number points (25 points) within this
area were defined in order to map the surface. Afterward, the PL
spectra were collected using a microscope (with a 5× high-working
distance lens). During the measurement, a confocal aperture (1100
μm) was fully opened, and the integration time was maintained at 15 s.
Finally, the spectra were presented after averaging out the PL of
individual points within the defined area at two different magnetic
orientations. The external magnetic field dependence on the PL of the
CdSe NP assembly, connected to the magnetic substrate via bR, was
investigated at room temperature.
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ASSOCIATED CONTENT
S Supporting Information
*
The Supporting Information is available free of charge on the
ACS Publications website at DOI: 10.1021/acsnano.6b00333.
Detailed about the sample preparation, characterization
of the samples, and results from controlled PL
experiments (PDF)
AUTHOR INFORMATION
Corresponding Author
*E-mail: ron.naaman@weizmann.ac.il.
Author Contributions
§
These authors contributed equally.
Notes
The authors declare no competing financial interest.
ACKNOWLEDGMENTS
This work was partially supported by the ERC-Adv grant and
by the Israel Science Foundation.
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