Optimizing electron transfer from CdSe QDs to hydrogenase for photocatalytic H2 production

Article abstract of DOI:10.1039/c9cc01150a

A series of viologen related redox mediators of varying reduction potential has been characterized and their utility as electron shuttles between CdSe quantum dots and hydrogenase enzyme has been demonstrated. Tuning the mediator LUMO energy optimizes the performance of this hybrid photocatalytic system by balancing electron transfer rates of the shuttle.

Full text of DOI:10.1039/c9cc01150a

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DOI: 10.1039/C9CC01150A
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Optimizing Electron Transfer from CdSe QDs to Hydrogenase
for Photocatalytic H2 Production
Monica L. K. Sanchez,a Chang-Hao Wu,b Michael W. W. Adams,b R. Brian Dyer*a
Received 00th January 20xx,
Accepted 00th January 20xx
DOI: 10.1039/x0xx00000x
www.rsc.org/
A series of viologen related redox mediators of varying reduction electron relays largely because of their stable, long-lived
potential has been characterized and their utility as electron radicals, commercial availability and solubility in water.9-12 Most
shuttles between CdSe quantum dots and hydrogenase enzyme has studies aimed at optimizing ET to and from the mediator have
been demonstrated. Tuning the mediator LUMO energy optimizes focused on manipulating the light harvesting/charge separation
peformance of this hybrid photocatalytic system by balancing material.9, 10 Not as much attention has been given to tuning the
electron transfer rates of the shuttle.
mediator structure and redox potential for improving ET
efficiency.8,
Here, we have investigated the effects of
12, 13
Artificial photosynthetic systems usually employ separate
modules to accomplish the essential functions of efficient light
harvesting, charge separation and catalytic proton coupled
electron transfer (PCET) reactions to make high energy chemical
bonds.1-3 This approach mimics natural photosynthetic systems
and allows for the independent optimization of each module for
its specific task. Hybrid quantum-dot/enzyme photocatalysts are
promising examples of this modular approach.3-5 The nano-
crystalline semiconductor (NCS) material acts as both the light
harvesting and charge separation module. It can be designed to
generate long-lived reductive or oxidative equivalents with high
quantum efficiency. Enzymes that catalyze PCET reactions
operate with little overpotential at rates that match or exceed the
rate of generation of redox equivalents by the solar flux.6
Thermophilic enzymes have high stability and durability,
yielding high turnover numbers (TON).7 Even when these
modules have been highly optimized, however, the difficult
challenge that remains is how to transfer reactive electrons
between modules. Both natural and artificial systems have
employed redox mediators, small molecule electron carriers
capable of moving between modules and efficient redox cycling.
The challenges with this approach include generating sufficient
driving force for multiple electron transfer (ET) steps, efficient
interfacial ET and avoiding back ET.8 Methyl viologen (MV)
and closely related molecules have been widely employed as
mediator structure and reduction potential on the overall
efficiency of a hybrid CdSe quantum-dot/mediator/[NiFe]-
hydrogenase photocatalytic system. We varied the structure of
viologen-like mediators by introducing methyl substituents and
a carbon chain linking the two pyridyl nitrogens, as shown in Fig.
1. These modifications expand the range of reduction potentials
of the mediators. We characterized this series of mediators
structurally, spectroscopically and electrochemically and
determined the effects of these mediator properties on
photocatalytic production of hydrogen in the hybrid
QD/hydrogenase system.
The mediator structure influences its performance as an
Fig. 1 Viologen-like molecules utilized as electron shuttles, along with electrochemically
determined reduction potentials (vs. NHE). The numbering scheme refers to the position
of the methyl substituents (4 or 5) and the length of the carbon chain (2 or 3). The X-ray
structures (right) of DQ52 and DQ03 show how the twist angle depends on the carbon-
linker chain length.
a. Department of Chemistry, Emory University, Atlanta, GA 30322 USA.
b. Department of Biochemistry and Molecular Biology, University of Georgia,
Athens, GA 30602 USA.
†Electronic Supplementary Information (ESI) available: Experimental details,
additional structural and spectral characterization of mediators and QDs, quantum
efficiency measurements. See DOI: 10.1039/x0xx00000x
This journal is © The Royal Society of Chemistry 20xx
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electron shuttle in several ways. The position of the pyridyl of the reduced mediator versus illumination time (Fig. 2B) is
View Article Online
DOI: 10.1039/C9CC01150A
methyl substituent affects both the electronic structure of the determined from the measured extinction coefficient of each
mediator and the sterics of its interaction with a nanocrystalline radical species. QErad was determined by dividing the moles of
semiconductor surface. The carbon chain linking the two pyridyl radical generated by the moles of photons absorbed by the
nitrogens introduces a twist in the torsion angle of the two rings
that depends on the chain length. Evidence of the twist along the
bipyridine core is clear in the X-ray structures (Fig. 1) and in
NMR spectra (Fig. S1, ESI†) of the mediators and is consistent
with previous reports.14 Representative X-ray structures for
DQ52 and DQ03 are presented in Fig. 1 (detailed structural
information for all mediators given in Tables S1, S2, ESI†). The
average torsional twist between pyridyl rings was ~19° for those
mediators with a two-carbon chain linker and ~53° for those with
a three-carbon chain linker. The torsional twist also causes
important changes to the electronic structure of the mediators.
These changes are reflected in the reduction potential, which
becomes more negative as the torsional twist increases. Previous
molecular orbital (MO) calculations for mediators with 2C and
3C linkers showed that increasing the torsional twist disrupts the
conjugated system and shifts the LUMO to a higher energy.14
The effect on mediator electronic structure is also reflected in the
Fig. 2. Steady-state photoreduction experiments with CdSe QDs and mediators. (A) UV-
vis extinction spectra for reduced mediators compared to oxidized DQ032+; spectra are
offset for clarity. (B) Kinetics of photoreduction of mediator, quantified by monitoring
absorbance at 450 or 510 nm for 2C or 3C linked radical species, respectively. (C)
Dependence of quantum efficiency for reduction of mediators on reduction potential.
(D) Schematic depicting the ET processes and energies of CdSe QD conduction band (CB)
and valence band (VB) relative to the mediator LUMO energies.
UV-Vis absorbance spectra of the di-cation and mono-cation
forms (Fig. 2 and Fig. S2, ESI†). The p®p* transition of the di-
cation is observed to shift to higher energy with increasing
torsional twist.15 This blue shift is related to the change in ∆E
between HOMO and LUMO with twist angle. MO calculations
indicate that ∆E increases due to the increase in the LUMO
energy, consistent with our observation of more negative
reduction potentials in the cyclic voltammetry data (Fig. S3).14
In contrast, the p®p* transition of the reduced mediators is
observed to shift to lower energy with increasing linker length
solution and correcting for reflection from the front face of the
cuvette. We calculate the quantum yield from the first 10 seconds
of illumination, before the concentration of mediator•+ builds up,
thus minimizing contributions from back ET (kCR) and other
parasitic processes that lead to mediator degradation (full details
of the calculation are presented in the ESI†).7
(Fig. 2A). This red-shift has been attributed previously to a more
15
planar structure for the radical species.14,
The decrease in
torsional twist associated with radical cation formation allows
for a greater degree of orbital overlap between the bipyridinium
rings, leading to the lower energy transition. Slower ET rates are
observed as the twist angle is increased, due to an increase in
reorganization energy required to reach the planar structure of
the reduced state.16 Electronic structure calculations of DQ03
also support a change in geometry of the mediator from the
twisted form to a more planar configuration upon reduction.14
The first step in the electron shuttle process is ET from the
conduction band (CB) of the excited CdSe QD to the mediator.
We performed steady-state photo-illumination experiments to
determine the quantum efficiency for reduction of the mediator
(QErad) as shown in Fig. 2. Illumination of the CdSe QD with
blue light (405 nm) produces an exciton state, which the mediator
quenches by extracting an electron from the CB, generating a
population of the reduced mediator radical cation (mediator•+).
The hole left in the VB of the CdSe QD is scavenged by the
sacrificial electron donor (SED), mercaptopropionic acid
(MPA). This ET event (kCS) is depicted schematically in Fig. 2D
with the relative LUMO energies of the mediators. Absorbance
spectra of the radical cations are shown in Fig. 2A. The
absorbance feature at either 450 nm or 510 nm was monitored
for each mediator depending on whether the spectrum belonged
to a 2C or 3C linked molecule, respectively. The concentration
The rate of formation of mediator•+ is constant in the first 10
seconds but begins to decline after this initial phase (Fig. 2B).
The decrease in the rate of formation of mediator•+ is attributed
to consumption of the mediator di-cation and to an increased rate
of charge recombination at high concentrations of mediator•+. At
longer times, the rate of mediator reduction and charge
recombination are balanced and the system reaches a steady
state. The initial rates of mediator•+ formation and steady state
concentrations vary with the reduction potential of the mediator
(Fig. 2B), with the 2C linker mediators having significantly
faster initial rates and reaching larger steady state populations
than the 3C linker ones. It is clear the 2C linker molecules, DQ42
and DQ52, have the highest net QErad (Fig. 2C). The differences
in QErad is best explained by considering the faster kCS and the
slower kCR observed for the 2C linked mediators relative to the
3C linked ones. The result of a faster kCS and slower kCR is a net
higher QErad and therefore larger steady state populations of
reduced mediator, as strongly suggested by the steady-state data.
The differences in ET rates and net QErad for this series of
mediators can be understood in terms of the reduction potentials,
which influence both the forward and reverse ET reactions.17 Fig.
2C shows the dependence of the net QErad on the reduction
potential of the mediator. The energetics of this process are
illustrated in Fig. 2D, where the relative energy levels were
2 | Chem. Commun., 2019, 00, 1-4
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determined from the reduction potentials of the mediators and
the band edge of the CdSe QDs. The 2C linker mediators with
the more positive redox potentials (lower energy LUMO’s) have
a larger downhill driving force for forward ET and a smaller
driving force for back ET, resulting in larger kCS and smaller kCR
(normal Marcus regime). The net result is a long-lived charge
separated state and high QErad. The situation is more complex for
the 3C linker mediators, since their more negative reduction
potential yields a driving force for back ET in the Marcus
inverted regime, resulting in a decrease in kCR.
Table 1 Steady State Hydrogen Production (at 5000 sec)
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DOI: 10.1039/C9CC01150A
Mediator
Solution Potential (mV)a
Moles H2
QEcorr (%)
DQ52
DQ42
DQ03
DQ53
DQ43
-375
-385
-410
-425
-495
4.1x10-7
8.1x10-7
2.7x10-6
3.7x10-6
2.6x10-6
4.7
7.8
14.8
16.8
11.5
[ꢅꢆꢇꢈ•
]
aVersus SHE; determined from the Nernst equation: ∆ꢀ = ∆ꢀ° − ꢁꢂ ꢃꢄ
Ϝ
[ꢅꢆꢇꢉꢈ]
It is also likely that the rate of ET from the QD to the
mediator and the net QErad are affected by the differences in
reorganization energy for forward and reverse ET across this
series. The reorganization energy is influenced by the torsional
twist between the pyridyl rings of the mediators, since the
reduced mediator adopts a more planar structure.16 Thus, the
reorganization energy for the more highly twisted 3C linker
molecules is expected to be larger than that for the 2C linker
molecules. This increased reorganization energy is expected to
slow down the ET to the 3C linker molecules relative to the 2C
linker ones, leading to less efficient charge separation. For
example, the net QErad drops dramatically from 74% to 31%
between DQ42 and DQ03 as the twist in the bipyridyl core is
increased from ~22° to ~55°. Further study would be required to
assess the relative contributions of reorganization energy and
driving force to the difference in net QErad, but both are likely
important.
hybrid photocatalytic systems.7 The current results are consistent
with the previous ones, showing greater overall efficiency of
hydrogen production with increased driving force for electron
transfer from the reduced mediator to the enzyme. The highest
observed quantum efficiency for H2 production is modest (QEhyd
= 16.8%) compared to previous results with nanorods (QEhyd
=
52% for similar conditions). This difference in efficiency is
primarily due to the NCS photosensitizer, since the nanorod
structure has a significantly longer exciton lifetime than the QD,
leading to a greater efficiency of the charge separation process.
Nevertheless, the yields for the three highest performing
mediators in the present work are significantly higher than what
has been observed previously with CdSe QD’s.19
The next step in the electron shuttle process is ET from
mediator•+ to the hydrogenase and turnover of the enzyme to
produce hydrogen. We measured hydrogen production
efficiency for a hybrid system consisting of CdSe QDs, mediator
and the [NiFe] SHI from Pyrococcus furiosus (Pf) as the
hydrogen production catalyst. Pf SHI is a robust catalyst, having
high thermal stability and oxygen tolerance.18 It also has a high
turnover rate at neutral pH (100 s-1 at room temperature) and
operates near the thermodynamic potential of the hydrogen
couple. Hydrogen production assays were carried out at pH 7.1
under conditions analogous to those used in the mediator
photoreduction experiments. Fig. 3A shows the time dependent
yields of light driven hydrogen production for each of the
mediators. Furthermore, addition of a mediator to this hybrid
system significantly improves overall quantum yield for
hydrogen production compared to related systems that rely on
direct ET from the NCS material to the hydrogenase. The net
production of H2 and the corrected QEhyd for each mediator are
summarized in Table 1.
Fig. 3. Steady-State H2 Production. (A) H2 production as a function of laser illumination
time: DQ53 (purple), DQ43 (green), DQ03 (blue), DQ42 (yellow), DQ52 (pink), no
mediator present (black). (B) Correlation of H2 generation efficiency (QEhyd) with
reduction potential. (C) Production of reduced mediator versus illumination time with
H2ase (closed circles) and without H2ase (open circles). (D) Energy diagram of ET steps.
Trends in the QEhyd indicate a strong correlation between the
reduction potential of the mediator and amount of H2 produced
as shown in Fig. 3B. Previously, we investigated the effect of the
mediator reduction potential on the efficiency of a related hybrid
CdSe/CdS nanorod-hydrogenase photocatalytic system.7 We
compared two mediators, methyl viologen (MV2+, E0 = -446 mV
vs. NHE) and DQ03 (or PDQ2+, E0 = -550 mV vs. NHE) and
found significantly better performance with DQ03, due to its
greater driving force for ET to the surface exposed FeS cluster
of SHI. With DQ03 and nanorods, we achieved the highest
reported quantum yield for hydrogen production with such
The correlation of photocatalytic hydrogen production
efficiency with reduction potential of the mediator is inverse to
the trend observed for the steady-state mediator photoreduction
experiments. This observation highlights the complex interplay
between the net yield of hydrogen production and the rates of
charge separation, charge recombination and ET to the enzyme,
as shown in the scheme in Fig. 3D. Optimum hydrogen
production requires a balance between driving force for the two
forward ET processes; decreasing the mediator LUMO energy
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decreases the driving force for ET to the catalyst (kET), but at the mediator that serves as an electron shuttle betweeVnietwhAertQicleDOnalinned
same time increases the driving force for reduction of the enzyme. Optimum performance requirDesOI:a10.c10a3r9e/fCu9lCCb0a1la15n0cAe
mediator (kCS). Thus, while the mediators that are easier to among the rates of charge separation, ET to the enzyme and
reduce (lower LUMO energies) exhibit a higher quantum charge recombination, which can be achieved by tuning the
efficiency for photoreduction by the QDs, they are less effective energy of the mediator LUMO. The versatility of this modular
at reducing the enzyme and producing hydrogen. In contrast, system makes it attractive for additional studies with other
charge recombination becomes more rapid as the LUMO energy photosensitizer materials and with other biological or manmade
is increased, which lowers the net yield of photoreduction in the catalysts for PCET processes such as CO2 reduction.
absence of enzyme. In the presence of enzyme, however, ET to
the enzyme is competitive with charge recombination and thus structure determination. Funding for this work was provided by
efficient hydrogen production can be achieved. the National Science Foundation (grants CHE1807865 and
The authors thank Dr. John Bacsa for help with X-ray crystal
Further insight on the optimum parameters for hydrogen DMR1808288 to RBD) and by the Division of Chemical
production is provided by considering the solution potential Sciences, Geosciences and Biosciences, Office of Basic Energy
achieved under illumination at steady state. Fig. 3C shows the Sciences of the U.S. Department of Energy (grant DE-FG05-
production of reduced mediator as a function of illumination time 95ER20175 to MWA).
for DQ03, DQ43, and DQ53 mediators with and without
hydrogenase present. The reduced mediator concentration
Conflicts of interest
There are no conflicts to declare.
increases initially then reaches a constant value; a lower steady
state population is reached in the presence of hydrogenase, due
to ET to the enzyme. It is clear that in all cases the system reaches
steady state (constant mediator•+ concentration) within an hour.
Therefore, we determined the steady state solution potential by
measuring the concentration of reduced mediator from the
radical absorbance after 5000 sec of illumination. The Nernst
equation was then used to calculate the solution potential from
the relative concentration of mediator•+/mediator++, yielding the
values shown in Table 1. For comparison, at pH 7.1 the hydrogen
couple is at -419 mV. The most efficient mediators DQ03, DQ53
and DQ43 reach steady state solution potentials near or more
negative than the hydrogen couple. In contrast, with DQ42 and
DQ52 the steady state solution potentials are significantly more
positive than the hydrogen couple and therefore proton reduction
is not as favorable for the 2C linker mediators.
The hydrogen production efficiency peaks with DQ53 even
though it does not have the most negative reduction potential.
DQ53•+ concentration levels close to those observed for DQ03•+
are achieved when the solution contains solely dots and mediator
(Fig. 3C). When the enzyme is present, however, steady state
illumination produces a barely observable population of DQ53•+,
indicating that its consumption by the enzyme is rapid. Based on
this evidence, it is likely that the conditions are not fully
optimized for hydrogen production in the case of DQ53.
Utilization of a photosensitizer with a longer-lived exciton, such
as a nanorod, would increase the QEhyd produced with DQ53,
since it would increase QErad. The lower QEhyd observed with
DQ43 is in part due to inefficient ET to the enzyme despite its
more negative reduction potential, resulting in a higher steady
state population of mediator•+ compared to DQ53 (Fig. 3C).
Slower ET to the enzyme for DQ43 might be an indication of
entrance into the Marcus inverted regime, wherein having an
increased driving force slows ET to the enzyme, resulting in a
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