Solar-Powered Organic Semiconductor–Bacteria Biohybrids for CO2 Reduction into Acetic Acid

Article abstract of DOI:10.1002/anie.202001047

An organic semiconductor–bacteria biohybrid photosynthetic system is used to efficiently realize CO₂ reduction to produce acetic acid with the non-photosynthetic bacteria Moorella thermoacetica. Perylene diimide derivative (PDI) and poly(fluorene-co-phenylene) (PFP) were coated on the bacteria surface as photosensitizers to form a p-n heterojunction (PFP/PDI) layer, affording higher hole/electron separation efficiency. The π-conjugated semiconductors possess excellent light-harvesting ability and biocompatibility, and the cationic side chains of organic semiconductors could intercalate into cell membranes, ensuring efficient electron transfer to bacteria. Moorella thermoacetica can thus harvest photoexcited electrons from the PFP/PDI heterojunction, driving the Wood–Ljungdahl pathway to synthesize acetic acid from CO₂ under illumination. The efficiency of this organic biohybrid is about 1.6 %, which is comparable to those of reported inorganic biohybrid systems.

Full text of DOI:10.1002/anie.202001047

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Accepted Article
Title: Solar−Powered Organic Semiconductor−Bacteria Biohybrids for
CO2 Reduction into Acetic Acid
Authors: Shu Wang
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To be cited as: Angew. Chem. Int. Ed. 10.1002/anie.202001047
Angew. Chem. 10.1002/ange.202001047
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COMMUNICATION
Solar−Powered Organic Semiconductor−Bacteria Biohybrids for
CO Reduction into Acetic Acid
2
a,b
a,b
a,c
a
b
a
a
a, c
Panpan Gai , Wen Yu , Hao Zhao , Ruilian Qi , Feng Li* , Libing Liu , Fengting Lv , Shu Wang*
Abstract: Photosynthetic biohybrid systems have emerged as a
promising platform for solar-to-chemical conversion by integrating
excellent light-harvesting ability of semiconductors with the synthetic
capability of biological cells. How to enhance the utilization of solar
energy, hole/electron separation efficiency and the electron transfer
between the semiconductor and biological cells is crucial to develop
high-performance photosynthesis platforms. In this work, we
reduction,[6-9] hydrogen production,[10,11] and dinitrogen
fixation,[12] etc. Among them, compared with that of the
bioenzyme, the whole-cell strategy has the advantages of self-
replicate and self-repair, as well as the involvement of the
complete biological process.[8,9] In the biological cell-based
photosynthetic biohybrid systems, the main light-harvesting
materials are generally the inorganic semiconductors, such as
cobalt phosphate (CoP),[3] indium phosphide (InP),[6] cadmium
sulfide (CdS),[7,12] and gold nanoclusters (AuNCs).[8] However, in
terms of the inorganic semiconductors, the toxicity of heavy
metals and phototoxicity to organisms are unfavorable for
photosynthetic biohybrid systems. In addition, the optical
property of inorganic semiconductors was also difficult to
regulate. Thus, how to enhance the solar energy capture ability,
hole/electron separation efficiency and the electron transfer from
the semiconductor to microorganisms is crucial to develop high-
performance photosynthesis platforms.[1]
developed
an
organic
semiconductor−bacteria
biohybrid
reduction
photosynthetic system, which could efficiently realize CO
2
to produce acetic acid through non-photosynthetic bacteria Moorella
thermoacetica. As the photosensitizers, both cationic electron-
transporting (n-type) perylene diimide derivative (PDI) and hole-
transporting (p-type) poly(fluorene-co-phenylene) (PFP) were coated
on the bacteria surface to form p-n heterojunction (PFP/PDI) layer,
affording higher hole/electron separation efficiency. The -
conjugated semiconductors possess excellent light-harvesting ability
and biocompatibility, and more importantly, the cationic side chains
of organic semiconductors could intercalate into cell membrane,
ensuring the efficient electron transfer to bacteria. As a result,
Moorella thermoacetica can harvest photoexcited electrons from the
PFP/PDI heterojunction, which can drive the Wood-Ljungdahl
Organic semiconductors, especially -conjugated molecules,
aroused our interest because of their good biocompatibility to
organisms in versatile biological system,[13-15] desirable
photoelectronic conversion capacity in electrochemical
devices,[
16,17]
as well as the fine-tuned frontier molecular orbital
pathway to synthesize acetic acid from CO
2
under illumination. The
energy levels and optical band gap.[
18,19]
Very recently, the
efficiency of this organic biohybrid is  1.6 %, which is comparable to
those of reported inorganic biohybrid systems. This work opens a
new avenue to explore bioenergy application of organic
semiconductors, and also provides a convenient biomanufacturing
approach to design organic semiconductor−bacteria biohybrids for
efficient solar-to-chemical conversion.
conjugated polymers have been found to exhibit the ability to
accelerate electron transfer to thylakoid, leading to the
enhancement of the photosynthesis of chloroplasts.[20,21] More
importantly, cationic conjugated polymers can greatly enhance
extracellular electron transport exoelectrogen to the electrode by
intercalating into the membrane of bacteria through electrostatic
interactions and hydrophobic interactions.[22] Thus, it can be
seen that organic conjugated semiconductors could provide an
excellent opportunity to develop efficient solar-to-chemical
conversion biohybrid systems. To the best of our knowledge,
organic semiconductors−bacteria biohybrid photosynthetic
system has not been explored up to date. In this work, we
developed an organic semiconductor−bacteria biohybrid
As one emerging technology, photosynthetic biohybrid systems
are considered as the promising chemical synthesis platform by
taking advantage of excellent light-harvesting ability of
semiconductors and the synthetic ability of biological cells or
bioenzyme.[1,2] Versatile solar-to-chemical production have been
investigated,
including
cofactor
regeneration,[3-5]
CO
2
photosynthetic system, which could efficiently realize CO
2
reduction to produce acetic acid through non-photosynthetic
bacteria Moorella thermoacetica (M. thermoacetica, ATCC
[
a]
Prof. S. Wang, Dr. L. Liu, Dr. F. Lv, Dr. P. Gai, W. Yu, H. Zhao, R.
Qi
Beijing National Laboratory for Molecular Sciences, Key Laboratory
of Organic Solids, Institute of Chemistry, Chinese Academy of
Sciences, Beijing 100190, P. R. China.
3
9073). Taking advantage of good solar energy capture ability
of -conjugated molecules, excellent biocompatibility, good
hole/electron separation efficiency of p-n heterojunction of
PFP/PDI pair and the enhanced electron transfer from PFP/PDI
to M. thermoacetica, this biohybrid system could efficiently
realize CO reduction to produce acetic acid under light
2
illumination with an efficiency of 1.6 %.
Scheme 1a shows the diagram of the PDI/PFP/M.
thermoacetica photosynthesis biohybrid system. To enhance the
hole/electron separation efficiency, the p-n heterojunction layer
composed of cationic PDI and PFP was served as the
photosensitizer through simultaneously coating them onto the
bacteria surface. Furthermore, it was found that PDI and PFP
interacted with M. thermoacetica by electrostatic interactions
and their cationic side chains could intercalate into cell
E-mail: wangshu@iccas.ac.cn
[
[
b]
c]
Prof. F. Li, Dr. P. Gai, W. Yu
College of Chemistry and Pharmaceutical Sciences, Qingdao
Agricultural University, Qingdao 266109, P. R. China.
E-mail: lifeng@qau.edu.cn
Prof. S. Wang, H. Zhao
College of Chemistry, University of Chinese Academy of Sciences,
Beijing 100049, P. R. China
Supporting information for this article is given via a link at the end of
the document.
1
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Scheme 1. Schematic diagram of the PDI/PFP/M. thermoacetica photosynthesis hybrid system (a) and the photoexcited electron
generated from PDI/PFP under illumination transferred by the membrane protein and finally passed on to the Wood–Ljungdahl
pathway for CO reduction(b). (c) The chemical structures of PFP, PDI, Cys and CySS.
2
the change from negative to zero for PDI/M. thermoacetica and
from a largely positive value to zero for PFP/M. thermoacetica,
owing to the different binding modes. In detail, the binding of PDI
and M. thermoacetica was an exothermic process mainly
caused by the electrostatic interactions between the cationic
quaternary ammonium groups of PDI and the negative charged
surface of M. thermoacetica. By contrast, the endothermic
binding between PFP and M. thermoacetica was mainly
attributed to PFP inserting into bacterial membrane through
hydrophobic interactions followed by electrostatic adsorption on
the bacteria surface. With the addition of PDI/PFP mixture, ΔHobs
was still positive but obviously smaller than that of PFP, which
suggested the coexistence of the aforementioned interactions.
membrane by hydrophobic interactions. This unique feature
could ensure the efficient electron transfer to bacteria and
circumvent the extra energy consumption when redox shuttles
transmembrane transport. As a result, M. thermoacetica can
harvest photoexcited electrons from the PFP/PDI heterojunction,
which drives the Wood-Ljungdahl pathway to synthesize acetic
2
acid from CO under illumination (Scheme 1b).
To check the successful construction of the p-n
heterojunction layer on the surface of M. thermoacetica,
photocurrent responses of PFP, PDI and PDI/PFP were carried
out. Compared to that of PDI with anodic photocurrent (Figure
1
a) and PFP with cathodic photocurrent (Figure 1b), PDI/PFP
heterojunction exhibited significantly higher anodic photocurrent
Figure 1c), which indicated that p-n heterojunction structure
Furthermore, the binding constant
K
a
of PDI/PFP/M.
(
5
-1
thermoacetica (8.72×10 M ) calculated by the fitting ITC curve
was significantly larger than that of PDI/M. thermoacetica (3.34
was beneficial to hole/electron separation efficiency. This could
also be verified from the appropriate cascade energy level of
PDI and PFP calculated by electrochemical and spectrographic
measurements (Figure S1 and Figure 1d). Both HOMO and
LUMO energy level offset between these two molecules
exceeded 0.3 eV (1.29 eV for △ELUMO and 0.48 eV for △EHOMO),
which can provide enough driving force for hole/electron
dissociation.[23]
5
-1
4
-1
×
10 M ) and PFP/M. thermoacetica (7.73×10 M ), implying
the PDI/PFP mixture possessed stronger bioaffinity towards M.
thermoacetica to form p-n heterojunction layer on the bacteria
surface.
Apart from the ITC measurement, zeta (ζ) potentials were
also measured to confirm the interaction of conjugated
molecules and M. thermoacetica (Figure 2b). Initially,
ζ
To clarify the interaction between PDI and/or PFP and M.
thermoacetica, isothermal titration microcalorimetry (ITC) was
carried out to examine the thermodynamic changes during the
binding process of M. thermoacetica with the conjugated
molecules.[24-25] As shown in Figure 2a, when PDI or/and PFP
was titrated into M. thermoacetica solution, the observed
enthalpy (ΔHobs) curves exhibited obviously different trend with
potentials of separated M. thermoacetica, PDI, PFP, and
PDI/PFP were -38.5 ± 0.7, 31.3 ± 1.2, 21.6 ± 1.5, and 25.2 ± 0.5
mV, respectively. When incubated with PDI, the ζ potential of M.
thermoacetica presented an obvious positive shift to -32.2 ± 0.2
mV, indicating that PDI bounded to the surface of
2
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Figure 1. Representative photocurrent responses of PDI (a), PFP (b), PDI/PFP heterojunction (c) on a carbon paper electrode with
the interval of 10 s, which were recorded at 0 V bias in phosphate buffer (0.1 M, pH=7.4) containing 0.1 M cysteine as the electron
donor. (c) Energy level diagram of PDI and PFP.
Figure 2. (a) The variation of observed enthalpy changes (ΔHobs) against PDI/M. thermoacetica, PFP/M. thermoacetica, PDI/PFP/M.
thermoacetica ratio by titrating PDI, PFP, PDI/PFP, respectively. (b) Zeta potentials of M. thermoacetica, PDI, PFP, PDI/PFP, PDI/M.
thermoacetica, PFP/M. thermoacetica, PDI/PFP/M. thermoacetica, respectively. (c) CLSM images of M. thermoacetica incubated with
PDI, PFP and PDI/PFP (10 μM) for 2 h. To avoid the crossover of PDI and PFP, for PDI, the excitation wavelength was 559 nm and
the fluorescence images were collected the signals from 580-680 nm. For PFP, the excitation wavelength was 405 nm and the
fluorescence images were collected the signals from 425-475 nm.
3
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Figure 3. SEM images of M. thermoacetica (a,e), PFP/M. thermoacetica (b,f) , PDI/M. thermoacetica (c,g), PDI/PFP/M.
thermoacetica (d,h). (e), (f), (g) and (h) were the enlarged images of (a), (b), (c) and (d), respectively.
M. thermoacetica through electrostatic interactions. By contrast,
PFP/M. thermoacetica displayed a slight increase of ζ potentials
to -36.2 ± 0.1 mV, suggesting that the positively charged side
chain in PFP intercalated into bacterial membrane.[26, 27] After
mM) or PFP/M. thermoacetica ( 0.4 mM) under the same
conditions (Figure 4a and Figure S2). The noticeable increase
was attributed to the efficient hole/electron separation and good
affinity of the PDI/PFP mixture towards bacteria surface.
Furthermore, the effect of illumination intensity and conjugated
molecule concentration on the efficiency of solar-to-chemical
conversion was investigated. The low power density could
reduce the photogenerated hole-electron pair while excessive
illumination intensity might result in the complete destruction of
the cell membrane, thus, the optimal light power density was 5.0
PDI/PFP mixture interacted with M. thermoacetica, the
ζ
potential was up-shifted to -32.9 ± 1.1 mV, owing to the co-
existed electrostatic and hydrophobic interactions. To obtain a
more straightforward understanding of the interaction between
the conjugated molecules and M. thermoacetica, confocal laser
scanning microscope (CLSM) imaging and scanning electron
microscopy (SEM) were conducted for M. thermoacetica
incubated with PDI, PFP and PDI/PFP mixture. From CLSM
images as shwon in Figure 2c, it can be observed that PDI and
PFP well localized at the surface of bacteria, accompanying with
green and blue fluorescence, respectively. As expected, M.
thermoacetica incubated with PDI/PFP could simultaneously
present green and blue fluorescence, indicating their co-binding
towards bacteria surface. The same results were also confirmed
by SEM images. As shown in Figure 3, Compared to that of
neat M. thermoacetica, the surface of M. thermoacetica
incubated with PDI, PFP and PDI/PFP mixture turned obviously
rough. In other words, the conjugated molecules could be
uniformly coated on the bacteria surface. Furthermore,
PDI/PFP/M. thermoacetica and PDI/M. thermoacetica or PFP/M.
thermoacetica were also in good shape, suggesting that the
good biocompatibility between the conjugated molecules and
becteria.
-2
mW/cm . Meanwhile, the PDI/PFP concentration was also
critical for the photosynthesis of the biohybrid system. When the
concentration of the PDI/PFP was 10 M, the maximum amount
of the acetic acid produced (Figure S3), which could be
ascribed to excessive holes formed in the bacterial surface
destructing cell membrane. To furthermore study the
photosynthetic behavior, the produced acetic acid amount of
PDI/PFP/M. thermoacetica was monitored in an alternating light-
dark cycle of 12 hours each. Because of the accumulation of
metabolic intermediates, acetic acid was continuously produced
during the day-night cycles, which was also confirmed by
previous studies.[7,8] At the third day, the accumulation amount of
the acetic acid was 0.63 mM. Eventually, the quantum yield of
1.6 % was calculated based on the initial Cys concentration (the
details in supporting information), which was comparable to the
year-long averages determined for plants and algae as well as
the inorganic biohybrid system ranging from ~0.2 to 2.8 %.[
Noticeably, during the photosynthesis, the cell number of M.
thermoacetica in the presence of PDI/PFP increased to ~ 300 %
after 3 days while that of M. thermoacetica in the control group
did not (Figure S4). This result suggested that PDI/PFP could
promote the growth of bacteria and exhibit good biocompatibility.
To clarify the mechanism of photoexcited electron transfer,
cyclic voltammetry (CV) was performed for M. thermoacetica
incubated with PDI/PFP (Figure 4d). The separated M.
thermoacetica has a couple of redox peaks at -0.2 V and a
reduction peak at -0.5 V, which might be attributed to the redox
3,6-8,28]
We investigated the photosynthetic ability of the biohybrid
system, in which, the product acetic acid was monitored by
quantitative proton nuclear magnetic resonance (H-NMR). To
study the photosynthetic behavior, the biohybrid system was
performed in the illumination of light-dark cycle of 12 hours each
to imitate the intermittent nature of the solar source. Figure 4a-
4
c shows that in the two deletional controls, namely M.
thermoacetica in the light and conjugated molecules/M.
thermoacetica in the dark, the concentration of the acetic acid
was only  0.1 mM, which might be the accumulation under the
initial autotrophic acclimation. Under light illumination,
conjugated molecules/M. thermoacetica could exhibit apparent
production of the acetic acid. As expected, the accumulated
acetic acid yield of PDI/PFP/M. thermoacetica ( 0.63 mM) was
significantly higher than that of PDI/M. thermoacetica ( 0.25
mediators rubredoxins (Rd) and flavoproteins (Fp) distributed on
the bacterial membrane.[
29,30]
Upon incubation with the PDI/PFP,
redox peaks of PDI/PFP and M. thermoacetica appeared
simultaneously in the PDI/PFP/M. thermoacetica biohybrid
system, suggesting the good combination between conjugated
4
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Figure 4. (a) Photosynthetic production of acetic acid by conjugated molecules/M. thermoacetica under light and deletional controls.
b) The optimal experiment of the light intensity when M. thermoacetica incubated with 10 M PDI/PFP. (c) The produced acetic acid
(
amount of PDI/PFP/M. thermoacetica in an alternating light-dark cycle of 12 hours each. (d) CVs of the M. thermoacetica, PDI/PFP,
and PDI/PFP/M. thermoacetica in 10 mM phosphate buffered saline (PBS) solution (pH=7.4). (e) Energy level diagram of PDI/PFP
and the representation of electron transfer mechanism to bacterial membrane.
molecules and bacteria. Furthermore, the reduction
potentials of the PDI/PFP were higher than that of the redox
mediators Rd and Fp (Figure 4e), ensuring the efficient direct
photoexcited-electron transfer from the PDI/PFP heterojunction
to membrane proteins.
In summary, we have pioneered -conjugated organic
semiconductor as the photosensitizer to develop non-
photosynthetic bacteria−based photosynthetic biohybrid system
for CO reduction. The p-n heterojunction (PFP/PDI) exhibited
efficient hole/electron separation efficiency and strong light-
harvesting ability, as well as good biocompatibility and bioaffinity
a
2
5
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with the bacteria. Interestingly, it was found that the positively
charged side chains of organic semiconductor PFP could
intercalate into bacteria membrane, which is beneficial to the
direct transfer of photoexcited electron from PDI/PFP to M.
thermoacetica. As a result, the electron passed on the Wood-
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Ljungdahl pathway to synthesize the acetic acid from CO
2
. This
work is paving a way to explore bioenergy application of organic
[
[
[
[
[
[
semiconductors,
biomanufacturing
semiconductor−bacteria
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solar-to-chemical conversion • CO reduction
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6
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Angewandte Chemie International Edition
10.1002/anie.202001047
COMMUNICATION
In this work, we
Panpan Gai, Wen Yu, Hao
Zhao, Ruilian Qi, Feng Li,
Libing Liu, Fengting Lv, and
Shu Wang
developed an organic
semiconductor-bacteria
biohybrid photosynthetic
system, which could
efficiently realize CO
reduction to produce
2
Page No. – Page No.
Solar−Powered Organic
Semiconductor−Bacteria
acetic acid through non-
photosynthetic bacteria
Moorella thermoacetica.
This work opens a new
avenue to explore
2
Biohybrids for CO Reduction
into Acetic Acid
bioenergy application of
organic semiconductors,
and also provides a
conven-ient
biomanufacturing
approach to design
organic semiconductor-
bacteria biohybrids for
efficient solar-to-
chemical conversion.
7
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