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REVIEW
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Carbon dioxide conversion to synthetic fuels using
biocatalytic electrodes
Cite this: DOI: 10.1039/c6ta07571a
Stefanie Schlager,*a Anita Fuchsbauer,b Marianne Haberbauer,c Helmut Neugebauera
and Niyazi Serdar Sariciftci*a
Carbon dioxide has evolved from being considered as a greenhouse gas to a valuable carbon feedstock for
the generation of artificial fuels and valuable chemicals. In this work, we review the biocatalytic approaches
towards CO2 conversion into chemicals and fuels. We display the opportunities and challenges of using
biocatalysts. Our work especially focuses on bio-electrocatalytic systems. These electrochemical
applications of biocatalysts gain increasing interest, as electrochemical redox processes can avoid
Received 1st September 2016
Accepted 2nd December 2016
expensive mediators and co-factors. This is also a pathway for renewable energy storage because wind
or solar energy can possibly be applied as electrical sources for the electrochemical CO2 conversion
DOI: 10.1039/c6ta07571a
www.rsc.org/MaterialsA
systems. Biocatalytic CO2 conversion together with renewable energy storage represents a viable and
sustainable route for the generation of chemicals and fuels.
1. Introduction
In recent years carbon dioxide has been regarded as the major
greenhouse gas, partly responsible for the global climate
change since greenhouse gas emissions are increasing and
fossil fuels are depleting increasingly.1,2 As a result of burning
hydrocarbons, carbon dioxide is released to the atmosphere to
an ever increasing extent. Although it is reported that methane
and water vapor contribute even more to atmospheric greenhouse gases, CO2 has a much higher impact on global warming
due to a much longer residence time in the atmosphere.3,4 This
duration is still just estimated for CO2 but it is at least 3 times
higher in comparison to that of methane and 7 times higher
than that of water vapor. In terms of its concentration in the
atmosphere, CO2 is the second most abundant greenhouse gas
next to water vapor.
This linear transformation of the fossil fuel bound carbon
into atmospheric carbon dioxide is to be changed to a cyclic use
of carbon dioxide. This would bring the necessity of capturing
and recycling of CO2. With this strategy of cyclic use, carbon
dioxide can be regarded as carbon feedstock for future generation of fuels and chemicals. CO2 neutral and renewable fuel
generation and use can bring our atmosphere to a sustainable
and stabilized equilibrium.
In contrast to the techniques of Carbon Capture and
Sequestration (CCS), where CO2 is stored in cavities under sea
and land, Carbon Capture and Utilization (CCU) uses carbon
a
Linz Institute for Organic Solar Cells (LIOS), Johannes Kepler University Linz,
Altenbergerstraße 69, 4040 Linz, Austria. E-mail: [email protected]
b
c
PROFACTOR, GmbH, Steyr, Austria
dioxide as a valuable carbon source for a variety of chemicals,
materials and fuels.5–8
Nevertheless, for products generated from CO2 as a carbon
source, it is required to chemically reduce carbon dioxide e.g. to
carbon monoxide or to hydrocarbons. Since the carbon dioxide
molecule is a very stable and low energy conguration of
carbon, such reduction reactions need a lot of energy input
(1st and 2nd law of thermodynamics) as well as cleverly designed
catalysts to overcome the energy barriers in such reactions.
Besides numerous studies on chemical and electrochemical
techniques using synthetic routes and synthetic catalysts, we
here focus on the biochemical and bio-electrochemical routes
toward CO2 conversion and biofuel generation.9 In these biocatalytic approaches we use natural processes as a model for the
choice of catalysts and process design.
Biocatalytic as well as bio-electrocatalytic approaches have
several advantages in comparison to routes using synthetic
catalysts. From the comparison of synthetic catalysts with biocatalysts it is obvious that the source or the synthetic pathway of
the catalyst plays an important role. While catalysts, such as
organic molecules or metal–organic complexes, have to be
synthesized prior to their use and therefore oen require elaborate steps and materials, biocatalysts can be obtained directly
from natural sources and can be provided in high amounts.
However, probably the most noteworthy properties of biocatalysts, like microorganisms or enzymes, are high selectivity
and yield with regard to the desired product. Moreover such
processes can be tuned to various possible products by choosing
the biocatalysts accordingly. Another advantageous property
to mention is that reactions can be performed under rather
mild reaction conditions (atmospheric pressure and ambient
temperature). Bio-electrocatalytic applications furthermore offer
Acib, GmbH, Linz, Austria
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Journal of Materials Chemistry A
the possibility of direct electron injection into the biocatalysts
where no mediators or electron equivalents are required. In
addition such techniques represent a highly attractive pathway
for chemical storage for renewable energies, because they can
serve as an electrical energy source.
In the following section different biocatalytic approaches for
CO2 conversion are discussed. In general we distinguish
between living biocatalytic systems such as microorganisms
and non-living biocatalysts such as enzymes. Furthermore we
comparatively present studies on biocatalytic as well as bioelectrocatalytic processes.10
2. Microorganisms as biocatalysts for
CO2 conversion
2.1
Conversion using reduction equivalents
Microorganisms particularly gained interest in carbon capture
and utilization research due to the ability to convert CO2 to
a broad range of possible valuable products and fuels. Application of such microorganisms has become highly attractive as
several different strains of pure as well as mixed cultures of
microorganisms are suitable for application in biofuel and
biochemical generation.11 Utilization of anaerobic bacteria has
since become attractive, as they provide suitable conditions for
biotechnological processes and biofuel production. Several
studies showed that such microorganisms can be favorable for
chemical and biofuel generation from fermentation. Particularly the generation of acetate or ethanol has been a main
focus.12 Those products are obtained due to the metabolism of
anaerobic bacteria as hydrocarbons serve as nutrients.
However, also the viability to grow acetogens using H2 and CO2
or CO instead of glucose was shown. Acetate formation was also
displayed for different growing conditions. Moreover various
models for the role of enzymes and possible metabolism pathways for acetogenesis have been proposed.13
Besides high selectivity towards a certain product, microorganisms are also favorable in terms of representing a selfregenerating catalyst, long-term stability, sustainability and
biocompatibility. In addition, sources of the microorganisms
are diverse and highly abundant.14 By tuning the kind of
microorganisms and/or environmental conditions such as
temperature and pressure, the metabolism of the biocatalysts
can be directed toward one or even several desired products.15
This direct conversion of CO2 using microorganisms opens
a favorable way for the generation of biofuels and biochemicals
in terms of ethical issues as well. In contrast to biofuels from
crop or other biomass which may compete with food production, CO2 can be converted directly using microorganisms and
serves as the only carbon source. This microorganism-catalyzedmethod is therefore not competing with food supply since
biofuels and biochemicals can be obtained from a non-food
source. However, for achieving high yield and high selectivity
using this approach, it is required to understand the corresponding enzymology and mechanism of the metabolism.16,17
To compete with fossil fuels, biofuels need to have high
energy density. Therefore, the main interest is on liquid target
J. Mater. Chem. A
Review
materials for the direct generation of e.g. higher alcohols such
as ethanol or butanol. Liou et al. demonstrated the generation
of e.g. acetate, ethanol and even butanol from CO, CO2 and
sugars as a growth support and carbon sources for an anaerobic
Clostridium strain. Those strains were chosen because the
Wood–Ljungdahl pathway for Clostridia serves as a model route.
This path gained main interest as it consists of multiple redox
steps, each catalyzed by a corresponding enzyme, and therefore
provides generation of various possible products.18,19
Detailed investigation of the Wood–Ljungdahl pathway as
a result led the focus toward application of archaea or bacteria
such as Clostridia.20 Younesi et al. focused their research on the
generation of acetate and ethanol as fuels from Clostridium
ljungdahlii. In their study they investigated the bioconversion of
syngas containing CO, CO2 and H2. Besides the inuence of
pressure they also studied growth inhibition and ethanol yield
upon CO content. They found acetate as the major product and
in general enhanced production rates of both, ethanol and
acetate, when the pressure was increased to 1.8 atm.21
Also the groups of Ragsdale and Tracy furthermore presented studies based on investigations of the Wood–Ljungdahl
pathway. In contrast to the group of Younesi, who investigated
syngas conversion by acetogens, Ragsdale et al. examined
CO2 xation or conversion and the corresponding enzymology.22,23 A detailed study on the conversion of CO2 and other
substrates for biofuel generation and biorenery application
was carried out by the group of Tracy. From investigations of
the enzymatic mechanism in microorganisms' metabolism
according to the Wood–Ljungdahl pathway, dependence of the
desired products on the source of substrate (e.g. CO2, cellulose,
glycerol) was observed (Fig. 1).24 Schiel-Bengelsdorf and Dürre
moreover presented a review of several acetogens following the
Wood–Ljungdahl pathway for the generation of acetate and
advanced products like ethanol and butanol (Fig. 2).25
Results on the potential of these microorganisms toward
CO2 xation and conversion gave rise to intensive research
toward syngas conversion with CO2 as the carbon source for
biochemicals and biofuels. Munasinghe et al. moreover
reviewed studies on syngas fermentation to biofuels using
Clostridia and acetogenic microorganisms.26
In another study the potential of microbial processes toward
syngas conversion, in comparison to the conversion of sugar,
toward different products using Moorella thermoacetica was
displayed by the group of Hu et al. They found productivity rates
at 0.585 g L 1 h for acetate only, which is in contrast to acetogenic Clostridium ljungdahlii, as presented e.g. by the groups of
Younesi, who also found ethanol as a second product.21,27
Particularly reaction conditions play an important role in
microbial processes for the synthesis of biofuels like ethanol or
higher alcohols like propanol and butanol. Besides parameters
like temperature, pH and pressure the constitution of buffer or
medium solution has an enormous impact on not only the
performance of syngas but also process costs.28,29
All these approaches showed the broad variety of possible
biofuel and biochemical generation from syngas or other
substrates to be converted. Above all, however, especially
biosynthesis using gaseous CO2 directly as a carbon source
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Wood–Ljungdahl pathway for the conversion of different carbon based substrates showing the individual steps with the corresponding
enzymes. Figure reproduced with permission from ref. 24.
Fig. 1
gained high interest in this eld. In general the strategy is to
nd a combination of generating biofuels and biochemicals,
reducing net carbon dioxide emission and nding a carbonneutral, renewable system solution.30–32
For such a direct conversion of CO2 Deppenmeier et al.
published a detailed study on using methanogenic microorganisms. In their paper they show the stepwise mechanisms of
the metabolism with the corresponding enzymes for the
conversion of CO2 together with H2 to methane, CH4. They
especially focused on microorganism strains belonging to
This journal is © The Royal Society of Chemistry 2017
Methanosarcina for investigating redox processes with electron
and hydrogen transfers involved. They propose that the process
of methane formation is due to proton and ion gradients in the
microorganisms that are generated from participating enzymes
and proteins over the membrane.33
Carbon xation pathways in general can be divided into six
different possibilities. The rst approach is the pathway via the
Calvin cycle or reductive pentose phosphate pathway from
photosynthesis and is normally used by algae, plants and cyanobacteria. In this cycle CO2 is xed through carboxylation of
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Possible acetogenic microorganisms with their optimum growth conditions and obtained products. Figure reproduced from SchielBengelsdorf et al.25
Fig. 2
D-ribulose-1,5-diphosphate
and subsequent conversion into two
molecules of 3-D-phosphoglycerate.
Alternatively there are ve possible autotrophic pathways
where carbon xation is performed due to incorporation of CO2
into a carbon backbone and using acetyl-CoA and/or succinylCoA cycles for carbon xation. A detailed description of the
possible CO2 xation pathways has been presented by Ducat
and Silver.34 However, these strategies provide information
J. Mater. Chem. A
about molecules obtained via carboxylation reactions. A direct
conversion of CO2 to acetate, ethanol or other fuels is only obtained from the Wood–Ljungdahl route as displayed in Fig. 1.
The Wood–Ljungdahl pathway for microorganisms, in
particular for Clostridia, exhibits their favorable properties, as it
is possible to obtain several products. Besides higher alcohols
like butanol, requiring a multi-step cascade of corresponding
enzymes, also shorter pathways are possible. From products
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like acetate moreover methane generation can be obtained.
Depending on the strain, products can be chosen from a huge
variety. In addition, considering reaction conditions, these
products can be obtained at high yields and selectivities,
making microorganisms notably attractive.
Among the 83 species of methanogens described so far
(including six synonymous species) 61 species (including ve
synonymous species) are capable of oxidizing H2 and reducing
CO2 to form methane. Examples of hydrogenotrophs are
Methanosarcina barkeri, Methanosarcina thermophila, Methanococcus thermolithotrophicus, Methanocaldococcus jannaschii,
Methanospirillum hungatei, Methanobacterium palustre, Methanobacterium formicicum or Methanothermus fervidus.35 To
obtain high selectivity and yield there have been also
approaches in genetic modication and synthetic biology.
These studies aim at designing systems that meet the requirements of high quality biofuels that are further generated from
sustainable sources and approaching a carbon neutral pathway
at the same time.36–38
Further there have also been industrial applications and
pilot processes that already implemented such technologies for
carbon dioxide conversion using e.g. syngas fermentation
processes or steel ue gas and microorganisms as catalysts.39–41
However, all of these approaches require hydrogen as
a reduction equivalent and/or supporting mediators for charge
and proton transport for the conversion of gaseous CO2.42
Hydrogen as well as mediators have to be produced previously e.g.
in case of H2 from water splitting which causes a further costintensive step in addition to the actual CO2 conversion and biofuel generation. For this reason, focus is increasingly on substitution or even avoidance of such supplements. For this purpose
the technique of microbial electrolysis evolved. Microbial electrolysis uses microorganisms attached to electrodes. This is
possible because some microorganisms can be addressed directly
in electrochemical systems for application in redox reactions and
therefore additional mediators are not required anymore.
Moreover, if renewable energies like solar or wind can be
used for such bio-electrochemical conversion systems, those
processes may also be considered as an opportunity for chemical energy storage.
The time and place of generation of renewable energies are
not aligned with the time and place of demand and consumption. A combination of a microbial system for reducing the
greenhouse gas CO2 together with an electrochemical system,
driven by a renewable energy source, would meet the requirements of both renewable energy storage and sustainable
biosynthesis at once (Fig. 3).43,44
2.2
Journal of Materials Chemistry A
electrosynthesis and by bio-electrocatalytic conversion of CO2.
However, probably the most crucial part for such methods is
charge transfer to and from biocatalysts and to understand the
mechanism of the redox processes.
In living biocatalysts like microorganisms charge transfer
may occur outside the cell via the outer membrane. This is
different from catalysts like the widely used metal–organic
compounds, which also comprise non-living biocatalysts like
enzymes, where charge transfer occurs via conjugated bonds
and metal ions.
Electrochemical reduction reactions in microorganisms are
reported to be possible in the so-called exoelectrogenic strains,
capable of transferring charges over the cell membrane. These
transfers usually happen via extracellular electron transport by
two possible mechanisms: direct electron transfer and mediated electron transfer.47–49
Rosenbaum et al. screened the different possibilities for
such extracellular electron transfer mechanisms in the case of
biocathodic microorganisms. For the direct electron transfer,
electron-shuttling via cytochromes (proteins that enable redox
reactions) on the outer membrane of the cell is proposed.50 The
involved c-type cytochrome electron transfer chains can further
be assisted by hydrogenases (cytochrome-hydrogenase partnership).51 Direct electron transfer furthermore can be performed with other enzymes, similar to a c-type cytochrome in
different biochemical processes (Fig. 4).52,53
In the case of mediated electron transfer mediators can act
endogenously (in the cell) or exogenously (outside the cell).
Electron mediators such as neutral red and methylviologen are
widely used for microorganisms as well as for non-living biocatalysts such as dehydrogenase enzymes.54–57
In a different investigation in terms of charge transfer in
microorganisms, the group of Ajo-Franklin examined the
Microbial electrosynthesis
Application of microorganisms in electrochemical cells was
found to be a favorable step toward substitution of mediators
and additives. Production, supply and regeneration of mediators and other additives pose the problem of high costs
and energy inputs. This is due to steps and processes that
are necessary in addition to the actual CO2 conversion.45,46
Many of those extra steps can be avoided using microbial
This journal is © The Royal Society of Chemistry 2017
Fig. 3 Correlation of time and space according to utilization and
transport for renewable energies.
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electron transfer between living and non-living organisms.
From an understanding of such electrical conduction in living
organisms they could generate a synthetic electron conduit and
therefore tune the property of a certain strain according to their
redox capabilities.58 Further they tried to apply nanostructures
for an even improved charge transport via cell membranes.59
All of these studies give advanced insight into the mechanistic
pathway of redox reactions and charge transfer in biocatalytic
and bio-electrocatalytic systems using microorganisms. This is
Review
crucial for the application for biosynthesis and improvement of
bio-electrocatalytic processes.
The rst report on bioelectrochemically synthesized methane
from CO2 without any electron shuttle or mediators was published by Cheng et al. They showed methane generation from CO2
or carbonate conversion. Besides the generation of hydrogen from
organic matter using exoelectrogenic bacteria, also an evolving
methane concentration due to the presence of carbonate in the
electrolyte solution was displayed. Methane generation actually
was an unwanted side effect. However, they were one of the rst
groups who moreover observed favored methanogenesis when
hydrogen was apparent to a high extent.60,61 In a subsequent study
Cheng and co-workers further found for the rst time that
methane could be generated from electrical current by direct
electron injection into microorganisms grown on a cathode
instead of methane generation from hydrogen gas evolution, as
presented previously. For their electromethanogenic approach
they presented electron capture efficiencies of 96%.62 The potential to use such microbial electrolysis cells for biofuel generation
was further addressed by Rabaey et al. They investigated methane
generation from hydrogenophilic microorganisms and combined
methanogenesis with anaerobic digestion. They used the oxidation of acetate to donate electrons for the reduction reaction.
Together with cathodically generated hydrogen, wastewater was
then converted to methane.63,64 Related to these previous studies
Villano et al. proposed in their paper a combined process for the
bioelectrochemical reduction of CO2 to methane in a bioelectrochemical system (BES) applying a methanogenic culture.
Besides indirect reduction via abiotically generated H2 they also
found direct reduction to methane due to extracellular electron
transfer. At potentials more negative than 650 mV vs. SHE
abiotic generation of hydrogen was observed. In addition to CO2
ushing, bicarbonate (NaHCO3) was present in solution as the
buffer salt. Both sources of CO2 (as gas and as a bicarbonate salt)
served as the carbon source to be reduced to methane by
providing electrons directly from an electrode. In another study
they further combined cathodic methane generation with
a microbial anode to oxidize acetate to provide electrons.65,66
A similar approach to cathodically convert CO2 to methane
was presented by Jiang et al. In contrast to Villano et al. they also
Fig. 4 Proposed electron transfer mechanisms in microorganisms via
(A) direct electron transfer involving c-cytochrome, (B) mediated
electron transfer to a periplasmic hydrogenase or (C) direct electron
transfer
due
to
cytochrome-hydrogenase
partnerships.
Figure reproduced with permission from ref. 50.
J. Mater. Chem. A
Two compartment microbial electrolysis cell used by Zhen
et al. for the electromethanogenesis with a biocathode. Figure reproduced with permission from ref. 70.
Fig. 5
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observed acetate formation using potentials of 850 mV vs.
Ag/AgCl (corresponds to 620 mV vs. SHE) and even more
negative potentials. They found that acetate production
increased when the potential was set to more negative values.
Also, besides acetate, methane generation increased subsequently
in comparison to more positive potentials. The coulombic efficiency of methane as the product increased to 95.8% at a set
potential of 950 mV, whereas it decreased again to 56.7% at
a more negative potential of 1150 mV. The coulombic efficiencies
of acetate as the product uctuated in a range of 0–28.4% for set
potentials between 950 mV and 1050 mV.67
Also Jourdin et al. observed production of acetic acid in
anaerobic microbial electrosynthesis operated at 850 mV vs.
SHE with bicarbonate as the carbon source. Differently, this
group used microorganisms from planktonic cells. They found
three predominant species of microorganisms in the biolm on
their electrode. Acetoanaerobium from the order Clostridiales is
known for the ability to convert CO2 to acetate and was mainly
dominant in the biolm. Besides, Hydrogenophaga from the
second apparent order, Burkholderiales, was dominant in
suspension as well as in the biolm and was also expected to
contribute to acetate formation. For microbial synthesis they
conrmed from comparison experiments that 100% of the
electrons consumed were used for acetate.68
Zhen et al. recently published a study on a two compartment
microbial electrolysis cell focusing on the bioelectrosynthesis of
methane. They showed results on the application of different
potentials and the corresponding change in hydrogen and
methane generation. For a constant potential of 900 mV vs.
Ag/AgCl (corresponds to 670 mV vs. SHE) applied they observed
the highest methane production and moderate hydrogen generation. For a potential as low as 600 mV vs. Ag/AgCl (corresponds
to 370 mV vs. SHE), only methane generation was observed,
although to a low extent. However, there was no hydrogen
evolution observed, since a higher overpotential was expected to
be required.69 Furthermore, they displayed the generation of
methane in a MEC at a constant cathodic potential of 900 mV to
Biocathode consisting of carbon felt. Microorganisms (white
algae-like coverage) were grown on the carbon felt electrode for
direct electron injection.
Fig. 6
This journal is © The Royal Society of Chemistry 2017
Journal of Materials Chemistry A
1400 mV vs. Ag/AgCl ( 670 mV to 1170 mV vs. SHE) using
graphite felt cathodes (Fig. 5).70
Another point in the application of microorganisms in
electrochemical cells is the viability of regeneration and therefore the possibility of long-term performance. A long-term
performance of 188 days of a microbial electrolysis cell was
presented by the group of Van Eerten-Jansen, who investigated
methane generation at potentiostatic conditions between 550
mV and 800 mV vs. NHE. As a carbon or CO2 source they
added bicarbonate as well.71
Recent studies on microbial electrosynthesis have also been
presented by Bajracharya et al. who used pure as well as mixed
cultures for CO2 reduction. In their investigations they applied
an assembly of graphite felt and stainless steel as the cathode.72
In our work, we used a direct approach for CO2 reduction
with an even lower potential of 700 mV vs. Ag/AgCl ( 470 mV
vs. SHE). Methanogenic microorganisms were grown on
a carbon felt electrode to provide electrons directly (Fig. 6).
In contrast to the previously mentioned studies, we did not use
bicarbonate in the electrolyte solution. Instead of this we purged
the cell with gaseous CO2 as the carbon source only. Further we
long-term operated the microbial electrolysis cell for over one year
(Fig. 7). We established a stable system that was even suitable for
a continuous and constant conversion of CO2 to methane. During
potentiostatic electrolysis we also found hydrogen generation as
was observed earlier by the group of Zhen.70 From the comparison
with blank measurements with a carbon felt electrode only, we
found that hydrogen evolution was only there with the microorganisms. In total, a faradaic efficiency of 22% could be determined for the long-term performance cell.73
Tuning the operation conditions as well as the microorganism
strains has shown that microbial electrolysis is highly suitable for
generation of biofuels and biochemicals.74 A summary of the
discussed approaches is presented in Table 1. High selectivities
and yields are unique advantages of biocatalysts and highlight
Fig. 7 Continuous production of H2 and CH4 during the long-term
performance of a microbial electrolysis cell with gaseous CO2 as the
carbon source only. The amounts of H2 and CH4 in the headspace of
the cell produced during potentiostatic performance were detected
using gas chromatography. The results show constant production
volumes.73
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Journal of Materials Chemistry A
Table 1
Summary of different microbial electrosynthesis approaches with corresponding parameters
Microbial electrosynthesis
Mixed culture
Mixed culture
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Substrate for
conversion
Product
Electrode material
Cathodic potential
Reference
Glucose,
cellulose
CO2
H2, methane,
acetate
Methane
Carbon cloth with
Pt catalyst
Carbon cloth
0.3–0.8 V vs. SHE
Cheng et al.60
Cheng et al.62
CO2, NaHCO3
H2, methane
Carbon paper
0.7–1.2 V vs. Ag/AgCl
(0.499–0.999 V vs. SHE)
0.65–0.9 V vs. SHE
Villano et al.65
Hydrogenophilic
methanogenic culture
Hydrogenophilic
methanogenic culture
Mixed culture
NaHCO3
H2, methane
Graphite
0.85 V vs. SHE
Villano et al.66
CO2, NaHCO3
Carbon felt
CO2
Mixed culture
CO2, NaHCO3
Methane
Flexible multiwalled
carbon nanotubes on
reticulated vitreous carbon
(NanoWeb-RVC) for
Carbon stick
0.85–1.15 V vs. Ag/AgCl
(0.653–0.953 V vs. SHE)
0.85 vs. SHE
Jiang et al.67
Planktonic cells
H2, methane,
acetate
Acetate
Mixed culture
CO2
Methane
Carbon stick/graphite felt
Mixed culture
Clostridium ljungdahlii
NaHCO3
NaHCO3
Methane
Acetate, H2
Graphite felt
Graphite felt/stainless steel
Mixed culture
NaHCO3
Graphite felt/stainless steel
Sporomusa ovata
CO2, NaHCO3
Clostridium ljungdahlii
CO2
Moorella thermoacetica
CO2
H2, methane,
acetate
Acetate,
oxybutyrate
Acetate,
oxybutyrate,
formate
Acetate
Sporomusa ovata
CO2
Acetate
Brewery wastewater sludge
CO2, NaHCO3
Adapted mixed acetogens
from brewery wastewater
sludge
Mixed culture domestic
wastewater treatment
plant sludge
Enriched culture from
bog sediment
Mixed culture
CO2, NaHCO3
H2, methane,
acetate
Acetate, H2
CO2
Acetate, H2
Carbon felt
0.9–1.1 V vs. Ag/AgCl
(0.69–0.89 V vs. SHE)
Bajracharya et al.72
CO2, NaHCO3
Acetate
Carbon ber rod
Bajracharya et al.72
CO2
Methane, H2
Carbon felt
0.6 V vs. Ag/AgCl
(0.39 V vs. SHE)
0.7 vs. Ag/AgCl
(0.49 V vs. SHE)
Unpolished graphite stick
Graphite stick
Graphite stick
Ni-nanowire coated
graphite stick
Graphite granules and
graphite rods
Graphite granules and
graphite rods
their attractiveness. As a result, not only mimicking of natural
process but even direct application of biological materials such
as biocatalysts gains a lot of interest in terms of renewable
energies and CO2 reduction. Microorganisms offer high potential
according to this purpose. However, considering the metabolic
pathway of microorganisms, as discussed previously in this
section, the reaction pathway of microorganisms consists of
several, individual steps. Those steps are each catalyzed by
a corresponding enzyme. The separate application of such single biocatalysts therefore additionally became attractive as
certain reactions toward distinct products can be extracted from
the multi-step pathway. This eases CO2 reduction reactions
and makes it even more favorable as enzymes are not living
J. Mater. Chem. A
0.6–1 V vs. Ag/AgCl
(0.399 V vs. SHE)
0.9–1.4 V vs. Ag/AgCl
(0.699–1.199 V vs. SHE)
0.7 V vs. NHE
0.6–0.9 V vs. Ag/AgCl
(0.395–0.695 V vs. SHE)
0.6–1.1 V vs. Ag/AgCl
(0.395–0.895 V vs. SHE)
0.6 V vs. Ag/AgCl
(0.39 V vs. SHE)
0.6 V vs. Ag/AgCl
(0.39 V vs. SHE)
0.6 V vs. Ag/AgCl
(0.39 V vs. SHE)
0.6 V vs. Ag/AgCl
(0.39 V vs. SHE)
0.79 V vs. Ag/AgCl
(0.58 V vs. SHE)
0.79 V vs. Ag/AgCl
(0.58 V vs. SHE)
Jourdin et al.68
Zhen et al.69
Zhen et al.70
Van Eerten-Jansen et al.71
Bajracharya et al.72
Bajracharya et al.72
Bajracharya et al.72
Bajracharya et al.72
Bajracharya et al.72
Bajracharya et al.72
Bajracharya et al.72
Bajracharya et al.72
Schlager et al.73
biocatalysts but are able to operate at comparable yields and
selectivities as living biocatalysts or microorganisms. In the
following sections application of enzymes for the conversion of
CO2 toward chemicals and biofuels will be discussed.
3. Enzymes as biocatalysts for CO2
conversion
In the elds of renewable energies and CO2 conversion particular focus has been on the use of dehydrogenase enzymes as
they are especially known for the ability to convert CO2 to
carbon monoxide75,76 or hydrocarbons like formate, formaldehyde or methanol.77–81 Such dehydrogenases further occur in
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Journal of Materials Chemistry A
human liver where they perform in the opposite direction or
oxidation to break down e.g. alcohols.82
Redox reactions catalyzed by dehydrogenases usually
proceed under ambient conditions and high yields and are
accompanied by the corresponding redox reactions of electron
and proton shuttles such as the co-enzyme Nicotinamide
adenine dinucleotide (NADH).83
Besides the application of dehydrogenase enzymes for the
chemical reduction of CO2, other enzymes such as carbonic
anhydrase are also capable of CO2 conversion. Carbonic anhydrase e.g. catalyzes the conversion of CO2 to bicarbonate in
a hydrogenation reaction. Such reactions can also be combined
with dehydrogenase processes to activate, enhance and accelerate CO2 reduction. Such improvements have been presented
among others, e.g. by the group of Addo. They report on
enhanced methanol generation from CO2 using dehydrogenase
enzymes as the CO2 is converted to bicarbonate prior to the
reduction reactions with carbonic anhydrase as the catalyst.57
Such improved mechanisms for electrofuel production from
CO2 using carbonic anhydrase has also been described in detail
by Hawkins et al.46 Other carboxylation reactions are e.g. the
xation of CO2 as carboxyphosphate catalyzed by biotin
carboxylase or the temporary xation by converting phosphoenolpyruvate to oxalacetate by phosphoenolpyruvate carboxylase. Similarly the enzyme ribulose-1,6-bisphosphatecarboxylase/oxygenase (RuBisCo) also catalyzes CO2 xation.84
This carboxylation step of ribulose-1,5-biphosphate is the initial
step responsible for the ability of plants or algae to take up
CO2.85 Another carboxylation, the one of 2-oxoglutarate to isocitrate, is catalyzed by isocitrate dehydrogenase.86 In general
conversion to bicarbonate is ubiquitous and essential particularly in cells and reduction processes using living biocatalysts
reported earlier in this review.87 However, the direct reduction
of CO2 to fuels or valuable chemicals without any carbonation
required prior to this, could be even more attractive as it spares
an additional step. Such a direct conversion can be obtained by
using the dehydrogenase enzymes carbon monoxide dehydrogenase, formate dehydrogenase, formaldehyde dehydrogenase
and alcohol dehydrogenase. Carbon monoxide dehydrogenase
(CODH) catalyzes the reduction of CO2 to CO. As a co-factor
ferredoxin is used for providing electrons.80,88,89 However, using
the enzymes formate-, formaldehyde- and alcohol dehydrogenase all together in a cascade is even more attractive, as methanol can be obtained and used directly as a fuel.
The main advantage of utilizing isolated enzymes instead of
directly using the microorganisms for certain reactions is the
even higher selectivity. In comparison to living organisms,
enzymes are restricted to mainly one product, independently
from reaction conditions. A change in e.g. pH or temperature
inuences mainly the performance and yield, but not the
product itself.90 Furthermore handling and maintenance are
more favorable in comparison to living biocatalysts as enzymes
don't have to be kept alive by nourishing regularly.
A well-known and common application of dehydrogenases,
mainly formate dehydrogenase, is for catalyzing the oxidation
of formate to CO2. Released electrons and protons further can
be used for the regeneration of NADH to NAD+. This is crucial
since many synthetic processes use NAD+ as electron and
proton shuttle or reduction equivalent. Studies on regeneration of NADH or NAD+ respectively have been done e.g. by the
group of Palmore and Whitesides. Whitesides et al. showed
the application of formate dehydrogenase in the regeneration
of NADH from its use in other synthetic routes. Palmore et al.
later merged a dehydrogenase catalyzed redox process with
benzylviologen catalyzed NAD+ regeneration in a methanol/
dioxygen fuel cell. In their process methanol was oxidized to
CO2 with the aid of NAD+. The generated NADH was then
regenerated to NAD+ by using benzylviologen as an electron
provider.91,92 Also Neuhauser et al. investigated the regeneration of NADH by the conversion of formate to CO2 using
formate dehydrogenase.93
However, besides the application of dehydrogenase enzymes
for NADH regeneration, primarily interest evolved in the
opposite reaction pathway, namely reduction reactions. Intensive research has therefore especially been on investigations of
biofuel generation and CO2 conversion. In the reductive
pathway using dehydrogenase enzymes for the reduction of
carbon dioxide, NADH serves as the oxidation equivalent or
electron and proton donor. Application of not only such bioinspired but even natural derivatives has become an evolving
topic in terms of CO2 reduction and biosynthesis.87
Fig. 8 Three step reaction cascade for the reduction of CO2 to
methanol using dehydrogenase enzymes and NADH as the electron
and proton donor.
Fig. 9 Schematic representation of Lu et al. for the co-immobilization
of enzymes in different substrates. Figure reproduced with permission
from ref. 104.
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Fig. 10 Alginate–silicate based beads containing the three dehydrogenases FateDH, FaldDH and ADH for the reduction of CO2 to methanol
with NADH as electron and proton donors. Figure reproduced with
permission from ref. 105.
3.1
Reduction reactions with the aid of co-factors
Considering CO2 reduction with the aid of dehydrogenase
enzymes as biocatalysts, mainly the enzymes formate dehydrogenase, formaldehyde dehydrogenase and alcohol dehydrogenase are reported as they are especially known for the conversion
of CO2 via the three step reduction reaction to methanol with
the intermediate products formate and formaldehyde. In this
reaction cascade, each step is catalyzed by the corresponding
enzyme. As a rst step formate dehydrogenase (FateDH) catalyzes
the conversion to formic acid or formate. This is followed by
reducing formate to formaldehyde by means of formaldehyde
dehydrogenase (FaldDH). The last step, the reduction of formaldehyde to methanol occurs with alcohol dehydrogenase (ADH) as
the catalyst responsible. Each of these steps is a two electron
reduction. In natural processes electrons and required protons
are delivered from the oxidation of a sacricial co-enzyme such as
nicotinamide adenine dinucleotide (NADH) (Fig. 8).85,94
Table 2
Related to the origin of the enzyme or microorganism that
the dehydrogenases are isolated from, the kinetics of these
reactions are inuenced to certain extents (eqn (1)). In particular the performance of formate dehydrogenase is highly
dependent on its source and this is crucial as it catalyzes the
initial step of the reduction of CO2. As it has been found e.g. by
Kim and co-workers, formate dehydrogenase obtained from
Candida boidinii requires a concentration of the co-factor NADH
for efficient activity in a certain range. The activity, however, is
inhibited when NADH concentrations were too low or too high.
Moreover, they found that formate generation is kinetically
favored when CO2 is used directly and not as carbonate. Also the
active site of formate dehydrogenase plays a noteworthy role in
the kinetics of such reactions. Formate dehydrogenase from
Pseudomonas oxalaticus or the tungsten containing FateDH from
Syntrophobacter fumaroxidans e.g. are both NADH independent
but were found to be very unstable and inactive in the presence
of oxygen.95 These dependencies on the active site moreover
dene the thermodynamic feasibility of the reduction reactions,
as the required potential or chemical energy respectively for the
reduction is either dened by NADH or other redox species
involved that enable electron transfer.96
Nevertheless, these rather simple reduction reactions using
formate, formaldehyde and alcohol dehydrogenase could be
imitated in several experimental approaches and delivered
promising results.
However, what has been found early from the use of enzymes
was in general their low chemical stability when exposed to air
or kept in inappropriate solvents or pH.97,98 Several studies
therefore are focused on stabilizing the enzymes by e.g. encapsulation for better performance. Furthermore, immobilization
provides the possibility to reuse the biocatalysts as they can be
separated more easily from the reaction solution and products.
First approaches of enzyme immobilization were reported by
Heichal-Segal et al. using alginate-silicate gel matrices for
Summary for co-factor supported enzyme catalyzed CO2 conversion approaches
Enzyme
Co-factor/mediator
Carbonic anhydrase
Biotin carboxylase
Phosphoenolpyruvate carboxylase
Isocitrate dehydrogenase
Product
Reference
HCO3
Carboxyphosphate
Oxalacetate
Isocitrate
Addo et al.,57 Hawkins et al.46
Alissandratos et al.84
Alissandratos et al.84
Alissandratos et al.,84 Sugimura
et al.86
Alissandratos et al.,84 Aresta et al.85
Ribulose-1,6-bisphosphatecarboxylase/oxygenase
Carbon monoxide dehydrogenase
Formate dehydrogenase
Mg
3D-Phosphoglycerat
Ferrocene
NADH
Carbon monoxide
Formate
Formaldehyde dehydrogenase
NADH
Formaldehyde
Alcohol dehydrogenase
NADH
Methanol
J. Mater. Chem. A
Tommasi et al.,88
Ruschig et al.,94 Aresta et al.,85 Kim
et al.,95 Baskaya et al.,96 Obert
et al.,101 Lu et al.,104 Dibenedetto
et al.,105 Luo et al.106
Aresta et al.,85 Baskaya et al.96 Obert
et al.,101 Xu et al.,104 Dibenedetto
et al.,105 Luo et al.106
Aresta et al.,85 Baskaya et al.,96 Obert
et al.,101 Xu et al.,103 Dibenedetto
et al.,105 Luo et al.106
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glucosidase immobilization to prevent it from thermal and
chemical denaturation.99
Later on Aresta et al. investigated enzymes immobilized in
agar as well as polyacrylamide, pumice and zeolite materials
concerning stability and activity of the carboxylase enzyme to be
used for the synthesis of benzoic acid from phenol and CO2.
They found that the immobilized enzymes remained active for
over one week and they could obtain over 90% conversion efficiency of the phenol derivative to benzoic acid within a few
days.100
Among the different immobilization techniques especially
encapsulation of enzymes in gels and gel beads is advantageous. Such gels yield a large surface area, provide high chemical stability for the enzymes and reduce costs due to possible
reusability of the biocatalysts.
Obert and Dave rst presented the immobilization of dehydrogenase enzymes for chemical CO2 reduction in silica sol–gel
matrices. They proved the performance of dehydrogenase
enzymes for the reduction of CO2 to methanol even when
encapsulated in a sol–gel. Moreover an improved yield to up to
90% according to the amount of NADH added was obtained for
methanol generation.101
Also sol–gel materials based on phospholipids were found to
be viable even for the co-immobilization of all three dehydrogenase enzymes for the conversion of CO2 to methanol.102
Furthermore Lu and co-workers investigated the immobilization of dehydrogenases separately and together in beads of an
alginate–silica hybrid gel. They moreover showed the dependence on gel constitution for the chemical CO2 reduction to
methanol and formate and improved performance for the
hybrid gel (Fig. 9). For silica containing sol–gels an even higher
yield was observed. Additionally co-encapsulation of the
enzymes in the gel improved the methanol yield further. Fig. 9
shows the encapsulation of enzymes in different systems,
screened by the group of Lu.103,104
In the work of Dibenedetto et al. NADH regeneration and the
use of new hybrid technologies, by merging biological and
chemical technologies, for the conversion of CO2 to methanol
with the dehydrogenase cascade, co-immobilized in alginate
based beads (Fig. 10), were investigated. They used an alginate–
silicate based sol–gel as well for the immobilization.105
In a recent study polymeric sheets were used and the
co-immobilization of formate, formaldehyde and alcohol
dehydrogenase was presented for the reduction cascade of CO2.
Luo and co-workers showed separate as well as co-immobilization in polymeric membranes with efficient and comparable
yields for methanol generation.106
Table 2 summarizes all discussed co-factor dependent
enzyme catalyzed CO2 conversion approaches. However, in
Fig. 11 Reduction mechanisms of CO2 catalyzed by dehydrogenase
enzymes. 3-Step reduction of CO2 to methanol, direct electron
transfer to the enzyme without any co-factor.
This journal is © The Royal Society of Chemistry 2017
Journal of Materials Chemistry A
most of these enzymatic CO2 reduction approaches, a co-factor
such as NADH was required as the oxidation equivalent and
as electron and proton donors for the reduction reactions.
This is because basically reactions of such processes follow
the Michaelis–Menten equation for enzyme kinetics and are
demonstrated in eqn (1).
[E] + [S] + [NADH] 4 [E + S + NADH]* 4
[E] + [P] + [NAD+]
(1)
In this equation E denotes the enzyme, S the substrate (such
as CO2 and its intermediate reduction products), and P the nal
product.107
As common in enzyme kinetics the use of dehydrogenase
enzymes for CO2 reduction with the aid of NADH can be
described with the formation of an intermediate state. In this
state the substrate and co-enzyme both link to the (metal)
active site of the enzyme. This is crucial for the reduction of
the substrate due to enabled proton and electron transfer via
the active site of the enzyme within the intermediate state.
Nevertheless, in those processes NADH is irreversibly converted to its oxidized form NAD+. In experimental approaches
co-factors therefore are sacricial and need to be regenerated
or steadily supplied to drive reactions repeatedly or even
continuously. This irreversible co-factor oxidation limits
dehydrogenase applications for CO2 reduction to small
scale experiments due to high costs of NADH synthesis and
regeneration.
Depletion of co-factors and related high costs for regeneration, additional process steps and high amounts of required
materials therefore give rise to intensive research for co-factor
substitution. Taking the role of co-factors during redox reactions into account, one has to consider especially the electron
transfer, which is crucial. A primary goal is therefore to nd
a pathway that provides direct electron transfer but does not
require a sacricial co-factor. To address this issue electrochemical approaches draw particular attention.
Proposed electron transfer from an electrode to formate
dehydrogenase during reduction of CO2 to formate, reported by Reda
et al. Figure reproduced with permission from ref. 1 and 111.
Fig. 12
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Preparation procedure for the immobilization of enzymes on a carbon felt electrode. Encapsulation of dehydrogenases in an alginate–
silicate hybrid gel (A). Blank carbon felt electrode (B) that is soaked with the alginate–silicate mixture and precipitated in CaCl2 (C). Alginate
covered carbon felt electrode after precipitation (D).
Fig. 13
3.2
Electro-enzymatic reduction reactions
The implementation of electro-enzymatic processes instead of
NADH as the electron donor is of great interest as this offers the
possibility of direct electron injection into enzymes without
any co-factor or shuttle. Similar to bio-electrochemical applications using microorganisms, electro-enzymatic applications
furthermore open the way toward renewable energy storage and
greenhouse gas conversion into articial fuels at the same time.
Fig. 11 demonstrates the possible reduction route using direct
electron injection from an electrode instead of NADH as the
electron and proton donor.
In the electrochemical process electrons are provided by an
external energy source and the cathode and protons are delivered from aqueous electrolyte solutions. An approach to
address enzymes electrochemically has been presented e.g. by
Minteer and co-workers. They showed direct electron transfer
from enzymes for biofuel cells. In a further study they used
dehydrogenase enzymes in the opposite direction for electron
uptake due to their viability to be electrochemically addressed.
They depicted this technique for the bio-electrocatalytic regeneration of NADH supported by (poly)neutral red.57,108
Amao and Shuto demonstrated the application of viologen
modied FateDH immobilized on an indium-tin oxide electrode
for the reduction of CO2 to formate in an articial photosynthesis approach. Viologen served as the support for the electron
transfer between the electrode and enzyme. This approach
delivered promising results for a bio-electrocatalytic approach
with production rates of up to 7.6 mmol formate/h, when the
length of the viologen-containing carbon chain between electrode and enzyme was increased.109
Further, for the direct reduction of CO2 Kuwabata et al.
presented an electrochemical approach for the conversion to
methanol using dehydrogenase enzymes and methylviologen as
well as pyrroloquinolinequinone as supporting electron mediators. Also in this work the viologen derivative turned out to be
highly favorable as an electron mediator with current efficiencies up to 91%.110
Reda et al. later demonstrated the electrochemical CO2
reduction in a heterogeneously catalyzed approach, using
tungsten containing formate dehydrogenase adsorbed on glassy
J. Mater. Chem. A
carbon without any electron shuttle. This work yielded faradaic
efficiencies of 97% and higher. They moreover proposed
a mechanism for the electron transfer to the enzyme and
subsequent reduction of CO2 as depicted in Fig. 12.111
Also Bassegoda et al. later used formate dehydrogenase with
a metal active site for the reversible conversion of formate and
CO2. They suggest the molybdenum containing FateDH as
a highly active electrocatalyst for such redox processes.112
We recently investigated the immobilization of dehydrogenases encapsulated in an alginate based matrix on a carbon felt
electrode (Fig. 13). We found that for the immobilization of
a single enzyme, namely alcohol dehydrogenase, conversion of
an aldehyde to the corresponding alcohol is possible simply due
to direct electron injection without any co-factor or electron
shuttle.113
In a similar approach, using this technique for electrode
preparation, we then investigated the co-immobilization of all
three dehydrogenases on such electrodes for the conversion of
CO2 to methanol (Fig. 14). We obtained faradaic yields of 10% for
methanol generation from electro-enzymatic CO2 reduction.114
Besides electrochemical methods one also has to mention
here the possibility of photo-reduction of CO2. For this charges
Fig. 14 Scheme of the setup of an electrochemical cell for electroenzymatic CO2 reduction. Electrons are injected directly into the
enzymes, which are encapsulated in an alginate–silicate hybrid gel
(green) and immobilized on a carbon felt working electrode. CO2 is
reduced to methanol at the working electrode. Oxidation reactions
take place at the counter electrode.114
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Table 3
Journal of Materials Chemistry A
Summary of electrochemical approaches using enzymes for the reduction of CO2 via direct electron injection
Enzyme
Immobilization Co-factor/mediator
Product
Formate, formaldehyde,
alcohol dehydrogenase
Formate dehydrogenase
No
Methanol Glassy carbon
Yes
Formate dehydrogenase, No
methanol dehydrogenase
Formate dehydrogenase
Yes
Formate dehydrogenase
Alcohol dehydrogenase
Yes
Yes
Formate, formaldehyde,
alcohol dehydrogenase
Yes
NADH/neutral red
Electrode
Cathodic potential
0.8 V vs. SCE
(0.556 V vs. SHE)
Viologen
Formate
ITO
0.55 V vs. Ag/AgCl
(0.34 V vs. SHE)
Methylviologen,
Methanol Glassy carbon 0.7–0.9 V vs. SCE
pyrolloquinolinequinone
(0.456–0.656 vs. SHE)
None
Formate
Glassy carbon 0.41–0.81 V vs. Ag/AgCl
(0.2–0.6 V vs. SHE)
None
Formate
Graphite-epoxy 0.5–0.6 V vs. SHE
None
Butanol
Carbon felt
0.6 V vs. Ag/AgCl
(0.39 V vs. SHE)
None
Methanol Carbon felt
1.2 V vs. Ag/AgCl
(0.99 V vs. SHE)
or electrons are provided by a light source. Upon light excitation
electrons can be transferred from a semiconductor electrode to
an enzyme. Such an approach has been presented by the group
of Chaudhary et al. who used CdS nanoparticles assembled with
carbon monoxide dehydrogenase. They obtained turn over
frequencies for the conversion of CO2 to CO up to 22 000 aer
5 hours. This is higher than what was observed for synthetic
catalysts but still smaller than the maximum capability of
enzymes.115
Such approaches as the electrochemical or photochemical
reduction of CO2, utilizing electrodes with immobilized dehydrogenase enzymes and without any co-enzyme or mediator
required, depict a sustainable route towards biocompatible
reduction of the greenhouse gas CO2. This approach further
shows a viable and promising strategy for the substitution of
expensive co-factors. This makes enzymatic redox reactions also
attractive for industrial applications not only in the elds of CO2
reduction and renewable energy storage but also for extended
applications like the production of food additives and base
chemicals catalyzed by different enzymes. A comparison of the
different electro-enzymatic approaches is displayed in Table 3.
4. Conclusions
Biocatalysis and especially bio-electrocatalysis are interesting
and promising methods for CO2 recycling into chemicals and
articial fuels. Existing industrial methods for this purpose and
chemically synthesized catalysts oen lack in selectivity or yield
for the obtained products. Furthermore, high temperatures or
pressures may be required in such processes. In contrast, biocatalysts usually work under mild conditions at room temperature and atmospheric pressure. As a result, direct application
of biocatalysts has become more and more industrially attractive. Utilization of microorganisms or enzymes therefore paves
the way for CO2 conversion and generation of various chemicals
and biofuels with high yield and high selectivity. As presented
in various studies, biocatalytic especially bio-electrocatalytic
approaches offer high economic potential. Even though there is
still intensive work required for optimization to possible large
scale application, small scale approaches already showed that
This journal is © The Royal Society of Chemistry 2017
Reference
Minteer et al.57
Amao et al.109
Kuwabata et al.110
Reda et al.111
Bassegoda et al.112
Schlager et al.113
Schlager et al.114
not only high yields can be obtained, but even costs can be
reduced for electrochemical approaches without co-factors or
hydrogen equivalents like NADH or H2. In particular in the case
of the co-factor NADH cost reduction for CO2 conversion can
be obtained by several orders of magnitude when electrolysis
approaches were used instead. Such useful recycling of CO2
moreover displays a viable approach for large scale chemical
storage of renewable energies, as these can serve as a source for
the electrical energy supply.
Acknowledgements
The authors acknowledge nancial support by the Austrian
Science Foundation (FWF) within the Wittgenstein Prize
(Z222-N19), FFG within the project CO2TRANSFER (848862) and
REGSTORE project which was funded under the EU Programme
Regional Competitiveness 2007–2013 (Regio 13) with funds
from the European Regional Development Fund and by the
Upper Austrian Government.
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