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Green Chemistry
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Published on 26 October 2017. Downloaded by University of Windsor on 26/10/2017 16:22:02.
PERSPECTIVE
Cite this: DOI: 10.1039/c7gc01801k
View Journal
An overview of cathode materials for microbial
electrosynthesis of chemicals from carbon dioxide
Nabin Aryal,
a,b
Fariza Ammam,
c
Sunil A. Patil
*†d and Deepak Pant
*e
The applicability of microbial electrosynthesis (MES) for chemical synthesis from carbon dioxide (CO2)
requires improved production and energetic efficiencies. Microbial catalysts, electrode materials, and
reactor design are the key components which influence the functioning of such processes. In particular,
cathode materials critically impact the electricity-driven CO2 reduction process by microorganisms.
Interest in cathode surface modifications for improving MES processes is thus consistently increasing. In
this paper, the recent developments and spatial modification of cathode materials for microbial CO2
reduction are systematically reviewed. The characteristics of commercially available materials, their
modifications, and developments in new materials that have been used as cathodes for MES are summarized. Key cathode–microorganism interactions that led to improved CO2 conversion are then discussed.
The cathode surface modification approaches have focused mainly on improving the surface area and
surface chemistry of the materials. Although the modified cathode surfaces improved biofilm growth in
direct electron uptake based bioconversions, they have achieved lower acetate production rates than that
Received 17th June 2017,
Accepted 5th October 2017
DOI: 10.1039/c7gc01801k
rsc.li/greenchem
1.
of hydrogen-based MES processes thus far. Research efforts on different materials suggest that the threedimensional cathodes that can retain more biomass, in particular in hydrogen-based bioconversions, are
promising for further improvements in production efficiencies. Further efforts toward reducing the energy
inputs for achieving energetically efficient MES processes by using electrocatalytically efficient cathodes
are needed.
Introduction
Microbial electrosynthesis (MES) is an emerging novel green
technology for the production of biochemicals and biofuels
from CO2 using energy sources derived from a poised
cathode1–3 (Fig. 1). The energy can be supplied from renewable sources such as solar, wind, and biogas to catalyze CO2
reduction at the cathode by autotrophic acetogenic bacteria.4
MES thus opens up an alternate sustainable route for
efficient storage of surplus electrical energy into chemical
bonds of easily transportable gas or liquid fuels or chemical
a
Biological and Chemical Engineering, Aarhus University, Hangovej 2,
DK-8200 Aarhus N, Denmark
b
Danish Gas Technology Centre, Dr Neergaards Vej 5B, DK-2970 Horsholm, Denmark
c
Department of Engineering Science, University of Oxford, Parks Road, Oxford,
OX1 3PJ, UK
d
Institute of Environmental and Sustainable Chemistry, TU Braunschweig,
Hagenring 30, 38106 Braunschweig, Germany. E-mail: sunil@iisermohali.ac.in
e
Separation and Conversion Technology, Flemish Institute for Technological Research
(VITO), Boeretang 200, Mol 2400, Belgium. E-mail: deepak.pant@vito.be,
pantonline@gmail.com
† Present address: Department of Earth and Environmental Sciences, Indian
Institute of Science Education and Research (IISER), Mohali, Sector 81, S A S
Nagar, Punjab 140306, India.
This journal is © The Royal Society of Chemistry 2017
commodities.5 When coupled to the photovoltaic system, this
essentially becomes an artificial photosynthesis device
mimicking the CO2-to-chemicals process, where the conversion efficiency is up to 10% higher than natural photosynthesis bioprocess based bioenergy systems.6,7 Electrons can
also be supplied from the anodic substrate oxidation process
in a so-called microbial fuel cell (MFC) through an external
circuit.8
Autotrophic acetogenic microorganisms utilize the acetylCoA/Wood–Ljungdahl (WL) pathway to fix CO2.9 MES from
CO2 relies on the electron uptake capability of these microorganisms from the cathode. Microbes can either utilize electrons directly from the cathode or use reduced mediators or
regenerated equivalents from the electrode as the electron
source.10 The molecular mechanisms involved in cathodic
electron uptake processes remain still poorly understood.11 So
far, limited microorganisms for cathodic CO2 conversion have
been identified through either screening of pure homoacetogens (mostly Sporomusa and Clostridium spp.) or enrichmentselection from the mixed culture inoculum sources.
The first report on CO2 conversion to organic compounds
such as methane and acetate using microorganisms in bioelectrochemical reactors dates back to the mid-1990s.12 Later, in a
pioneering study, the possibility of providing the acetogenic
Green Chem.
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Published on 26 October 2017. Downloaded by University of Windsor on 26/10/2017 16:22:02.
Perspective
Fig. 1 A schematic of the MES for CO2 reduction to products on a
biocathode.
microorganisms such as Sporomusa and Clostridium spp. with
electrons delivered directly from a cathode to synthesize
acetate from CO2 was reported.1,4 Since then, the production
of a wide range of other chemicals, such as formate, butyrate,
ethanol, isopropanol, and butanol has been reported in
CO2-fed bioelectrochemical reactors.13–17 Another potential
approach in the power-to-gas and CO2 conversion framework
is electromethanogenesis, which leads to the production of
methane gas.18–20 This production pathway is not considered
in this paper as it has been recently reviewed in detail.18,21 The
major bottlenecks for the development of MES technology as
an economically feasible CO2 utilization approach are poor
production indicators such as low production rates, low
Dr Nabin Aryal is a post-doctoral
researcher at Danish Gas
Technology Centre (DGC) and
Aarhus University Denmark. He
received his M.Sc. degree in
Environmental Technology and
Engineering
from
Ghent
University, Belgium, with an
Erasmus Mundus fellowship and
then a Ph.D. degree from the
Technical University of Denmark
(DTU)
in
Environmental
Biotechnology. Currently, his
Nabin Aryal
research focuses on the optimization of bioelectrochemical cells for methane production, biogas
upgradation and carbon dioxide utilization from gasifiers. He has
6 peer-reviewed publications and >95 citations (h-Index 4).
Green Chem.
Green Chemistry
product titers, and energetic efficiencies. Microbial catalysts,
the target product, and electrode materials mainly determine
these key performance indicators. Different approaches have
been deployed in the recent years to optimize the MES process
and improve these production indicators. These include, e.g.,
the manipulation or augmentation of cultivation medium
composition to provide sufficient nutrients, improving reactor
design and feeding conditions, enrichment of mix culture
inoculum, operating reactors at optimized conditions and the
spatial arrangement of the cathode to enhance its interaction
with microorganisms.22–26
The cathode, by acting as an electron donor source to
microbes, critically determines the MES performance. Desired
electrode materials for use as biocathodes should have the following properties: (i) high conductivity, (ii) excellent chemical
stability, (iii) high mechanical strength, (iv) biocompatibility,
(v) high surface area and (vi) low cost.27–29
Recently, an increasing number of research efforts have
been devoted toward cathode material development and
spatial surface modification to achieve MES productivity
enhancements and bring it closer to its counterpart fermentation technology. Acetate, being the most widely investigated
and most prominent product of autotrophic CO2 fixation, is
often considered for evaluating the cathode performances in
MES systems.14 In this review, we provide up-to-date information on the cathode materials used for CO2 conversions
to liquid chemicals (mainly acetate) via the MES route in
bioelectrochemical systems (BESs). Firstly, the commercially
available materials used as cathodes in MES processes are
described. This is followed by a discussion on the spatial
modifications of the materials and purposely built cathode
materials. The key interactions between bacteria and cathodes
that lead to enhanced bioproduction are then discussed.
Finally, future research perspectives and directions for
advancing MES as a sustainable CO2 utilization approach are
provided.
Fariza Ammam
Dr Fariza Ammam is a postdoctoral researcher at the
Engineering
Department,
University of Oxford. She
received her M.S. degree in
Microbiology and a Ph.D. degree
in Molecular Microbiology from
the University of Paris Sud XI.
Her main interests are microbial
physiology, bioenergetics and
synthetic biology for anaerobes.
She is currently working on
engineering and optimising CO2fixing cell factories for the bioproduction of fuels and chemicals in bioelectrical systems.
This journal is © The Royal Society of Chemistry 2017
View Article Online
Green Chemistry
Nevin et al. (2010) described the first proof-of-principle of
direct CO2 reduction by using a negatively charged solid-state
graphite block cathode as an electron donor source.1 Since
then, several commercially available carbon electrodes of
different shapes and types such as rod or stick, block, cloth,
plate, activated carbon, gas diffusion activated carbon, granules, fiber rod, felt and reticulated vitreous carbon (RVC) have
been commonly used as cathodes in MES systems (Table 1).
Characteristics such as chemical resistance to corrosion, biocompatibility, and low-cost fabrication along with their proven
applicability as bioanodes in several other BESs drive
their wider and regular usage as cathodes in MES
processes.23,25,30–32
In particular, graphite has become a predominantly used
commercial carbon material. It is mainly used in the form of
block or plate, rod or stick, and granules. It possesses a plane
sheet structure and offers intrinsic advantages in aqueous
solution, such as a wide electrochemical window, relative inertness, sufficient electrical conductivity, low residual current,
ease of modification, recyclability, reusability and very high
biocompatibility.33 However, the use of a single graphite block
or rod has a limitation to achieve higher productivity because
of its low porosity and low accessible surface area for the
adherence of microorganisms. Marshall and coworkers, therefore, proposed to use granular graphite as a cathode and
achieved a high volumetric acetate production rate from
CO2 with an enriched electrosynthesizing mix microbial
culture community. 15,34 Electron micrographs confirmed
increased bacterial cell attachment and growth on such
cathodes over time. Such granular graphite materials provide a
high volumetric surface area and porosity to favor electrode–
microorganism interactions and sustain electrogenic biofilm
activity.15,34
Other two-dimensional (2D) thin morphology carbon
materials such as carbon plate and carbon cloth are also
widely used owing to their better electrical conductivity,
chemical stability, light weight, flexibility, and higher porosity
compared to the graphite electrode. An early representative
study by Zhang et al. used carbon cloth in MES systems due to
its simplicity, flexibility and ease for further surface modification.29 Such plane 2-D electrodes, however, possess several
disadvantages such as availability of low reactive specific
surface area, low electrocatalytic activity, high internal resistance, high activation overpotential, and rapid creation of a
passivation layer on the electrode surface thereby limiting their
use in MES systems.
Carbon felt and carbon fiber rod electrodes are examples of
three-dimensional (3D) materials that have been explored in
MES systems (Table 1). The three-dimensionally arranged topology of these electrodes offers a high volume reactive surface
area for the growth of biomass and minimizes mass transfer
limitations. Furthermore, electrodes with 3D structure are flexible for further spatial modification, and their catalytic reactive
sites offer better interactions for electron exchange through
either direct or mediated processes.35 Carbon felt has been
widely used due to its high porosity, high surface area, and
Dr
Sunil
Patil
(Ph.D.,
Microbiology, 2011) is an
Assistant Professor at Indian
Institute of Science Education
and Research (IISER), Mohali.
His research interests include
microbial electrochemistry, CO2
conversion to biochemicals and
biofuels through microbial electrosynthesis, resource recovery
from
wastewaters
using
microbial fuel and electrolysis
cells, and electro-bioremediation
Sunil A. Patil
of micropollutants. He has been
a recipient of the DAAD scholarship (2008–2010), the Marie
Skłodowska-Curie fellowship (2013–2015) and the Humboldt
fellowship for experienced researchers (2016–2017). He has published 28 peer-reviewed publications (>1350 citations; H-index 21)
and 8 book chapters.
Dr Deepak Pant is a senior scientist at Flemish Institute for
Technological Research (VITO)
currently working on bioenergy,
specifically, the design and
optimization of microbial fuel
cells (MFC) for energy recovery
from wastewaters and microbial
electrosynthesis (MES) for the
production
of
value-added
chemicals through electrochemically driven bio-processes. He
has a Ph.D. degree in environDeepak Pant
mental biotechnology and has 82
peer-reviewed publications (>4700 citations; h-index 36) and 22
book chapters to his credit. His research experience lies in bioelectrochemistry, microbial fuel cells, electrosynthesis, biofuels, bioenergy and life cycle analysis (LCA). He serves as the Editor for the
new Elsevier Journal “Bioresource Technology Reports”.
2. Cathode materials used for
MES from CO2
Carbon based materials are the most widely used cathodes for
the bioconversion of CO2 in the MES systems. Fig. 2 depicts
the timeline of the use of different commercially available and
surface-modified cathode materials in CO2 fed MES systems
along with performance improvements (in terms of cathode
surface based production rates) over the years.
Published on 26 October 2017. Downloaded by University of Windsor on 26/10/2017 16:22:02.
Perspective
2.1
Commercial cathodes
This journal is © The Royal Society of Chemistry 2017
Green Chem.
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Perspective
Green Chemistry
Fig. 2 Timeline depicting the developments of the cathode materials for CO2 reduction to acetate in MES systems. The highest acetate production
rates (in terms of g m−2projected cathode surface area d−1) achieved in each year are presented in parentheses. For detailed information on different other
aspects of these MES studies, refer to Tables 1 and 2. SS – stainless steel, Au – gold, Pd – palladium, Ni – nickel, CNT – carbon nanotube, Si–TiO2 –
silicon-titanium oxide, 3D RVC – three dimensional reticulated vitreous carbon, rGO – reduced graphene oxide, TEPA – tetraethylene pentamine,
MWCNT – multiwall carbon nanotube.
flexibility for further surface modifications. In a recent study,
Bajracharya et al. optimized the acetate production rate by
adding a stainless steel current collector to the carbon felt
cathode and by lowering the applied potential to −690 mV
versus SHE for in situ hydrogen generation to mediate electron
transfer.31 Its use for the bioconversion of CO2 has also been
successfully demonstrated in MES systems operated in a galvanostatic mode.25,36 In galvanostatic control, by applying a constant current, H2 can be generated continuously at cathodes
for achieving non-limiting H2-based bioproduction.
Recently, the direct use of unmodified RVC foam as cathodes
has also been reported.37 In this study, the combination of galvanostatic control and the high surface area of the RVC
cathode along with a continuous flow mode operation of biocathodes resulted in the high rate production of acetate
(196.8 g m−2 d−1) from CO2. Stainless steel (SS) materials have
been mostly used either as current collectors or in combination with the carbon-based cathodes in MES systems.25,31 Its
direct ‘as is’ use without any surface modification is limited
mainly due to its poor biocompatibility. However, its potential
applicability as cathodes, in particular for H2-based bioproduction, has been demonstrated.38,39
2.2
Purposely built or modified cathodes
The use of surface modified and purposely built materials
have been increasingly proposed for biocathode optimization
for MES from CO2 (Table 2). Before surface modification, electrodes are subjected to pretreatment, which potentially
exposes the reactive surfaces for further modification and
immobilization. The electrodes undergo either chemical treatment or thermal treatment to remove impurities from their
surfaces. Commercially available carbon cloth and carbon felt
are the most commonly used base materials for the spatial
modification of electrodes because of their outstanding
characteristics of flexibility, high porosity, high surface area for
bacterial adherence and ease of spatial modification.23,29 For
example, Zhang et al. modified carbon cloth electrodes by
Green Chem.
immobilizing chitosan, cyanuric chloride, 3-aminopropyltriethoxysilane, polyaniline, melamine, ammonia, gold, palladium, carbon nanotube (CNT) cotton and CNT polyester for
CO2 reduction with S. ovata.29 Among the modified cathodes,
chitosan, an amino and hydroxyl-group rich polysaccharide,
increased the acetate production rate by 7.6-fold compared to
its counterpart, unmodified carbon cloth cathode. This was
attributed to its better biocompatibility resulting in improved
electrostatic interactions between negatively charged bacterial
cells and the positively charged chitosan-modified electrode.
The catalytic surface with suitable pore size properties also
enhanced biofilm growth on the cathode. Furthermore, carbon
cloth modification with metal nanoparticles, such as gold
(Au), palladium (Pd), or nickel (Ni) resulted in an increase of
acetate production rates by 6-, 4.7- and 4.5-fold, respectively,
compared to untreated electrodes. The low charge transfer
resistances and the high conductivity of the nanoparticles
were suggested to be at the origin of the enhanced acetate production in MES reactors.29 Similarly, cotton and polyester
fabric based cathodes treated with CNTs also showed 3.4- and
3.2-fold higher acetate production rates compared to the
untreated carbon cloth cathode. CNTs are one of the most
promising materials for designing electrodes of bioelectrochemical devices, in particular, of biosensors and MFCs due to
their high conductivity and biocompatibility but are relatively
expensive.50,51 In another study by the same group, nickel (Ni)
nanowires coated on a graphite stick with microwave treatment
enhanced its surface roughness by almost 50 times compared
to untreated graphite52
The porous structure of Ni-nanowire graphite substantially
enhanced cathode–microorganism interactions leading to a
2.3 fold increased acetate production rate over untreated electrode.52 Jourdin et al. developed a NanoWeb-RVC cathode by
using a chemical vapor deposition (CVD) method, which
resulted in substantial enhancement of acetate production rate
by 33.3 fold compared to the unmodified carbon plate electrode.27 Modified NanoWeb-RVC offers a high surface area
This journal is © The Royal Society of Chemistry 2017
View Article Online
Green Chemistry
Table 1
Perspective
Commercial cathode materials used in CO2 fed MES systems
Acetate production
Cathode
materials
Microbial culture
or inoculum source
Operation
mode
Applied
potential
(mV vs.
SHE)
Carbon rod
Anaerobic digestion
slurry
Sporomusa ovata
S. sphaeroides
S. silvacetica
Clostridium aceticum
Clostridium ljungdahlii
Moorella thermoacetica
Brewery wastewater
Batch
−201
−4.1
0.0431
0.2
CH4
Ng
12
Batch
Batch
−400
−400
−400
−590
1.38
0.062
0.045
0.006
0.14
0.104
Ng
0.063
0.0028
0.002
0.0027
0.0065
0.0065
1.7
2-Oxobutyrate
—
2-Oxobutyrate
—
2-Oxobutyrate, formate
—
H2, CH4
86 ± 21
84 ± 26
48 ± 6
53 ± 4
88 ± 2
85 ± 7
67
1
Batch
−0.207
−0.017
−0.006
−0.024
−0.031
−0.031
Ng
Brewery wastewater
Batch
−590
Ng
Ng
10.5
H2, CH4
69
Batch
−853
−953
−400
−3.3
−9.2
−0.03
16.3
19.2
0.063
0.33
0.39
0.02
24
40
18
35.2 ± 4.4 41
−1.5
−3.1
Ng
−3.23
−5
12.8
1.58
9.75
38
19
0.127
0.11
Ng
0.34
1.29
81
56.6
89.5
40 ± 4
58 ± 5
39
42
Batch
Batch
−690
−703
−903
−600
−1260
H2, CH4
H2, CH4
Ethanol, H2, butyrate,
propionate, & butanol
—
H2
H2
H2, formate
H2
Batch
−1140
−5
20.4
13.5
—
60.8
36
−1.7
−12.3
9.68
2.7
2.065c
Ng
H2
CH4
89 ± 12
28.9
44
45
Batch
Batch
−895
−690
−600
−690
−10
−1
−34.53
−2.1
40
7.51
18.35c
51.1
0.63
0.63
4.13
0.89
H2, CH4 and ethanol
Ethanol, H2
Ethanol
—
45 ± 7
31
64 ± 35
29.13
46
85.3 ± 8.3 26
Batch
−800
−20b
92.54c
2.8c
16
Batch
Batch
Batch
−660
−690
−690
−795
8.2c
33.28
8.1
14.41
3.04
10.4
10.7
16.57
0.244
0.1
0.41
0.73
0.18
0.53
0.54
10
53
87.6 ± 6.5
91.8 ± 5.3
61.1 ± 12
84.9 ± 4
69.9 ± 0.9
90.8 ± 12
50
38
22
30
Batch
−1.4
Ng
−0.45
−0.78
−0.19
−0.57
−0.7
−10
Ethanol, butyrate &
butanol
H2
Ethanol
—
—
—
—
—
H2, butyrate, ethanol
Continuous −800
∼−23
108
2.56
H2
33.6
48
Continuous −1100 to
−1300
Continuous −1000
−83.3
196.8
3.6
H2
35
37
−5
21
3.5
Butyrate & isopropanol
63
17
−0.37
4.9
0.1
—
4.9
49
Published on 26 October 2017. Downloaded by University of Windsor on 26/10/2017 16:22:02.
Graphite stick
Graphite stick
Graphite
granular
Graphite
granular
Carbon felt
Domestic wastewater
sludge
Carbon fiber rod Bog sediment
SS felt
Carbon felt
Graphite rod
Carbon felt
Batch
Acetobacterium woodii
Batch
Domestic WWTP sludge Batch
Brewery wastewater
Enriched mix culture
(from UASB effluents)
Carbon felt with Enriched mix culture
SS
(from UASB effluents)
Graphite stick
S. ovata
Graphite
Anaerobic digester
granular
sludge
Carbon felt with Wastewater sludge
Clostridium ljungdhalii
SS
Graphite stick
Enriched mix culture
Graphite stick
Methanol adopted
S. ovata
Carbon cloth
Enriched mixed culture
from syngas
SS plate
S. ovata
Graphite block
S. ovata
Graphite block
S. ovata 2662
S. ovata 2663
S. ovata 3300
S. acidovorance
S. malonica
Graphite felt
Enriched anaerobic
with graphite
sludge
stick
Carbon felt with Enriched anaerobic
SS
sludge
RVC foam
Enriched acetogenic
culture
Carbon felt with Enriched mix culture
SS
Carbon Paper
S. ovata 2662
Batch
−740
Continuous −600
Batch
Batch
−690
Maximum
Current
titer
densitya Ratea
(A m−2) (g m−2 d−1) (g L−1)
Other products
CE in
acetate
(%)
Ref.
4
15
34
43
25
47
a
Calculated based on projected surface area. b Maximum reported current density on the 34th day. c Approximate calculation from given production graph, WWTP – wastewater treatment plant, ng – not given, SS: stainless steel; CE: Coulombic efficiency.
with macroporous size that enhances mass transfer and
biofilm formation.27 These researchers further developed CNT
modified RVC electrodes (referred to as EPD-3D) using an electrodeposition method and reported a high rate synthesis of
acetate from CO2 with an enriched, stable acetogenic microbial
community.58 They further modified RVC with multi-walled
CNTs (MWCNTs) using the same technique. MES systems with
This journal is © The Royal Society of Chemistry 2017
these cathodes resulted in an acetate production rate of up to
1330 g m−2 d−1, the highest to date based on the projected
cathode surface area. This exceptionally high rate of bioproduction was achieved by utilizing highly open macroporous
RVC with a pore size of 0.6 mm that resulted in a good balance
between high surface area availability for biofilm formation
and efficient mass transfer between the biocathode and the
Green Chem.
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Perspective
Table 2
Purposely built and surface modified cathode materials used in CO2 fed MES systems
Cathode materials
Published on 26 October 2017. Downloaded by University of Windsor on 26/10/2017 16:22:02.
Green Chemistry
Carbon cloth +
Chitosanb
Cyanuric chlorideb
3-Aminopropyltriethoxysilaneb
Polyanilineb
Melamineb
Ammoniab
Goldb
Palladiumb
Nickelb
CNT-cottonb
CNT-polysterb
Graphite stick – Ni nano wire
Nanoweb 3D RVC
3D RVC with CNT
MWCNT-RVC
Activated carbon
VITO-CoRE™d
Si–TiO2 nanowire
photocathode
Carbon cloth-reduced
graphene oxide tetraethylene
pentamine (rGO-TEPA-CC)
3D-graphene carbon felt
composite
Gas diffusion activated
NORIT® carbon
3D iron oxide modified
carbon felt
Graphene paper
Microbial
culture source
S. ovata
S. ovata
WWTP sludge
Enriched mix culture from
WWTP sludge
Same as above
Mix culture
Acetate production
Applied
Current
potential
densitya
Maximum Fold
CE in
(mV vs. SHE) (A m−2) Ratea (g m−2 d−1) titer (g L−1) increase f acetate (%) Ref.
−400
−0.47
−0.45
−0.20
13.51 ± 3.30
12.09 ± 2.95
5.6 ± 1.18
0.59e
0.79e
0.31e
7.6
6.8
3.1
86 ± 12
81 ± 16
82 ± 11
5.32 ± 1.29
1.8 ± 0.47
1.65 ± 0.82
10.67 ± 2.59
8.32 ± 2.06
8.024 ± 1.94
6.618 ± 1.47
5.66 ± 1.416
3.38
195 ± 30
685 ± 30
0.18e
Ng
−400
−850
−850
−0.18
−0.06
−0.06
−0.38
−0.32
−0.30
−0.22
−0.21
−0.63
−37
−102
0.35e
0.45e
0.23e
0.3e
0.13e
0.094
1.2
11
3
Nil
Nil
6
4.7
4.53
3.4
3.2
2.3
33.3c
—
85 ± 7
80 ± 15
82 ± 8
83 ± 14
79 ± 16
80 ± 15
83 ± 10
82 ± 8
82 ± 14
70 ± 11
100 ± 4
52
27
53
−1100
−400
−200
−0.165
1330
9.49
11
4.1
—
—
84 ± 2
29.91
24
54
Ng
6
—
86 ± 9
55
29
S. ovata
−595
−3.5
Methanol adapted S. ovata
−690
−0.23
62.4 ± 26.64
1.88
11.8
83 ± 3
28
S. ovata
−690
−2.4
54.57 ± 1.7
1.4
6.8
86 ± 3
23
Enriched Anaerobic sludge −1000
−20
36.6
2.89
—
35.46–88
56
e
S. ovata
−690
Ng
25.40e
1.8e
4.8
86 ± 9
57
S. ovata
−690
−2.5
39.8
0.77
8g
90.7
49
a
Calculated based on projected surface area. b Modified on the carbon cloth surface of electrode. c Compared to control carbon plate electrode.
Trade mark plastic inert support electrode. e Approximate calculation from given production graph. f The fold increase is compared to the
respective unmodified cathodes. CE – Coulombic efficiency, Ni – nickel, CNT – carbon nanotubes, Si–TiO2 – silicon–titanium oxide, 3D – Three
dimensional, RVC – reticulated vitreous carbon, ng – not given, nil – negative result or no improvement. g Compared to control carbon paper
electrode.
d
bulk electrolyte.59,60 In an interesting approach, Liu and coworkers developed the silicon-titanium oxide nanoparticle
(Si-TiO2) photocathode to harvest sunlight directly. Using this
photocathode, which harvested light as the sole electron
source, up to 6 g L−1 acetate was produced with S. ovata.55
Recently, Cui et al. used iron oxide modified 3D carbon felt
cathodes and reported 4.8-fold enhancement in the acetate
production rate compared to the unmodified carbon felt
cathode.57 The semi-conductive properties of ferric oxide were
suggested to enhance the efficiency of extracellular electron
transfer in this case.
Graphene, whose use for the development and surface
modification of different non-conventional carbonaceous
materials is on the rise,61 has also been used for developing
cathodes for MES systems. For instance, Chen et al. functionalized tetraethylene pentamine in situ after reducing graphene
on a carbon cloth electrode.28 In this case, the electric charge
interaction accelerated biofilm formation and led to 11.8-fold
enhancement in the acetate production rate compared to the
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unmodified electrode.28 Aryal et al. developed a 3D graphene
carbon felt electrode for the formation of robust biofilm and
reported enhanced acetate productivity by 6.8-fold compared
to unmodified carbon felt.23 This research group further developed the freestanding and flexible graphene paper cathodes
and reported 8-fold enhancement in acetate production compared to commercially available carbon paper electrode. The
application of graphene electrodes49 in MES systems would be
attractive considering its relatively low production costs.62,63
The use of other composite electrodes such as activated
carbon VITO-CoRE® electrode and gas diffusion electrodes
(GDEs) has also been investiagted.54,56 The porous composite
activated carbon gas diffusion electrode provides an ideal
three-phase interface (gas–liquid–solid). It consists of a hydrophobic gas diffusion layer to diffuse the CO2, a current collector, and a catalyst layer for the synthesis of chemicals by bacteria. The use of such a GDE led to an improved and controlled
transfer of CO2 to the biocatalyst in MES as compared to the
conventional gas sparged systems. The mass transfer coeffi-
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cient (kLa) for GDE was twice that of the sparged system.56
However, CO2 solubility was often limited by a thin diffusion
layer formed with the wetted electrode surface.64–66 The same
research group developed the VITO-CoRE™ electrode with
plastic inert support as the cathode. This cathode with a high
surface area led to enhanced biofilm formation and better productivity of MES from CO2 in single chamber reactors.54
3. Key cathode–microorganism
interactions that lead to improved
MES performance
Electrode surface modification is an important strategy for
enhancing electrode–microorganism interactions. Several
reviews have summarized the required surface properties for
engineering electrodes for bioanode applications.67–69 Some of
the approaches reported for anode surface modification have
also been employed successfully to generate better surfaces for
cathodic processes. Biocompatibility and a high active surface
area together with chemical stability are the main properties
that have been taken into consideration for developing cathodes for MES processes so far.27–29,69 In microbial electrochemistry, projected surface area, Brunauer–Emmett–Teller
(BET) surface area, biofilm covered area, electrochemically
active surface and bioelectrochemically active surface have
been used for the performance analysis of electrode
materials.69 The BET surface is often used for reporting the
performance of the modified electrode materials in MES
systems. The consideration of bioelectrochemically active
surface area in MES depends on the physical and biological
interactions at the electrode materials.
Perspective
The key approaches used for the surface modification of
cathodes are depicted in Fig. 3. These have mainly led to
improving either the surface chemistry or the surface area or
both, of the modified electrodes. A considerable improvement
in the cathode surface based acetate production rates has been
achieved by using surface modified or purposely built cathodes in MES systems. The key reasons or effects that led to
improvements in MES performance indicators are briefly discussed below.
3.1
Improved surface area
The 3D electrodes having multiple layers of micro, meso and
macro pores allow efficient mass transfer and provide more
surface to increase the bacteria loading (Fig. 3A). In this
regard, a highly conductive 3D NanoWeb-RVC, developed by
coating MWCNTs on RVC, generated a cathode with high
surface to volume ratio optimal for bacterial attachment and
mass transfer within the biofilm.28 Another electrode developed by using electrophoretic deposition by coating CNTs on
RVC followed by chemical treatment resulted in a highly conductive cathode that delivered 100% electron recovery compared to 70% obtained with the NanoWeb-RVC.27,58 All these
modifications benefitted from a macroporous structure of RVC
that possessed high porosity and surface area. Besides
improved surface area, these modifications also imparted
additional properties to the cathode. For instance, the deposition of CNTs was suggested to improve the electrochemical
communication between the microbes and the cathode.58
Furthermore, the functionalization of MWCNTs improves the
electrochemical communication between the microbes by
chemical treatment and was suggested to improve the conductivity of the material. It has been reported that the higher BET
Fig. 3 Approaches adopted for modifying cathode surfaces and resulting effects on biofilm growth enhancement due to (A) improved 3D surface
area and porous structure, (B) improved 3D surface area and functional group attachment, and (C) positively charged surface.
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active surface area on an electrode helps to reduce the ohmic
loss by improving the current density.70 In one MES study, the
BET surface area of the reduced graphene oxide (rGO) functionalized carbon felt was increased by 2.2 fold after the modification of the base electrode (Fig. 3B).23 In this case, this modification led to manifold improvement in the MES productivity.
Increase in the specific surface area using Fe2O3 nanoparticle
deposition on the carbon felt cathodes that resulted in
improved MES performance has also been reported.
3.2
Improved cell attachment and biofilm formation
Improved surface chemistry can have a positive impact on the
adherence of bacteria by providing a better electroactive nanosurface through hydrogen bonding, electrostatic attraction,
and van der Waals interaction.24,29,71 The bacterial community
used as biocatalysts greatly impacts biofilm formation and the
electron transfer process. Therefore, a comparison between
pure culture and mix culture driven MES regarding biofilm formation would not be appropriate. Mix cultures have been
reported to be more tolerant to environmental stress conditions and fluctuations, and have shown higher production
rates (Tables 1 and 2), which would suggest that they show
better bioelectrocatalysis and form a better biofilm on the
cathode than pure cultures.16,31,58 Two independent studies
with 3D electrodes by Jourdin et al. highlight the role of modified materials in enhancing biofilm formation by the mix
culture.27,58 In these studies, the same inoculum was used to
allow the comparison between the efficiencies of different
materials including graphite plates, carbon felt, NanoWebRVC and EDP-3D. A well-developed and uniform biofilm with
multilayers of microorganisms (thickness in the range of
5–10 µm) associated with a manifold increase in MES productivity was reported for the EDP-3D electrode. However, no
uniform biofilm coverage was observed in the case of other
electrodes inoculated with the same inoculum.
MES with pure cultures in different studies can be compared if the same microorganism and the same cathode potential were used. The pure cultures of many acetogens tested in
MES systems including S. ovata, which represents the most
well-studied electroautotroph so far, showed poor biofilm
growth on unmodified graphite, carbon felt or stainless steel
cathodes.1,4 Several initial reports on MES from CO2 described
non-uniform, dispersed, patchy monolayers of cells on the
poised cathodes.1,4,31 Among the numerous surface treatments
applied by Zhang et al. for engineering a positively charged
cathode only carbon cloth coated with cyanuric chloride or
chitosan increased acetate production by 6 to 7 fold compared
to the untreated electrodes.29 The confocal laser scanning
microscopy images of the biocathodes showed nine times
higher cell density biofilm on the chitosan modified cathode,
thereby most likely supporting the higher acetate rate observed
with this modified cathode.29 The authors argued that the
Gram-negative bacterium S. ovata surface is negatively charged
and the untreated carbon felt is neutral. Thus, the treatments
applied had the objective to promote bacterial attachment and
biofilm formation by means of adding positively charged
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molecules on the electrode surface (Fig. 3C). Similarly, Chen
et al. used rGO and positively charged tetraethylene pentamine
nanoparticles to modify carbon cloth for improving cell attachment and reported a highly structured biofilm with the presence of what they named as self-assembled spheres formed by
an adapted strain of S. ovata to methanol.28
3.3
Improved (bio)electrocatalysis
Although the cathodic bioconversion processes have gained an
increasing interest during the recent years, very little is known
about the mechanistic of electron uptake by bacteria from a
poised cathode.10,72,73 Extracellular electron transfer (EET)
mechanisms from the cathode to the microbes have been
hypothesized based on the electron transfer from the microbes
to the anode.74
The cathodic EET may occur via two different mechanisms
depending on the microorganism and other experimental conditions involved: (i) mediator-free transfer (direct EET) or
(ii) mediator-dependent transfer (indirect EET) (Fig. 4). In
direct EET (Fig. 4A), a physical connection between the extracellular structures of the microorganism and the cathode is
required. A few acetogenic bacteria like C. ljungdahlii which do
not have cytochromes have been reported to be able to receive
electrons directly from a poised electrode.4 The ability of the
most commonly used homoacetogen, S. ovata, to achieve DET is
suggested to not necessarily depend on the presence
of specialized structures like nanowires but rather on the quantity of cellular redox active enzymes released under specific operating conditions. This is likely a realistic explanation for electron
uptake by S. ovata in the absence of any redox mediators or
energy carriers in MES processes. In fact, most of the operating
conditions applied so far in pure culture driven MES systems,
consisted of an additional step of pre-establishing biofilm on
the cathode. This step requires growing bacteria with hydrogen
for several days and may result in cell lysis and enzyme release
that can eventually mediate the electron transfer.
No direct contact with the solid surface is required for
indirect EET. The indirect EET requires diffusible extracellular
compounds such as redox mediators and energy carriers like
H2 and formate that transport electrons between the electrode
and the microorganisms. Enzymes like hydrogenases, and
formate hydrogenases secreted by the biofilm matrix and
released due to the cell lysis, have been identified to mediate
indirect EET, for instance, in the case of identical processes
with the electromethanogenic archaeon Methanococcus maripaludis.63,75 Like in direct EET, the mechanisms of mediatordependent cathodic EET are also still unclear (Fig. 3B and C).
In the case of H2-mediated MES processes, a considerable lowering of the H2 evolution overpotential by biocathodes has generally been observed.24,25,37 This effect has been attributed
mostly to the biocatalytic activity of the microbial community
grown on the cathodes. The role of modified cathode surfaces
on enhancing the H2 electrocatalysis has not been reported
and thus remains unclear in MES studies.
Most of the studies on MES from CO2 with modified
materials reported enhanced cathode–microorganism inter-
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Perspective
Fig. 4 Proposed extracellular electron transfer mechanisms between the cathode and the microorganisms. Direct electron transfer may occur via
cytochromes and/or nanowires (A), and indirect electron transfer may occur either by hydrogen mediation or enzyme mediation (B–C).
actions but did not shed more light on the electron transfer
mechanisms. However, these studies highlighted the impact of
better engineered surfaces on biofilm development and
enhanced bioelectrocatalysis. In this light, it can be speculated
that independent of the electron transfer mechanism, which
may be direct and/or indirect, biofilm growth and probably its
thickness and heterogeneity play major roles in electron transfer efficiency.
A control experiment without microbes has been performed
to explain whether product formation has the direct contribution from the abiotic electrocatalytic activities of the electrode.49 None of the control experiments in MES has identified
the electrochemical reduction of CO2 in aqueous solution.
Hence, it can be concluded that the bioelectrocatalytic activity
was principally responsible for the CO2 reduction process in
MES systems. It is important to note that MES studies employ
mostly carbon-based and SS materials as the cathodes. The
electrochemical reduction of CO2 into hydrocarbons and other
products has been reported on copper electrodes.76 In a pioneering study, Hori et al. reported the electrochemical formation of CH4, C2H4, EtOH and PrnOH by using single crystal
electrodes and then described the molecular mechanism
involved in this conversion.77 The surface morphology of the
electrode had a critical role in the selectivity of product formation. Firstly, CO2 was reduced to CO2− by accepting an electron from the electrode and then it further reduced to CO. It
was further proposed that CO was reduced to HCOO− at potentials more positive than −1.10 V vs. SHE.76–80 The mechanisms
of CO2 reduction by biological catalysts differ considerably. For
example, several enzymes are involved in the conversion of two
CO2 molecules into acetate via an acetyl-CoA pathway.9 As
mentioned before, the electron uptake in biocathodes is either
H2 mediated or direct microbe–cathode interaction based,
depending upon the experimental conditions, in particular,
the operational cathode potential and type of microbial catalysts used. The molecular mechanisms involved in electron
This journal is © The Royal Society of Chemistry 2017
uptake processes at biocathodes are still not clear. The impact
of the electrode surface properties on the biofilm structure
and electron transfer mechanism is better understood and
characterized in the case of bioanodes. For instance,
Artyushkova et al. investigated the relationship between
surface chemistry and the electrogenic biofilm by a multi-technique study combining analytical, spectroscopy, microscopy
and electrochemical techniques. The aim of the study was to
determine how functional groups like –N(CH3)3+, –COOH, –OH
and –CH3 at the anode surface affect the morphology, the
chemistry and the functional properties of Shewanella oneidensis MR-1 biofilm.81,82 Positively charged and hydrophilic surfaces were found to be optimal for the growth of a uniform
biofilm with very small cluster size and intercluster diffusion
distance, which was suggested to be at the origin of the high
electron transfer efficiency observed. The authors also stipulated that the biofilm heterogeneity is more important than
the biofilm thickness. In contrary to what was expected, the
influence of the substratum chemistry was found not only to
affect the initial cell attachment phase to the electrode surface
but also to influence the cell–cell interactions and the biofilm
architecture. In a different study, Guo et al., investigated the
effects of surface charge and surface hydrophobicity on the
anodic biofilm formation by using glassy carbon surfaces
modified with –OH, –CH3, –SO3−, or –N + (CH3)3 functional
groups. The results demonstrated that current output was correlated with the biomass quantity of the Geobacter population.
Positively charged functional group attached surfaces and
hydrophilic surfaces were more selective towards the electroactive microbes and thus formed more conducive electroactive
biofilm.71 Recently, a model of mechanistic stratification
occurring in the electroactive biofilm was described for
G. sulfurreducens.83 According to this model, the nanowires
coordinate with cytochromes present in the biofilm matrix to
transfer electrons from the cells located in the upper layers of
the biofilm to the cells located close to the anode. In this case,
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the nanowires directly discharge electrons from cells to cytochromes that act as gates between the biofilm and the anode.
Similar mechanisms might also be speculated for the highly
functionalized biocathodes obtained with different surface
modifications described in this review where the surface
substratum improves the cell–cell interactions and the biofilm
architecture, which in turn improves the electron transfer from
the cathode to microbes.
4.
Future perspectives
The main challenge for MES processes is the performance
improvement while maintaining low production costs. Multiple
strategies such as enrichment of microbial inoculum, screening
of new electroautotrophic microbes, reactor design, improving
feeding conditions and cathode material modification have led
to considerable improvements in CO2 conversion in MES
systems. Key research considerations concerning cathodes and
other components of MES systems that can be useful to advance
this CO2 utilization approach further are presented below.
• One of the limiting factors for the development of cathode
materials is a lack of experimental understanding of electron
exchange mechanisms from the cathode to the microbes.
Moreover, a good understanding of the biofilm formation
process on poised solid surfaces is necessary for further improvement of MES processes. In addition to the biocompatibility and
high surface area, other parameters may favor the attachment of
bacterial cells to the electrode surface. For instance, Philips et al.
recently reported that C. ljungdahlii biofilm development on
graphite and glassy carbon, two materials often used in MES,
may be induced by NaCl addition.84 RNA-sequence analysis
revealed the mechanistic of biofilm formation under stress conditions. Pilus-like appendages were observed and seen between
the cells.84 Similar structures referred to as nanowires have been
suggested to conduct electrons in the case of two electroactive
bacteria Shewanella and Geobacter species.85,86 These findings
on inducing biofilm formation on cathodes may provide a valuable approach for developing pure-culture driven MES processes.
• Biofilm engineering for bioelectrocatalysis is as important as understanding the electron transfer mechanisms. The
conductivity of the biofilm depends mainly on the physiological state of the cells within the biofilm. Due to the presence of
different strata of cells and depending on their location from
the electrode, some cells in the biofilm may face respiratory
limitation due to the lack of oxidised electron carriers. Indeed,
a redox gradient has been reported to occur within the biofilm
in an anodic process.83,87 Engineering biofilms with the right
and precise thickness is crucial for the control of pH and
nutrient gradients inside the biofilm matrix to ensure a
uniform distribution of cell activity inside the biofilm. This
will also contribute to maintaining the physiological state of
the cells located in different strata but also the redox and electrical gradients inside the biofilm.83,87
• The cost of cathode material development is one of the
major bottlenecks toward approaching the practical appli-
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cations for this process. Acetate production rates have been
substantially improved in lab scale reactors; however, the pilot
scale production has not been demonstrated yet. MES
reactors with MWCNTs deposited on RVC and graphenebased cathodes have shown better performances, however,
they are expensive. Recent analysis indicated that acetate production from MES is much more expensive than anaerobic fermentation technology due to the extra costs associated with
the use of membrane and electrodes.88 Therefore, to make
MES profitable, the recommendation was made on the development of high performance and durable electrode materials
and membrane at minimum costs. Here, the knowledge
gained in electrode development for other microbial electrochemical technologies can be explored for further development of cathodes for MES processes.
• Achieving high current densities at the cathodes to realize
a high rate production is a good strategy for enhancing MES
productivity.23,58 Thus, the current density of the biocathode
needs to be optimized by developing cheap and efficient electrodes, for instance, for H2 production. Decreasing the H2
evolution overpotential of the cathodes by exploring metal-based,
graphene, or composite materials is one option. So far, a
limited number of metal-based composite electrodes has been
applied in MES. These include mainly metals such as SS, iron,
Pt, Au, and Ni.29,37 The experience of microbial electrolysis
cells for H2 production might be applied to explore cathode
materials for MES processes. The supply of H2 produced by
electrolyzes to feed acetogens in fermenters might be an
alternative strategy that needs to be explored further to achieve
higher production rates.38
• More work on DET based bioproduction is necessary
because the productivity is relatively low compared to the H2
mediated bioproduction in MES systems (Tables 1 and 2). This
approach circumvents the washing out of the biomass from
the systems, for instance in continuous reactors. As the bioconversions are facilitated at higher electric potential, this
might also allow achieving higher energetic efficiencies
thereby reducing the energy input for MES processes.
• Optimization of operational conditions like improving
electron supply turnover by galvanostatic control and continuous flow supply of growth medium to overcome nutrient limitations could warrant the productivity enhancement.25 A recent
study by LaBelle et al. with controlled operating conditions
resulted in a high rate acetate production.37 This study was
performed with an unmodified RVC electrode previously
reported to be not able to promote the biofilm development.
In this case, the constant flow of fresh medium coupled to
galvanostatic control resulted in 52-fold higher volumetric production rates compared to the one obtained with NanoWebRVC (0.78 g L−1 h−1 versus 0.015 g L−1 h−1, respectively).43,58
This represents the highest volumetric acetate production rate
achieved thus far via the MES process, that too merely optimizing two operational conditions and without electrode surface
modification. Consideration of other process parameters may
also further enhance the MES process. For instance, CO2 is
usually supplied by continuous bubbling in reactors, and due
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Green Chemistry
to its low solubility in aqueous medium and its low mass
transfer, only a small fraction of the total CO2 supplied during
the process is utilized by the microorganisms. An efficient
gas supply with improved mass transfer is required for any
real application considerations of MES. A gas diffusion electrode applied in MES by Bajracharya et al. has proved that
appropriate gas supply may potentially lead to improved MES
efficiency.56
• The anodic reaction on most of the MES systems has
been water oxidation thus far. Further research should thus
also be focused on identifying useful anodic conversions to
make the whole MES system productive.
• Importantly, further carbon chain elongation or product
selection other than acetate is desired for developing economically attractive MES processes. The application of synthetic
biology tools, metabolic engineering and adaptive evolution of
acetogens might warrant targeting higher carbon chain compounds in MES.26 By applying a certain set of operational conditions, it is also possible to divert the production pathways, in
particular, for mixed culture based MES processes, as recently
reported.17
5. Conclusions
This review summarizes the cathode materials that have been
used in MES for the synthesis of chemicals from CO2. Along
with the fundamental requirement of biocompatibility, it is
essential to develop high surface area, highly porous and good
conductive cathodes. Most of the strategies adopted to
improve the cathode–microorganism interactions were targeted mainly toward biofilm enhancement. Biocompatibility
and a high surface area were demonstrated to be required for
developing uniform biofilms on the electrode, especially for
pure culture biocathodes. The recent progress made with 3D
electrode configuration seems to be the most promising
material for MES processes. Further development of cheap and
efficient electrode materials will have a significant impact on
the scaling-up potential of the MES technology. Undeniably,
understanding the molecular mechanisms of electron transfer
between a surface with low redox potential and microbial cells
is necessary for further development of MES processes.
Conflicts of interest
The authors have no conflicts of interest to declare.
Acknowledgements
Nabin Aryal was supported by a FutureGas project from
Innovation Fund Denmark – Innovationsfonden. Sunil Patil
acknowledges the Alexander von Humboldt Foundation for the
financial support.
This journal is © The Royal Society of Chemistry 2017
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