Renewable Energy 98 (2016) 153e170

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Renewable Energy
j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m/ l o c a t e / r e n e n e

An overview on emerging bioelectrochemical systems (BESs): Technology for

sustainable electricity, waste remediation, resource recovery, chemical
production and beyond
a, b, 1 a, c, 1 a
Suman Bajracharya , Mohita Sharma , Gunda Mohanakrishna , Xochitl
a b c a, *
Dominguez Benneton , David P.B.T.B. Strik , Priyangshu M. Sarma , Deepak Pant
a Separation & Conversion Technologies, VITO e Flemish Institute for Technological Research, Boeretang 200, 2400, Mol, Belgium
b Sub-Department of Environmental Technology, Bornse Weilanden 9, P.O. Box 17, 6700 AA, Wageningen, The Netherlands
c Environmental and Industrial Biotechnology Division, The Energy and Resource Institute (TERI), Darbari Seth Block, Habitat Place, Lodhi Road, New Delhi, 110003,
India
article info abstract

Article history: Bioelectrochemical systems (BESs) are unique systems capable of converting chemical energy into electrical energy (and vice-
Received 12 January 2016 versa) while employing microbes as catalysts. Such organic wastes including low-strength wastewaters and lignocellulosic
Received in revised form 23 biomass were converted into electricity with microbial fuel cells (MFCs). Likewise, electrical energy was used to produce
February 2016 Accepted 2
hydrogen in microbial electrolysis cells (MECs) or other products including caustic and peroxide. BES were also designed to
March 2016
recover nutrients, metals or removal of recalcitrant compounds. Moreover, photosynthetic micro-organisms as well as higher
Available online 24 March 2016
plants were implemented to use solar energy for electricity generation. The diversity on microbial and enzymatic catalysts
offered by nature allows a plurality of potential applications. As compared to conventional fuel cells, BESs operate under
Keywords:
relatively mild conditions and do not use expensive precious metals as catalysts. The recently discovered microbial
Recalcitrant removal
Microbial electrocatalysis electrosynthesis (MES) of high-value chemicals has greatly expanded the horizon for BES. Newer concepts in application as
CO2 sequestration well as development of alter-native materials for electrodes, separators, catalysts along with innovative designs have made
Biosensors BES very promising technology. This article discusses the recent developments that have been made in BESs so far, with the
Value-added chemicals production emphasis on their various applications beyond electricity generation and resulting perfor-mances as well as existing
limitations.

2016 Elsevier Ltd. All rights reserved.

1. Introduction
There is a growing demand for new energy sources due to the limited
accessibility and pollution caused by the use of fossil fuels. At present, the
annual energy demand is approximately 13 terrawatts (TW) worldwide and it
is estimated to reach around 23 TW by the year 2050 [15]. Meanwhile,
intensive resource utili-zation in municipal, industrial and agricultural
activities will continue the process of environmental degradation creating
envi-ronmental threats of global warming and related consequences. In
* Corresponding author.
E-mail addresses: deepak.pant@vito.be, pantonline@gmail.com (D. Pant).
1
Equal contribution.
this context, the development of renewable energy sources has become crucial
for a sustainable landscape, especially by decreasing the dependency on
energy import and by diversifying energy production sources [147].
Bioelectrochemical systems (BESs) have considerably boomed over the past
decade for their contribution as an emerging sustainable technology for
concurrent electricity production and wastewater treatment [122]. In addition,
BESs also offer unique possibilities for clean and efficient produc-tion of fuels
and high-value chemicals using microorganisms [48]. As the BES functions in
a completely multi-disciplinary approach, a large quantum of research have
been conducted worldwide in the fields of microbiology, electrochemistry,
bioelectrochemistry, biotechnology, environmental science, materials science,
etc. In these electrochemical systems, the redox potentials of an oxidation
reaction at the anode and a reduction reaction at the cathode create

http://dx.doi.org/10.1016/j.renene.2016.03.002 0960-
1481/ 2016 Elsevier Ltd. All rights reserved.
154 S. Bajracharya et al. / Renewable Energy 98 (2016) 153e170

a potential difference which is the
driving force for electrons to flow
from a low potential to high
potential, spontaneously [137]. This
flow of electrons through an
external circuit is measured as
electric current. Whenever,
microbes or enzymes are involved
in the oxidation or reduction or both
reactions, the system is termed as a
microbial electrochemical system
(MXC) or in a broader term BES
[64]. If microbes catalyze the
anodic reaction, they are applied as
bioanode and if microbes catalyze
the cathodic reactions, they are
applied as biocathode. Microbial
fuel cells (MFCs) are a type of
MXC that generate electricity from
the degradation of organic matter in
anode chamber. A low redox
potential for the oxidation of
organic matter at the anode and a
high redox potential for the oxygen
reduction reaction (ORR) at the
cathode, typically results into
bioelectricity generation. In the case
of microbial electrolysis cells
(MECs), an external voltage is
applied to subject the cathode po-
tentials driving the production of
valuable chemicals [169]. The BES
in which CO2 or organic molecules
are cathodically reduced to higher
value organic molecules is called
microbial electrosynthesis (MES)
[144]. In addition, BESs have also
emerged with other ap-plications
such as microbial desalination cells
(MDCs) for the desalination of
water, and sediment or plant
microbial fuel cellsdwherein
microbes are intermingled with
plant roots for the electricity
generation [12,27,47]. Moreover,
BESs are also identified as efficient
bioreactors for the treatment of
recalcitrant pollutants and toxic
wastewaters; the process is termed
as bioelectrochemical treatment
(BET) or microbial
electroremediation [124].
In this direction, the present
review provides the overview of (i)
all types of BESs and their
applications, (ii) the basic working
principles involved, (iii) substrate
utilization, (iv) synthesis of tar-
geted chemicals and (v) the recent
concepts and developments made in
BES. This review emphasizes the
recent advances in BES that were
developed beyond electricity
generation. This review also helps
to attract the young researchers
from the allied disciplines of BES
to advance the technology with
multiple applications.
2. Types of bioelectrochemical
systems
Based on the desired end
objectives, BESs can be broadly
clas-sified into electrogenesis
systems, electrohydrogenesis
systems, microbial desalination
systems, microbial electrosynthesis
systems and bioelectrochemical
treatment systems. Each type of
BES with specific names as shown
in Fig. 1 are discussed in the
following sections.
2.1. Microbial fuel cells (MFCs)
MFCs harness electrical current
from the microbial oxidation of
organic matter using a solid
electrode as an electron acceptor
[143]. The anode surface of MFCs
facilitates microbial attachment and
oxidation of organics, thereby
generating electrons which are then
simultaneously transferred to the
cathode compartment via an
external circuit containing an
external load. Electroneutrality is
warranted by ions transport through
an ion-permeable medium or a
membrane while electricity is
produced in the process. The first of
such systems was demonstrated by
M.C. Potter in 1911, which
achieved a maximum voltage of
0.3e0.5 V [140]. Electroactive
bacterial biofilms developed on the
anode of BES function as the
electrocatalytic unit for electricity
generation. Production of
bioelectricity in MFC is directly
dependent on the capacity of
exoelectrogens (microbes
generating electricity) present on
the anode, which facilitate the
transfer of electrons from the
reduced substrate to the anode.
Oxidation of complex organic
matter in wastewater requires
diverse microbial communities.
Dozens of bacterial species have
been found of being able to produce
electric current. The Shewanella
and Geobacter species were earlier
identified as the electron-
transferring microbes and as such
well-studied. However, stable and
higher currents have been recorded
more often in MFCs with mixed
cultures in bioanodes, rather than
with pure cultures. The presence of
Geobacteraceae in the bioanode
community often showed high
power densities registered in MFCs
[86,101]. The highest current
density reported so far in MFC was
2 achieved as a result of low internal
390 A m obtained using mixed
culture at the layered-corrugated
carbon anode with high surface area
[19]. The nature of substrate, anode
potential and electrolyte chemistry
affect the microbial ac-tivity and
electron transfer [52,134]. Higher
electrolyte conductivity ascertains
the better performance of microbial
electrochemical systems but the
electrolyte conductivity should not
go beyond the tolerance level of
bacteria [168]. However, it was
identified that the application of
halophilic bacteria in BESs have
reported to produce the current
2
densities up to 85 A m with
bioanodes formed from a salt-marsh
inoculum and cultivated in a 1.5
times more saline electrolyte than
seawater [151]. Significant current
densities and power densities
obtained from MFCs, as reported in
various studies, are listed in Tables
1 and 2 respectively. The
performance of MFCs also relies on
the electrode material used and its
structure. Graphite electrodes with a
roughened surface have shown to
produce higher power densities than
flat graphite electrodes [189].
Likewise, increasing the surface
area of MFC anodes using porous
materials such as graphite brush,
carbon felt and carbon nanotubes,
have shown considerable increase
in current density [20,53,123].
Higher surface area of electrodes
provides a larger surface for
bacterial adhesion and electron
transfer between the bacteria and
electrode, thereby demonstrating
noteworthy improvement in current
den-sities. Direct electron transfer
phenomenon of microbes with
metal electrodes has also been
demonstrated including
dimensionally stable anodes (DSA,
titanium over iridium and tantalum
oxide), stainless steel and platinum
electrodes [44,139]. Current
densities obtained with porous
carbon anodes are typically higher
than those reported with metals
except for platinum [217]. A switch
from planar electrodes to three-
dimensional electrodesdhaving
opti-mized microstructuresdwas
correlated to a considerable increase
on bioelectrode performance [167].
Macrostructure modification in
anode, with multi-layered
corrugated carbon configuration evi-
denced a huge rise in current
densities [19]. Especially once mass
transport limitations are tackled by
flow-through electrodes, higher
current and power densities can be
resistances [170]. The relevance of
cathode materials in the power
densities obtained from MFCs is
demonstrated in Table 2 based on
the MFC studies reporting similar
anode materials. Cata-lysts e.g.
MnO2 coated air cathodes and
membrane and cloth electrode
assemblies as cathode in MFCs
reported higher power densities.
Materials used for MFC
construction, design and config-
uration influence the internal
resistance, which in turn govern the
total performance of the system.
2.2. Microbial electrolysis cells
(MECs)
MECs utilize the property of
bacteria to convert chemical energy
to electrical energy and allow
electrolysis of water [194]. External
power applied onto the electrical
circuit of BES drives electrons from
anode to the cathode and also
supports the hydrogen gener-ation
at the cathode [78]. Contrary to the
MFCs, the cathode of MECs
operates under anaerobic conditions
that facilitate hydrogen production.
However the anoxic environment in
MECs, along with high
concentrations of hydrogen
production, can also promote
and
methane production once CO 2
methanogens are available.
A few of the methods to
mitigate methane
production includes the
aeration of the cathode
chamber between batches,
lowering of the pH,
operation at short retention
times and giving a heat
shock to the inoculum, or
adding chemicals that
inhibit the growth of
 S. Bajracharya et al. / Renewable Energy 98 (2016) 153e170 155

Fig. 1. Schematic overview of various types of bioelectrochemical systems (BESs).

methanogens [23]. Hydrogen
production in MECs, according to
their configurations and the
substrates treated, are listed in Table
3. Higher electric currents are
typically observed in MECs, when
compared to MFCs, which is due to
the additional applied voltage that
helps overcoming the cathode
limitations in MEC [170]. The
energy required for MEC operation
can also be provided by another
separate MFC as a power source
[198]. This study reported a
hydrogen production rate of 0.24
3 3 1
m -H2 m d and energy re-covery
of 23% using a fermentation
effluent as substrate. However, for
the supply of a stipulated voltage
that allows for maximal hydrogen
production in MEC, efficiently
connected multiple MFCs are
required [198]. In a MEC with
bioanode and biocathode, expensive
metals like platinum are not
required as catalyst and preferably,
the enrichment of microbes on the
carbon cathode de-creases the start-
up time and produces comparable
current den-sities to those of
bioanode [78]. Furthermore, the
hydrogen synthesized in MECs can
also drive the biochemical
production of other chemicals
[144]. Most common examples of
reduction re-actions at the cathode
are proton reduction to hydrogen,
oxygen reduction to H2O2 and CO2
reduction to methane (CH4) and
acetate [23,26,158]. These recently
developed BESs for the production
of valuable chemicals and biofuels
such as organic acids, or alcohols
from low value compounds or CO2
[125,130,166] are deliberated in the
next section.
2.3. Microbial electrosynthesis
(MES)
MES, also known as
bioelectrosynthesis, is a new-
fangled perspective of BES which
utilizes the reducing power
generated from the anodic oxidation
to produce value added products at
the
cathode. Cathodic biocatalysts (with
attached cathodic biofilms) reduce
the available terminal electron
acceptor to produce value added
products [112,125,144]. The
bioelectrosynthesis process can be
highly specific, depending on the
biocatalyst catalyzing the redox
reaction and the terminal electron
acceptor involved in the process,
along with the electrochemically
active redox mediators or suitable
reducing equivalents. Biocathodes
are the key components of
microbial electrosynthesis, where
the electrode oxidizing mi-
croorganisms are involved in the
formation of reduced value-added
product such as acetate, ethanol,
butyrate [6]. MES refers to the
production of chemical compounds
in an electrochemical cell by
electricity-driven CO2 reduction as
well as reduction/oxidation of other
organic feedstocks using microbes
as biocatalyst [144]. As a proof of
concept [130] presented MES as a
microbial catalysis of CO2
reduction to multi-carbon organic
compounds using electrical current
at the cathode. As such, MES is also
prospected as an alternative strategy
to capture electrical energy in
covalent chem-ical bonds of organic
products. Several studies have
reviewed and highlighted different
aspects of MES including
microbiology, technology and
economics, as well as deep
understanding on the metabolic
routes involved, electron transfer
mechanisms and practical
considerations [41,143,144].
2.4. Enzymatic fuel cells (EFCs)
Enzymatic fuel cells (EFCs)
make use of specific enzymes on the
electrode surface (or in electrolyte
suspension) that facilitate the
catalytic oxidation of fuel and drive
specific reactions desired for
various applications. Davis &
Yabrough [37] demonstrated the use
of microbes and enzymes in biofuel
cells using glucose oxidase.
156 S. Bajracharya et al. / Renewable Energy 98 (2016) 153e170

Table 1
Overview of current densities reported in MFCs in connection to the type of microbial culture used and anode material.

Source inoculum Type of MFC and anode material/specifications 2 Reference

Current density (A m )
Geobacter spp. Two chamber/graphite sticks 0.065 [10]
Geobacter spp. Two chamber/graphite anodes at 0.2 V/AgAgCl 0.16e1.14 [10]
Anaerobic culture of Escherichia coli K12 2 5 [150]
Two-chambered MFC/platinum paddle electrodes (5 cm )
and ethanol as substrate
Anaerobic culture of Escherichia coli K12 2 50 [150]
Two-chambered MFC/platinum paddle electrodes (5 cm )
and formate as substrate
Pre-acclimated bacteria from MFC Cube shaped single-chamber MFC/graphite fiber brush 8 [100]
2 3
anode (7170 m m brush volume)
Mixed culture 2.5 ml anode chamber, bicarbonate buffer/Double cloth 9.9 [51]
2
electrode assemblies (CEAs); (2 7 cm projected electrode area),
Klebsiella pneumonie L17 Two chamber/Carbon felt 1.2 [216]
Rhodopseudomonas palustris DX-1 Single chamber/graphite brush 9.9 [206]
Geobacter sulfurreducens Single chamber/DSA at 0.2 V/AgAgCl 5 [44]
Geobacter sulfurreducens Single chamber/solid graphite at 0.2 V/AgAgCl 8 [44]
2

Geobacter sulfurreducens Single chamber/multiple stainless steel anode at 0.2 V/AgAgCl 2.4 [45]
Mixed culture Single chamber/Graphite plates projected surface area of 70 cm 0.27 to 0.35 [124]
Mixed culture 3D carbon fiber anode prepared by gas assisted electrospining; 30 [20]
anode polarised at 0.2 V/AgAgCl
Mixed culture Half-cell semi batch reactor/Layered corrugated Carbon 70e400 [19]
anode/polarised at 0.2 V/AgAgCl
Mixed culture from air cathode MFC 30 ml anode chamber/Double cloth electrode assemblies 16.4 [50]
2
(CEAs); (2 100 cm projected area);
Geoalkalibacter subterraneus Planar graphite electrode poised at 0.2 V/SCE; Saline 4.68 0.54 [14]
electrolyte 3.5% NaCl
Mixed culture 3D scaffold-NanoWeb reticulated vitreous carbon 68 30 [54]
electrode at 0 V/AgAgCl
Garden compost Carbon cloth, 0.2 V/SCE 33.5 [85]
Garden compost Stainless steel foam at 0 V/SCE 100 [85]
Geobacteraceae dominated secondary Ag sheet anode at 0.2 V/AgAgCl 11 [9]
mixed culture from wastewater Cu sheet anode at 0.2 V/AgAgCl
Geobacteraceae dominated secondary 15 [9]
mixed culture from wastewater
Geobacter sulfurreducens Ice-templated titanium based ceramic anode, 88% porosity 128.7 [115]
Mixed culture Carbonized corn stem 31.2 [84]

DSA: Dimensionally stable anode.

SCE: Standard calomel electrode.

Glucose oxidase has been widely used in pacemakers, indicator lights, small
actuators, micro pumps, and other glucose electro-oxidizing anode-based
systems, because of its thermostability and high selectivity [75]. Several
enzymes are used on anode and cathodes, based on their specific redox
function. If highly selective enzymes are used at the anode and cathode, this
eliminates the need of any membrane between the anode and cathode
compart-ments. However, enzymatic catalysts are usually reported to oxidize
the fuel partially and heat generation occurs as a result of side reactions,
which might be detrimental to the enzymatic ac-tivity [118,132]. The shelf
life of these enzyme-based systems has been extended through encapsulation
in micelle polymers that provide a buffering capacity for pH control and a
hydrophobic niche to prevent enzymatic degradation [118]. The flavin adenine
dinucleotide-dependent glucose dehydrogenases (FADGDH)/ Osmium (Os)-
polymer-based electrodes showed high sensitivity towards glucose and also
reported higher current densities, which made them suitable for use as
bioanodes in glucose based EFCs [211]. The Pyrroquinolinequinone-
dependent alcohol dehydroge-nase (PQQ-ADH), enzyme originating from
acetic acid bacteria, has been reported for the development of EFCs and
biosensors, as it can undergo quasi-reversible electrochemistry at an exposed
carbon surface [59,207]). This enzyme was reported to be capable of using
different redox mediators and also has a good electron transfer kinetics [207].
Higher energy densities in combination with lower power outputs make EFCs
suitable for independently powering the wireless sensor applications such as
video monitoring and also for the development of other portable power
devices [7,59]. The use of FAD-dependent fructose dehydrogenase, obtained
from Glucono-bacter, as an anodic catalyst, and copper containing laccase
from
mushrooms, have been evaluated as cathodes, showing a high turnover rate,
good stability and high selectivity [83,211]. Multi-enzyme based EFCs are
generally preferred over single enzyme systems so as to increase the substrate
conversion and the perfor-mance of the system as a whole [118]. Many
studies are now focusing on cascade of enzymes in FECs to facilitate complex
mechanisms and 3-D electrode configurations to provide ample surface area
for enzymatic reactions. However, due to the utiliza-tion of purified enzymes
with catalytic capacity, the cost for EFCs are still high.
2.5. Microbial solar cells (MSCs)
Microbial solar cells (MSCs) make use of photoautotrophic microbes or
higher plants to entrap solar energy which is further utilized by electroactive
bacteria to perform electrode-driven reactions. These reactions include
generation of electric current or compounds like hydrogen, methane, ethanol,
hydrogen peroxide etc. Primarily photosynthesis leads to the generation of
organic compounds, which are subsequently fed into the anode compartment
where they are oxidized by electroactive microbes to produce electrons. These
electrons are then transferred to the cathodic side where reduction of oxygen
leads to the formation of water [46]. The phototrophic biofilms developed on
the anode contain species of cyanophyta including Synechocystis, chlor-
ophyta and other electroactive microbes [182]. A system for treatment of algal
blooms in lakes has been reported based on MSC principles, where algal
biomass provided by Microcystis aeruginosa and Chlorella vulgaris was fed
along with lake water, for concomitant
as a substrate in MFCs
power production and
 S. Bajracharya et al. / Renewable Energy 98 (2016) 153e170 157

Table 2
An overview of power densities reported in MFCs in connection to cathode material.

MFC design Anode Cathode Maximum power Reference

2
density (mW m
projected cathode)
MFCs with carbon paper, carbon cloth and similar anodes
Single chamber Toray carbon paper (without MEA with Pt catalyst; PEM-carbon 262 10 [94]
wet proofing; E-TEK) clothes assemblies
Dual chamber Plain carbon paper Aqueous air-cathode; Carbon paper 33 (anode area based) [102]
with platinum catalyst
Single chamber Carbon cloth (type A, E-TEK) Air-cathode; Carbon clothes, PTFE 766 [24]
(diffusion layer)
Single chamber air-cathode Carbon cloth Double Cloth Electrode 4300 [50]
Assemblies (CEA) 3
9.8 W m
Miniatured tubular MFCs Untreated carbon veil Air cathode; untreated carbon veil; [203]
MFCs with granular graphite and similar anodes 83 11 W m
3
Open air biocathode with granular graphite Sludge biocathode; graphite [29]
tubular MFC configuration felt with MnO2 total electrolyte
Dual chamber Graphite granules Aqueous air cathode without catalyst; 5.88 (nominal cathode [56]
granular graphite with nano pores surface area based)
Dual chamber Graphite granules Sludge biocathode; graphie fiber brush 3 [210]
68.4 W m anolyte
Tubular air-chamber MFC Graphite felt and graphite granules MEA; Canvas cloth with Ni and 86.03 [221]
MnO2 coating
Tubular air-chamber MFC Graphite felt and graphite granules MEA/Canvas cloth with graphite 24.67 [221]
and MnO2 coating
Tubular air-chamber MFC Graphite felt and graphite granules b-MnO2 catalyzed air cathode 172 7 [215]
Two chambered MFC Carbon granules anode; acetate Activated nitrogen-doped 1377 46 [208]
fed mixed culture carbon fiber cathode

MFCs with carbon and graphite brush anodes

Tubular cathode in single
chamber configuration
Single chamber MFC
Single chamber
Two chamber MFC
Single chamber MFC
Single chamber MFC
MFCs with carbon felt anodes
Plain graphite fiber brush MEA/ultrafiltration membrane; 3
18 W m [222]
graphite coating with CoTMPP catalyst total electrolyte
Graphite fiber brush MEA; Ion exchange membrane-graphite 449 35 [223]
coating and CoTMPP catalyst; AEM
Graphite fiber brush treated Air cathode; stainless steel mesh 1610 56 [213]
with ammonia gas and Nafion binder with diffusion layer 3
3.3 W m
Carbon brush anode Crumpled graphene cathode [205]
carbon fiber brush anode Goretex diffusion layered carbon 1330 30 [108]
cloth cathode
carbon fiber brush anode; PTFE diffusion layered carbon 1390 70 [108]
acetate fed mixed culture cloth cathode
 Two chamber upflow MFC Carbon felt Aqueous air cathode; activated 315 (cross-sectional [40]
carbon fiber felt area of separator)
Tubular air-cathode MFC Graphite felt A tubular air-cathode; non-Pt; 175.7 [220]
continuous MFC stack with
swine wastewater
Single chamber MFC carbon felt anode Manganese dioxideegraphene nano 2083 [201]
sheet (MnO2/GNS) air cathode
MFCs with graphene coated anodes 3.6 W m
3
Two chamber MFC Crumpled graphene anode Carbon brush cathode; [205]
Two-chamber MFC Graphene coated stainless with Carbon cloth cathode with 2143 [70]
steel fiber felt anode; Acetate ferricyanide catholyte
fed mixed culture
Two-chamber MFC Graphene coated carbon cloth Carbon cloth cathode with 1018 [70]
anode (acetate fed mixed culture) ferricyanide catholyte

CoTMPP: Cobalt tetramethylphenylporphyrin.

MEA: Membrane electrode assembly.
water treatment [200]. The algal
biomass from photo-
bioreactordafter the treatment in an
anaerobic digester, can be used as a
feed for the fuel cell [38]. A MSC
with a photobioreactor using
Chlorella at the anode, reached a
light to electricity con-version
efficiency of 0.04% resulting in 14
2
mW m of average power density
[182]. Without mediator or carbon
source in the anolyte, Synechocystis
PCC6803 was reported to produce
2 by electro-active microbes [180].
539 mA m , under higher light
intensity (10,000 lux) and resulted
on effective CO2 sequestration (625
3 transforming it into green electricity
mmol CO2 m ) [109].
Improvement of performance is
possible by photo-bioreactor
optimization, improved chemical
energy transfer from algae to
bioanode, higher surface electrode
area and enriched electroactive
biofilm [181]. The advantages of
this system lie on simultaneous
CO2 sequestration and direct
conversion of light to
electricity [109].
2.6. Plant microbial fuel cells
(PMFCs)
Plant microbial fuel cells
(PMFCs) incorporate the living
plant's root system into the MFC
anode so that the organic products,
called as rhizodeposits, released to
the soil by the roots, can be used as
substrate for electricity production
Hence, in a broader sense, PMFCs
harness solar radiation by
in a clean and efficient manner. The
rhizodeposits from the roots mainly
comprise exudates (sugars, organic
acids), secretions (polymeric
carbohydrates and enzymes),
lysates (dead cell materials) and
gases [180]. The choice of a plant
for PMFC is crucial, as it directly
158 S. Bajracharya et al. / Renewable Energy 98 (2016) 153e170

Table 3
An overview of experimental conditions and performances of hydrogen producing MEC with mixed culture biocatalyst.

BES specifications and anode/cathode Hydrogen Current Electric Efficiencies and Reference
material production rate density energy input recovery in %
3 3 1 2 3
(m H2 m d ) (A m ) (kWh m H2)
A) Bioanode and abiotic cathode
Two chamber; Graphite felt anode; 0.1 0.447 NA 53 3.5% overall efficiency [154]
TiePt cathode; 0.5 V applied voltage
Single chamber; Graphite brush anode; 3.12 11.6 NA 78% overall efficiency [11]
carbon cloth with Pt coating cathode;
0.8 V applied voltage
Two chamber; graphite felt forced flow 5.6 16.4 NA 43% overall, 71% [172]
through anode; PteTi mesh cathode; cathodic H2 recovery
1 V applied voltage
Cloth separator; carbon felt anode; 6.3 4.7 NA 90% COD recovery [188]
carbon cloth cathode with Pt coating;
1 V applied voltage
Two chamber; graphite felt; nickel foam; 50 22.8 2.62 90% cathodic H2 recovery [80]
1 V applied voltage
Single chambered cube MEC; Graphite 7.9 0.3 33.28 4.7 0.5 40 1% overall efficiency [128]
brush anode at 0.2 V/AgAgCl; Pt coated
carbon cloth cathode
Single chambered cube MEC; graphite 6.9 0.8 26.08 2.9 0.4 54 5% overall efficiency [128]
brush anode at 0 V/AgAgCl
Single chambered cube MEC;graphite brush 3.6 0.6 14.6 2.3 0.3 58 6% overall efficiency [128]
anode at 0.2 V/AgAgCl [25]
Single chamber; graphite fiber brush anode; 17. 8 26.14 NA ~80% overall efficiency,
Pt coated carbon cloth; 1 V applied voltage 93% cathodic H2 recovery
Two chamber MEC with AEM; Carbon NA 10.2 2.62 90% cathodic H2 recovery [171]
felt anode; 1 V applied voltage
Wastewater feed 100 L reactor with 6 0.006 NA NA 48.7% energy recovery; [67]
MEC cassettes; 2 carbon felt anodes in 41.2% CE
each cassette; stainless steel wool cathode;
1.1 V applied voltage 3
150 A m
Glycerol, milk and starch feed single chamber MEC; 0.94 NA 91% cathodic H2 recovery [126]
graphite fiber brush anode; Pt coated graphite
fiber cloth cathode; 0.8 V applied voltage;
enriched anaerobic sludge inoculum
H-type reactor; Spent yeast and ethanol fed MEC;; 2.18 0.66 222 31.3 NA 87 2% COD recovery, [173]
3 71 4% CE
Graphite fiber brush anode at 0.3 V/AgAgCl; Am
Stainless steel mesh cathode;pig manure inoculum
B) Biocathodes and abiotic anodes 1.2
Continuous mode double chamber reactor; 0.63 NA 49% H2 recovery [157]
graphite felt cathode at 0.7 V/SHE 2.2 2.7 50% H2 recovery [79]
Continuous mode double chamber reactor;
graphite felt cathode at 0.7 V/SHE 2.5% H2 recovery [114]
Double chamber reactor; graphite granules 2.5 NA NA
cathode at 0.59 V/SHE; autotrophic biocathode 376.5 mmol 1.28 NA 70% H2 recovery [57]
Double chamber reactor; plain carbon cloth
cathode at 0.8 V/SHE; autotrophic m2d1
thermophilic biocathode
Double chamber reactor; graphite plate cathode; 9.2 L m 2 d 1 1.88 NA 39.4% electron recovery as H2 [82]
autotrophic biocathode at 0.75 V/SHE 3 NA 81% energy efficiency,
205 A m
Single chamber PANI/MWCNT modified carbon 0.67 [21]
cloth biocathode; 0.9 V applied voltage 42% H2 recovery, 72% CE
NA: Information not available; PANI: Polyaniline; MWCNT: Multi-walled carbon nanotube; CE: Coulombic efficiency; COD: Chemical oxygen demand.
controls the amount of
rhizodeposits for bioelectricity
genera-tion. Reed manna grass
[180], rice plants [39] and Spartina
anglica [69] have been utilized in
separate studies. PMFCs from
Pennisetum setaceum have been
reported to be the most sus-tainable
in terms of power production so far,
with a maximum power generation
2 system in combination with MFC
of 163 mW m [27]. S. anglica
PMFCs with integrated oxygen
reducing biocathodes reached the
highest long-term (2 weeks) power
2 compartments, for water desali-
output of 240 mW m [202].
PMFCs along with MSCs having
phototrophic biofilms are
considered a promising and novel
energy harvesting systems. It was
also identified that the total amount
of rhizodeposits available for
oxidation at anode is directly
proportional to bioelectricity gen-
eration, rather than the
photosynthesis process occurring in
the plant [191].
2.7. Microbial desalination cells
(MDCs)
Microbial desalination cells
(MDCs) utilize the electric potential
difference developed across the
anode and the cathode via MFC
technology to operate in situ
desalination. Cao et al. [12]
reported the first water desalination
technology. MDCs comprise an
additional middle compartment in
between the anode and cathode
nation. The middle compartment is
partitioned by an anion ex-change
membrane (AEM) towards the
anode and a cation exchange
membrane (CEM) towards the
cathode. Bacteria on the anode
oxidize biodegradable substrates
and generate electrons and pro-tons;
the electrons are externally
transferred to cathode whereas the
anions (e.g., SO24 , Cl ) in the
desalination compartment migrate
to the anode and the cations (e.g.,
K, Na) are transferred
S. Bajracharya et al. / Renewable Energy 98 (2016) 153e170 159

to the cathode to maintain charge
neutrality, thereby, desalination of
the middle chamber solution occurs
[12,106,107]. In MDC, the
migration of ions from the saline
water in the middle chamber
towards the anode and cathode
increases the conductivity of the
anolyte and catholyte. Thus,
electrical power production in
MDC has been improved due to
higher conductivity and mass
transfer. However, the increased
salinity of water could adversely
affect the anodic/cathodic bacteria
as well as the effluent water quality
from MDC [107]. The MDC can be
operated for simultaneous organic
and salt removal with power
production or can be combined to
the conventional reverse osmosis
(RO) process as a pretreatment for
lowering the salinity of feed
solution, and to decrease energy
consumption. Studies have
estimated that an MDC can
generate up to 58% of the electrical
energy needed by downstream RO
systems [76]. Jacobson et al. [76]
compared RO systems that use 2.2
kWh energy to desalinate 1 m of
3
seawater with MDCs, that can
produce 1.8 kWh of electric energy,
with a net benefit of 4 kWh by
3 applied only to treat the sludge from
treating 1 m of seawater. When an
MDC is operated in electrolysis
mode for hydrogen production at
the cathode, 180e231% surplus
energy than the input electricity can
be recovered as H2, with the added
advantage of water desalination
[106,117].
3. Wastewater treatment in BES
Bioelectricity generation has
been the primary outcome from the
MFC technology. Apart from this,
several other advantages are
associated with BES technology.
Wastewater treatment is one of the
most important applications of
BES. Current processes for biolog-
ical treatment of low concentrated
wastewaters are based on the
energy intensive conventional
technologies which are not envi-
ronmentally friendly. New
approaches of wastewater treatment
enabling substantial energy
recovery are the most effective way
to compensate the huge amount of
energy consumed in conventional
wastewater treatments. BES
associates the benefit of wastewater
treatment from diverse origin and
energy and resource recovery
through the production of
bioelectricity or other valuable
products [133]. Conventional
activated sludge process in
domestic waste-water treatment
3
needs 0.3 kWh m for aeration and
about twice of this amount of
energy for the pumping and other
purposes [116]. Energy can be
recovered from domestic
wastewaters via anaerobic
conversion of organic components
to methane. But only a portion of
the potentially available energy is
recovered through the com-bined
anaerobic digestion and
conventional aerobic wastewater
treatment. The energy contained in
the dissolved organic fraction is lost
in the aerobic oxidation processes.
If anaerobic digestion is used in
place of an aerobic process
(activated sludge treatment), energy
recovery as methane is possible but
still the requirement of concentrated
waste stream >3 kg m
3
organic
load and the main-tenance of
warmer temperatures >20 C are the
main limitations [103]. Also very
large digesters are required to make
the process economical. Due to
these reasons anaerobic digestion is
wastewater and high strength
wastewaters, but not low strength
wastewater. When BESs are used
for treating the wastewater, only
small amounts of solids (sludge) are
produced. Therefore, there is no
need of additional sludge
management and treatment
strategies. Direct electricity
generation from wastewaters in
MFC can attain high energy
efficiencies due to the absence of
carnot cycle limitations in power
generation unlike in combustion
processes [103]. However, the
energy recovery from BES still
remains low. Power densities
produced in MFCs using only
domestic wastewater has attained
3 decolorization.
up to 12 W m [65] which is
3
equivalent to 0.07 kWh m
produced over 6 h (6 h is typical
activated sludge treatment time).
However, this energy recovery is
still low as the organic waste in
domestic wastewater can poten-
tially produce up to around 2 kWh
3 and food industries. Industrial
m based on the methane gas
that could be generated in anaerobic
digestion.
A prediction of the economic
gain from the scaled up MFCs
treating wastewater concluded that
although electricity generation will
not rationalize the MFC operation,
the organic waste removal is more
attractive with this more sustainable
technology [55]. In this context, it is
more realistic to utilize wastewaters
as the source of energy and
materials for valuable chemical
production in-situ in MEC/MESs
[103]. Production of hydrogen or
hydrogen peroxide in MECs with
wastewaters as the source of
electrons is energetically beneficial
as compared to the production via
conventional elec-trolysis or other
means, because the energy
contained in waste-water is further
used in the production of chemicals
[103]. But as an exception, in a
comparative experimental study
between MFC and MEC, Cusick et
al. [34] showed that the treatment
efficiency in terms of chemical
oxygen demand (COD) removal
and the energy recoveries in terms
1
of kWh kg -COD were higher for
MFCs than MECs with winery and
domestic wastewaters. Eventually,
utiliza-tion of BES technology for
the treatment and recovery of
energy and chemicals from lower
value wastes may become
environmentally and economically
beneficial. An estimate of hydrogen
production cost of $4.51/kg-H2
from winery wastewater and
$3.01/kg-H2 from domestic
wastewater was reported when both
wastewaters were treated in MEC;
these costs of hydrogen production
were less than the estimated market
1
value of hydrogen ($6 kg -H2)
[34].
4. Recalcitrant pollutants
degradation in BES
4.1. Dye decolorization and
removal
Azo dyes, most of which are
xenobiotics, contain one or more
azo groups (-N]N-), and are the
most widely used synthetic dyes in
textile, leather, cosmetics, plastics
wastewaters containing dyes creates
environmental problems due to their
persistent colors which spoil the
aesthetic values and causality to
toxic effects [127,193]). The
contamination of azo dyes in
surface water hampers light
penetration and decreases the
amounts of dissolved oxygen,
thereby threatening the aquatic life.
Studies have shown that azo dyes
are toxic and mutagenic [164,192].
Dyes are designed to be chemically
and photolytically stable and are
also not easily degradable to natural
microbial action. Due to their
complex chemical structures, the
decolorization of these wastes is a
challenging task. A range of
physicochemical treatments exists
to decolorize effluents containing
dyes. Namely,
(i) chemical treatments like
ozonation [31], alkalinisation etc.;
(ii) physical treatments like
adsorption, flocculation-coagulation
etc.; (iii) photo degradation; (iv)
membrane processes [111] and (v) a
few biological treatments [89] can
effectively decolorize the in-dustrial
wastewaters. But these techniques
are generally very expensive
because they require large amounts
of chemicals and additionally
produce considerable amounts of
sludge.
Bioelectrochemical systems are
successfully proven to decol-orize
the dyes [33,127,186]. The range of
the half-cell potentials for the
reduction of azo dyes to their
constituent aromatic amines was
reported to be between 530 and 180
mV versus the standard hydrogen
electrode (vs SHE) [193]. Sun et al.
[186] carried out the decolorization
of active brilliant red X-3B
(ABRX3) utilizing the electrons
generated from the biodegradation
of readily biode-gradable organic
matter at the anode of air-cathode
single-chamber MFC with
concurrent bioelectricity generation.
Glucose and con-fectionery
wastewaters were found to be
suitable co-substrates for ABRX3
ABRX3
decolorization was significantly
improved in MFCs as compared to
conventional anaerobic treat-ment.
Mu et al. [127] used BES to
decolorize acid orange 7 (AO7)
abiotically in the cathode, using
acetate as the electron donor at the
bioanode. AO7 decolorization rates
3 1
up to 2.64 0.03 mol m d
160 S. Bajracharya et al. / Renewable Energy 98 (2016) 153e170

Fig. 2. Possible mechanism of Acid Orange 7 reduction in bioelectrochemical systems. Adapted with permission from (Mu et al. [127] Copyright (2009). American Chemical Society.

were achieved with simultaneous power generation, whereas the
decolorization rate was enhanced five times when power was supplied to the
BES maintaining the cathode potential at 400 mV (vs SHE). The identification
of decolorization products suggests the cathodic reaction mechanism depicted
in Fig. 2.
Alizarin yellow R (AYR) was decolorized in a dual-chamber BES with a
biocathode of enriched autotrophic biodegrading inoculum [33]. Within 48 h
of operation under the optimized condition of pH 5.2, and 0.5 V of supplied
voltage, the decolorization efficiency was as high as 99.2% (from initial
1 chlorinated aliphatic hydro-carbons (CAHs) in groundwater, by using them as
concentration of 100 mg L ), which was higher than the efficiency obtained
from abiotic and mixed sludge-inoculated biocathode operations.
4.2. Organochlorine removal
Organochlorines are organic compounds containing at least one covalently
bonded chlorine atom. Many derivatives of or-ganochlorines persist in the
environment and have been found toxic to plants and animals, including
humans. Industrial chlori-nated solvents, bleaching and preservative agents
and chlorine-containing pesticides are the main anthropogenic source of
recalcitrant organochlorines. Improper handling and disposal of industrial
solvents and degreasing agents such as per-chloroethene (PCE) and
trichloroethene (TCE) contaminate the soil and groundwater. The physico-
chemical technologies to treat these subsurface pollutants are normally very
expensive. Natu-rally existing anaerobic microorganisms can decay and
detoxify the chlorinated pollutants via in situ bioremediation processes and
restore the contaminated soil and groundwater effectively and inexpensively
[105]. A brief list of the removal of organo-chlorines through different types
of BES, is overviewed in Table 4. Anaerobic bacteria can dechlorinate
terminal elec-tron acceptor for microbial respiration [165]. Incomplete
dechlorination of PCE and TCE to the interemediate cis-dichloroethene (cis-
DCE) and then to vinyl chloride (VC) gener-ally occurs in halorespiration.
VC is a singly chlorinated ethene and a known carcinogen. Chlorinated
compounds (PCE, TCE and cis-DCE) reducing microorganisms compete for
electrons in ace-tate and hydrogen intermediates with sulfate, iron (III), and
CO2 reducers [165]. Generally hydrogen (H2) is considered as ultimate
electron donor for reductive dechlorination by Desulfitobacterium

Table 4
BESs for dechlorination of trichloroethene and other chlorinated compounds.
Compound BES Electrode Operating mode Removal rate Reference
3 1
(mol m d )
Trichloroethene Mediator- Methyl Viologen Glassy carbon cathode, Batch fed 0.001 [2]
platinum disk anode 1
25 mmol d
Trichloroethene Direct graphite electrodes Batch [184]
Trichloroethene Direct Carbon paper [1]
Trichloroethene Undetectable mediator Glassy carbon cathode, Batch fed 0.002e0.004 [3]
platinum disk anode 1 1
64 2 mmol L d
Trichloroethene Direct Graphite cathode [4]
4-chlorophenol MFC; acetate in anode, Carbon fiber anode Batch fed 0.3 [61]
4-chlorophenol in and cathode
abiotic cathode
1,2-dichloroethane MFC; Dichloroethane in anode Graphite plate Recirculated 0.061e0.068 [138]
Ferricyanide in cathode anode and graphite anode and batch
granule cathode fed cathode
2-chlorophenol MEC acetate in anode, Graphite granule anode Batch fed 0.04 [183]
2-chlorophenol in biocathode and cathode
S. Bajracharya et al. / Renewable Energy 98 (2016) 153e170 161
spp and Dehalococcoides spp. [43,96,209]. But acetate and H2, solely or in
combination, were identified as key electron donors to stimulate anaerobic
microbial dechlorination of chloroethenes to ethene at the chloroethene-
contaminated site [66]. When ac-etate or H2 alone was the electron donor,
syntrophic acetate-oxidizing species or H2/CO2 acetogens respectively were
present as the co-culture. Certain dechlorinating bacteria were discovered to
be able to accept electrons directly from polarized graphite electrodes to
sustain the dechlorination process [1,184]. These findings have led to the
development of BESs for groundwater remediation. TCE-dechlorinating
bacteria can directly gain the required electrons from a negatively polarized
carbon paper electrode [1]. Aulenta et al. [4] investigated the performance of
TCE dechlorination in bioelectrochemical reactor operating for about 570
days at different cathode potentials ranging from 250 mV to 750 mV vs SHE.
At a cathode potential of 250 mV vs SHE, methanogenesis was almost
suppressed and 94.7% of available electrons were accounted for
dechlorination, whereas at the cathode potential below 450 mV vs SHE, a
1 1
higher TCE dechlorination rate up to 64 2 mmol L d was achieveddbut
simultaneous methanogenesis was reported consuming about 60% of electric
current [4]. BES for dechlorina-tion has shown stable and reproducible
performance even in the absence of organic carbon sources confirming long-
term direct exocellular electron transfer [1,4]. Studies have also been carried
out to demonstrate the dechlorination of other chlorinated compounds in the
BES including the dechlorination of chlor-ophenols and 1,2edichloroethane
[74].
4.3. Sulfide removal
Organic wastes and wastewaters generated from many pro-cesses
ubiquitously contain sulfur compounds. Biological conver-sion of sulfur
compounds in the wastewaters by sulfate reducing bacterial releases sulfides,
which are toxic, odorous and corrosive. Sulfate reducing bacteria like
Desulfovibrio desulfuricans are commonly found in the wastewaters
containing high organic load. Treatment of sulfate-rich wastewaters with
biological sulfate reduction processes is a well-known effective method but
the treatment process is limited due to the generation of sulfides and other
sulfur-based gases which inhibit the bacterial metabolism and even cause the
failure of the process, associated to the corrosive and toxic nature of the
sulfides [219]. MFCs can be used to remove sulfides by oxidizing them
electrochemically at the anode and, in
parallel, power can be generated [62,145]. As per the reactions mentioned in
Eqs. (1) and (2) and also according to Fig. 3, sulfate was biologically reduced
to sulfide which was then catalytically oxidized to sulfate using different
anodes such as a metal hydroxide-modified graphite [62], charcoal [32],
graphite foil, car-bon fiber veil and activated carbon cloth [219]. In these
studies, oxygen was reduced at the air-cathode to maintain the electron flow
through the external circuit.
D:desulfuricans Anode
Sulfate Sulfate
Sulfide
!
Biocatalytical reaction reaction
! Electrochemical
(1)
Sulfate Paracoccus spp Paracoccus spp anode (2)
! Sulfide ! Sulfur
Rabaey et al. [145] reported sulfide and sulfate removal from the
wastewater, as solid sulfur accumulation on the granular graphite anode of the
MFC, with the ferricyanide redox couple for the cathodic reaction. The
biocatalysts identified in this anaerobic oxidation of sulfide were Paracoccus
species. In this process, sulfide was shuttling the electrons between the
bacteria and anode, un-dergoing an oxidation to insoluble elemental sulfur. In
1 1
the tubular MFC with air-cathode, at most 514 mg sulfide L day (unit
normalized to net anodic compartment volume, NAC) was removed via
biocatalytical oxidation to elemental sulfur that resulted elec-tricity generation
1
which accounted maximum power outputs of 101 mW L NAC [145].
Activated carbon cloth was identified as a superior anode material for sulfide
oxidation to sulfate, when compared to graphite foil and carbon fiber, and it
2
enabled to extract higher electric power density (0.51 mW cm ) in the batch
mode operation of a single-chambered, air-cathode MFCs, using sulfate-rich
solutions [219]. Oxidation of solid sulfur to sulfate requires a high positive
overpotential, whereas sulfide can be oxidized to elemental sulfur when the
anode potential is controlled at or above 0.27 V (vs SHE) in aqueous solutions
at neutral pH (Fig. 3). In the sulfide removing MFCs, elemental sulfur and/or
soluble polysulfide species were the dominant sulfide oxidation products in
the anode chamber [219].
4.4. Chromium removal
Reduction of hexavalent chromium Cr(VI) at the cathode of MFCs has
high utility in the bioremediation of Cr(VI) contaminated
Fig. 3. Pathways of sulfide/sulfate removal in MFCs. Reactions 1 is biological metabolism in sulfur reducing bacteria (SRB); Reactions 2 and 3 are chemical in nature.
162 S. Bajracharya et al. / Renewable Energy 98 (2016) 153e170

sites, as the technology has low cost
of operation, self-regenerating
ability and also provides a
sustainable power supply [74].
Cr(VI) can be electrochemically or
biocatalytically reduced to less
toxic, less soluble and less mobile
trivalent chromium Cr(III). Acidic
envi-ronment is required at the
cathode for the electrochemical
Cr(VI) reduction in abiotic
condition [199]. Several bacterial
species of Bacilli and Clostridia as
well as a number of proteobacter
species such as Pseudomonas
dechromaticans, Escherichia coli,
Desulfovibrio vulgaris, Shewanella
oneidensis, Aeronomas
dechromatica and
Enterobacter cloacae were reported
to catalyze Cr(VI) reduction
whenever a suitable carbon source
like acetate was available to the
biocatalysts [18,187]. The reduction
of Cr(VI) was also attained in an
air-bubbling-cathode MFC in which
the electrochemical reduction of
oxygen to H2O2 strongly favored
the reduction of Cr(VI) [95].
Improvement to the biocathode for
Cr (VI) reduction and electricity
generation was reported by [73]
using tubular MFCs in which the
cathode to anode surface area ratio
of 3:1 was maintained. Specific
rates of Cr(VI) reduction between
1 two electron acceptors V
12.4 and 20.6 mg g volatile
1 Cr
suspended solid (VSS) h were
achieved with power generation
3 makes it sustainable and
from 6.8 to 15 W m using a
graphite-fiber as cathode support for
the biocatalyst. The graphite fiber
biocathode showed better per-
formance for chromium reduction
when compared to graphite felt or
graphite granules [73]. The rate of
Cr(VI) reduction and elec-tricity
generation in MFCs were affected
by various physicochem-ical and
biological conditions, like pH,
redox mediators and the bacterial
electrochemical activity. In
addition, the anode potential,
electrode materials and reactor
configurations also influenced the
efficiency of the Cr(VI) reducing
biocathode [74].
5. Metal and nutrient recovery in
BES
Application of MFCs has not
been limited only to the wastewater
treatment and electricity generation,
it has also expanded to electricity-
driven production of number of
value-added compounds such as
H2, acetate, etc. at the cathode [63].
MFCs have also been applied for
the removal and recovery of metals
from leachates and effluents from
mining and metallurgical processes
that would pref-erably result in the
recovery of metals especially
copper for (re-)use in industries
[63]. A subsequent study by Ter
Heijne et al. [68] demon-strated the
electrochemical reduction of copper
at cathode, using
bioelectrochemical acetate
oxidation at the anode. In this bio-
electrochemical process, a bipolar
membrane (BPM) was used for
simultaneous bioelectricity
generation along with copper
reduction/ removal at the cathode.
The reduced copper was plated onto
a flat plate graphite electrode at a
2
current density of 3.2 A m . Further
studies accomplished higher current
densities in the range of 0.9e7 A m
2 formation at the cathode occurs
along with copper removal by
using a larger anode surface than
the cathode surface [119,212].
Zhang et al. [214] validated the
recovery of vanadium (V) and
chromium (Cr) in dual chambered
MFCs by employing vanadium and
chromium-containing wastewater as
the cathodic electron acceptor with
simultaneous bioelectricity genera-
tion. The maximum power density
2 energy input when compared to
of these MFCs was 970 mW m
and showed enhanced electrode
reduction efficiency by using the
5 operation has shown promising
and
6 compounds
together [214].
Apart from metals, nutrient
recovery was also observed with
MFCs. Particularly, successful
ammonium (NH 4) recovery from
urine was demonstrated by Kuntke
et al. [90]. The electrons required
methane. On COD basis, H 2
for the migration of NH 4 from
anode to cathode are generated by
the anodic bacteria from the
oxidation of organic matter. At the
cathode, diffusion of ammonia
(NH3) promotes the total
ammonium trans-ported to the
cathode. Due to the localized high
pH prevailing in the cathode, NH3
stripping occurs and thus improves
the transport of ammonium. The
ammonium recovery rate and
current density were registered as
1 2
3.29 g-N d m (vs membrane
2 electrochemical
surface area) and 0.50 A m (vs
membrane surface area),
respectively and the process
V is required for H2 production in
produced a surplus energy of 3.46
1 MEC, which is less than the typical
kJ gN which was more than the voltage (>1.6 V) required for water
required energy for the ammonium electrolysis [98,99]. A mem-brane
recovery by stripping [90]. separates the anode and cathode
chamber to avoid the mixing of the
substrate and product. The reactions
6. Production of chemicals in
that occur in a MEC with acetate as
BES
substrate are as below.
6.1. Hydrogen
Wastewaters from industrial,
agricultural and municipal sources
contain large amounts of dissolved
organic matter that are a po-tential At anode :
resource for chemical and fuel CH3COO 4H2O/2HCO3 8e
production [155]. Biological
At cathode :
treatment technologies are known 8H 8e /4H2 or 8H2O 8
for the production of energy from
8OH
wastewaters. Methanogenic
anaerobic digestion has already (4)
been used worldwide for the
production of biogas (a mixture of Theoretically, hydrogen
methane and CO2). Hydrogen
after overcoming the endothermic
production from wastewaters by
barrier of 0.414 V vs SHE by
acetogenic fermentation is another
applying only a small external
method of utilization of
voltage difference of 0.14 V to the
wastewaters [120,121]. However,
low yields and thermodynamic MEC, the oxidation reaction carried
limitations in microbial metabolism out by the anodic bacteria can
exist in the fermentation process. supply the remaining overpotential (
BESs offer an alternative 0.279 V) [98,154]. Concom-itant
technology to upgrade the hydrogen wastewater treatment and H2
yield at a relatively low electric production in MEC is an effi -cient
conventional water electrolysis;
approach to generate clean
more specifically, MEC mode of energy. The utilization of a
wide range of organic
rates of hydrogen production. This
by
technology is also termed as bio-
electrohydrogenesis exoelectrogens in MECs
[97,136,152,156]. Hydrogen is
extensively used both as chemical
and fuel, in various industrial economically advantageous.
processes such as upgrading fossil However, the hydrogen
fuels and saturating fats, hence H 2 evolution reaction (HER)
has unique values compared to
occurs very slowly on
production from wastewater is 7
carbon cathodes of MEC and
times more valuable than methane need to overcome a high
produced from the same amount of endothermic po-tential
wastewater [155]. H2 production in barrier (overpotential). To
MEC can be done from various
organic sources, including waste reduce the overpotentials,
materials as well as non- plat-inum (Pt) has been used
fermentable substrates [98].
as the catalyst. Electrodes
Principally, bacteria oxidize organic
with different amounts of
compounds typically, acetate and
generate CO2, electrons and protons platinum loadings are
at the anode of an MEC. The commercially available and
interaction of
also prepared in laboratory.
bacteria transfers the electrons to
the solid anode. With an external Titanium with platinum
voltage, the electrons flow to the coating is used as
cathode where they combine with
protons to form hydrogen gas (Eqs.
(3) and (4)) [99]. For charge
neutrality, the protons migrate from
anode to cathode in the solution. In
practice, an applied voltage of >0.2
S. Bajracharya et al. / Renewable Energy 98 (2016) 153e170 163

cathode to avoid the overpotentials.
However, platinum based electrodes
are very expensive. Cathodes made
from cheap non-noble metals like
stainless steel, nickel (Ni) or nickel
alloys have also been tested for H2
production in MEC
[71,110,162,163]. Nickel and
Nickel Molybdenum (NiMo)
electrocatalysts have shown good
results with only a slightly larger
overpotential than platinum
[72,156]. By increasing the specific
surface area of the Ni cathodes, the
cathode overpotential was lowered
and high hydrogen pro-duction over
3 3 1 to overcome the potential losses due
50 m m MEC d was attained
[80].
It has been shown that bacteria
can also catalyze the HER at
biocathodes [78,157]. Studies have
focused on the upscaling and
improvement of H2 production in
MEC by finding good performing
cathodes materials. A bench scale 4
L MEC reactor using stainless steel
3 3
as cathode produced 0.9 m H2 m -
1
MEC d which had graphite felt as
anode to treat acetate-containing
saline wastewater [13]. An
overview of the performances of H 2
producing MECs along with their
operating conditions is presented in
Table 3. Although the applied
voltage controls the electric current,
the current den-sities reported in
MECs increased with the specific
surface area of electrodes. Higher
current densities are reported with
larger spe-cific surface anodes like
carbon felt and graphite brush
anodes (Table 3). Likewise, the
production at the cathode of MEC
is also enhanced by increasing the
cathode surface area. Generally,
metal catalysts, like Pt and Ni are
used for higher hydrogen
production.
6.2. Acetate
MES took another approach to
fix CO2 in multi-carbon com-
pounds such as liquid fuels or
chemicals by electricity-driven
reduction reactions. This
application is considered as a
technol-ogy for the storage of
electrical energy in the
CarboneCarbon bond of value-
added chemicals [130].
demonstrated the first proof of
microbial electrosynthesis using the
acetogen Sporomusa ovata that
could use electrons directly derived
from a graphite cathode for the
reduction of CO2 to produce acetate
and small quantities of 2-
oxobutyrate [130]. Electron
recovery in these products was
more than 85% of the electrons
transferred at the cathodes.
Subsequent studies demonstrated
the process of CO2 reduction using
MES with a wider range of
microorganisms [129]. These
studies showed the ability of other
acetogenic bacteria, including
Sporomusa silvacetica, Sporomusa
sphaeroides, Clostridium
ljungdahlii, Clostridium aceticum
and Moorella thermoacetica to
reduce CO2 to acetate, 2-
oxobutyrate and formate. Electron
recoveries in acetate and 2-
oxobutyrate were accounted for
84%, 48 6%, 82 10% and 53
4% in S. silvacetica,
S. sphaeroides, C. ljungdahlii and
C. aceticum respectively. Gong et
al. [60] showed that sulfide can be
used as electron donor at the anode
for microbial electrosynthesis. The
study used a sulfur oxidizer,
Desulfobulbus propionicus, at
anode as a biocatalyst to oxidize
elemental sulfur to sulfate. The
electrons generated in biotic anode
were used for CO2 reduction to
acetate growing S. ovata on a
graphite cathode. Marshall et al.
[113] showed the improvements in
rate of acetate production by CO 2
reduction using mixed microbial
communities termed as
microbiomes. Jiang et al. [81] used
a biotic cathode of mixed culture of
that accepts electrons from the
anode and produced H2 abiotically
to fix CO2 into methane and acetate.
Bioelectrochemical CO2 reduction
with electron capture efficiency of
97% was reported controlling the
cathode potential below 950 mV vs
NHE [81]. Marshall et al. [114]
demonstrated improved
performance of microbial
electrosynthesis for acetate
production at the highest rate of 1 g
1 1
L d by autotrophic microbiomes
when operated for long term.
Furthermore, the long term
adaptation resulted into a stable and
resilient biocathode.
The conditions of the MES
process must be created to allow the
optimal metabolism of biocatalyst
present at the biocathode. A suitable
terminal electron acceptor should be
available for the
reduction reaction. In addition, the
cathodic or applied potential that
breaks the thermodynamic barrier
of a biological reaction should be
applied for a successful reduction
reaction in MES. Homoacetogenic
bacteria can efficiently convert CO2
to acetate, which is a major
intermediate molecule for the
production of bio-chemicals [8].
Thermodynamically, the conversion
of CO2 to acetate requires 280 mV
vs SHE cathodic potential.
However, under practical conditions
a much lower potential is required
to the microbial energy uptake and
mass and charge transfer resistances
involved in bioelectrochemical
system. Apart from the above
factors, several other underlying
factors such as electrode materials,
reactor design, mediators in
electron transfer influence the
overall process efficiency [41]. At
present the MES technology is at its
infancy, therefore current studies
are mainly focused on fabricating
new proofs of concept.
6.3. Methane
Methane generation from
anaerobic digestion of organic sub-
strates has long been in practice and
it is considered as a renewable
process. Still, to improve the
sustainability of the methane gener-
ation process, recycling of the CO 2
generated from various biolog-ical
processes can be integrated to
produce more methane through
microbial electrosynthesis.
Microbial electrosynthesis of
methane, also known as
electromethanogenesis, can proceed
at lower tem-peratures than
anaerobic digestion. The specialty
of electro-methanogenesis through
MEC is that the organic matter
present in wastewater can be treated
and at the same time methane pro-
duction is achieved. This process
provides more advantages than
traditional methanogenesis in terms
of higher methane yield and
utilization of the effluents issued
from anaerobic digestion pro-cesses
[30,197].
Clauwaert and Verstraete [30]
showed bioelectrochemical methane
production using a single chamber
configuration in MEC mode, using
plain graphite as electrode. An
applied potential of 0.8 V (vs SHE)
was employed, reporting a
maximum methane production rate
1 1
of 0.75 0.12 L L -MEC d from
3 1
4.13 kg m -MEC d COD loading
with 86 14% of acetate to
methane con-version, whereas
without voltage application only
1 1
0.17 0.06 L L -MEC d of
methane were generated at a COD
3 1
feeding of 1.38 kg m -MEC d
with 47 17% of acetate to
methane con-version. Treatment of
anaerobic digestion effluents in a
single chamber MEC with methane
production was prospected as a
viable technology for efficient waste
treatment [30]. Sasaki et al. [161]
focused on the use of a membrane-
less configuration under a working
potential of 0.395 or 0.595 V (vs
SHE) at neutral pH and
demonstrated efficient methane
production. It was observed that the
dominating methanogens on the
cathode were different from those
grown in control reactors with no
electrochemical reactions [161].
In the scalability studies on
MEC with multi-electrode configu-
rations for H2 production using
acetate as substrate Rader et al.
[146], reported that the
methanogenesis rates increased
gradually with time. After 16 days
of operation, the system showed
little H2 production but a
subsequent CH4 production with
good substrate conversion
efficiency, showing that
electromethanogenesis became the
predominant process at the
biocathode, when operated with
effluents from dark fermentation
and anaerobic digestion processes
[146].
A biocathode dominated by
Methanobacterium palustre was
shown to successfully reduce CO2
to methane, in combination with an
abiotic graphite anode through a
mediator-less mechanism (kind of
direct electron transfer) [26]. The
thermodynamic con-straints of
methane production from CO2
reduction, predict a cathodic
potential requirement of 0.244 V vs
SHE at standard
164 S. Bajracharya et al. / Renewable Energy 98 (2016) 153e170

biological conditions. Practically, a
wide range of applied cathode
potentials (i.e. between 0.5 and 1.0
V vs SHE) have been re-ported for
electromethanogenesis [22,26,196].
Cheng et al. [26] demonstrated
electromethanogenesis in
combination with abiotic and biotic
anodes and also with dual chamber
and single chamber combinations.
Methane production with 80%
overall efficiency (electrical energy
substrate enthalpy) at 0.8 V vs
SHE cathode in a single-chamber
MEC was reported, with an anodic
biofilm growing on acetate. In a
double-chamber BES with an
abiotic anode [26] achieved 4.5 L m
2 1
d of methane production with
96% en-ergy/coulombic efficiency,
controlling the cathode at 0.8 V vs
SHE. Compared to conventional
methanogenesis, the advantage of
bio-electrosynthesis is the physical
separation of the oxidation of
organic waste from methane
production, which protects the
methanogenic consortia from the
inhibitory compounds that can be
present in the waste stream, and
CO2 can be recycled for methane
production. Villano et al. [195,196]
used mixed meth-anogenic cultures
as cathodic biocatalysts in dual
chamber configuration to produce
methane from CO2 at several
applied cathode potentials between
-0.65 V to -1.0 V (vs SHE).
6.4. Other chemicals
In recent studies on BESs, the
production of value-added
chemicals and fuels other than
acetate, methane and hydrogen has
been highlighted [103,144].
Valuable products such as hydrogen
peroxide and caustic soda were
produced at the metallic cathode of
MEC by applying external electric
potential and at the concomitantly
achieved improved performance
efficiency for wastewater treatment
[25,142,158]. Electrosynthesis of
fuels such as methanol has long
been reported from the
electrochemical reduction of CO2
using metal catalysts like copper [5]
but the process is energy intensive
and not sustainable. In this context,
microbial electrosynthesis could be
a less energy intensive and
sustainable solution for electricity-
driven fuel and chemical pro-
duction. In recent studies, small
amounts of ethanol and butyrate
production have been reported as
secondary products in MES, from
CO2 reduction using lithoautotrophs
[6] whereas the heterotrophic
production of ethanol from acetate
as substrate has been demon-strated
at the cathode of BES [179]. Most
of the MES studies on CO2
reduction reported H2 evolution at
the cathode as a mediator for the
microbial CO2 reduction [6,81,114].
As an alternative to H2-driven MES
for CO2 fixation, an innovative
strategy has been sug-gested that
uses formic acid (HCOOH) as an
energy carrier [175]. Formic acid
production from CO2 and water by
bioelectrochemical reactions, and
its further conversion to isobutanol
by engineered Ralstonia eutropha
was demonstrated [91]. The R.
eutropha strain was engineered to
divert the usual poly-
hydroxybutyrate synthesis pathway
to produce liquid fuel and also
made it able to withstand electric
current. The metabolically
engineered strain was also used for
the conversion of CO2 to ethanol
[131]. Xafenias et al. [204] showed
increased 1,3-propanediol titers
using a mixed-culture as
biocatalyst, with glycerol as a
substrate. Along with the all the
above discussed products, few
reports are available on the pro-
duction of butanol, acetone and
succinate through MES processes
[58,166].
7. BES based biosensors
MFC technology can be applied
for the easy and fast testing of the
water quality. MFC based
biosensors have been proposed in
recent studies for the detection of
toxic compounds and for the
measurement of biochemical
oxygen demand (BOD) of water
samples. MFCs have the potential
advantage for on-site and real-time
monitoring of water quality [16,17].
MFC technology can also
be highly cost-effective in
comparison with the conventional
sen-sors, as it can be built on low
cost carbon-based materials. In
MFC based biosensors, oxidation of
organic matter in the inflow feed
was catalyzed by the bacteria
growing on the anode and produce
electrons giving an electrical signal.
The electrical signal generated by
the MFC is associated with the rate
of metabolic activity of the biofilm
at the anode [42]. Any disturbance
in the bacterial activity is
interpreted into a change in the
electric current. When toxic
compounds are present in the feed
water, the bacterial activities will be
affected, which can be detected in
the variation in electrical signal.
This extent of change in electric
current was shown to be directly
associated to the specific
disturbance imposed to the bio-
anode when other operational
parameters of MFC such as pH,
temperature and conductivity of the
feeding solution were kept constant
[185]. MFCs were highly sensitive
with regards to many compounds
present in the feed water. Hence, it
can be used as an early warning
signal. In MFC based biosensors,
transducers were not required to
translate the signal to a readable one
as the bacterial growth on the anode
directly produce measureable
electrical signal from the sensing
element. The application of MFC as
biosensor for BOD and toxic
contaminants in water has been
separately discussed as in the
following sections.
7.1. BOD sensors
BOD has been used as a basic
parameter to quantify the extent of
organic contamination in the water
systems. The electronic charge
generated from a mediator-less
MFC is in good positive correlation
to the concentration of organic
matters. So, MFCs have been
investigated as BOD sensors
[16,17,87]. Chang et al. [16]
continu-ously monitored the BOD
of sample water on-line using an
MFC, by measuring the electric
current in amperometric mode.
1
BOD values of up to 100 mg L
were in good linear fit with the
electric current generated. An
extrapolation of the fitted model can
be used to measure higher BOD
values [16,17]. MFC as a BOD
sensor can operate with stable
performance for over 5 years with
minimum maintenance service [16].
A performance overview of MFC-
based BOD sensors is presented in
Table 5, along with the operational
characteristics of the MFCs. In all
of the literature mentioned in Table
5, inoculation of the anode with
mixed bacterial cultures is-sued
from wastewater was carried out to
widen the variety of us-able
substrates and also for long-term
performance stability. The quickest
response time of MFC-based BOD
sensors was 2.8 min for a scaled-
down single chamber MFC and the
response-time varied with the
reactor design [42]. Table 5 shows
that the most recent studies have
improved the BOD detection range
and response time of MFC based
sensors.
7.2. Toxicity sensors
MFC-based toxicity sensors was
first demonstrated by [88] which
showed the variation in the
electrical current in response to the
presence of contaminants such as
heavy metals, like Pb and Hg,
organophosphorus pesticides (e.g.
Diazinon) and poly-chlorinated
biphenyls (PCBs) in the water
samples. Principally, the substrate
consumption rate and the microbial
activity in MFC bio-sensors are
directly linked to the electric current
generated. A decrement in electric
current under the exposure to a
toxin, when all of the operational
conditions remain same, is an
indication of toxic inhibition. An
effect of toxic components on the
electrochemically-active bacteria
has been shown by a shift in the
polarization curves, specifically a
doseeresponse relationship for
nickel was visualized in the
polarization curves [178]. A higher
concentration of contaminant leads
to a lower current at all over-
potentials [177,178].
MFC-based
biosensors studied for the
 S. Bajracharya et al. / Renewable Energy 98 (2016) 153e170 165

Table 5
Overview of performance, design and functional characteristics of MFCs used as BOD sensors.

Source of inoculum Anode Configuration Detection range Saturation signal Response time References
1
(BOD5, mg L )
Enriched consortium (waste water) Graphite felt Two chamber 2.58e206 1.1 mA 0.5e10 h [87]
(based on charge)
Consortium (activated sludge) Graphite felt Two chamber 23e100 6 mA 1h [16]
Consortium (primary clarifier) Carbon paper Two chamber 10e250 2 40 min [218]
233 mA m
Consortium (from an active MFC) Carbon cloth Single chamber 3e164 35 mA 2.8e8.7 min [42]
(air breathing cathode)
Table 6

Overview of the reactor, performance and functional characteristics of MFCs used as toxicant sensors.

Source of inoculum Anode material 1 Baseline signal Response time References

Toxicant-detection range (mg L )
Mixed culture (Activated sludge) Graphite felt Diazinon:1e10 0.04 mA 20 mine2 h [88]
Pb: 1e10
Hg: 1e10
PCBs: 1e10
2 2
Mixed culture (active MFC) Graphite plate Cu : 85 1.37 A m 50e100 min [176]
Geobacter sulfurreducensn Ti/Ni/Au tri-layer Formaldehyde 0.1%e4% 2 <5 min [36]
4 mA cm
Mixed culture (active MFC) Graphite plate Ni: 10 2.25 mA 30 min [177]
6
Mixed culture (waste-water) Carbon cloth Cr : 1e8 0.10e0.12 V 5 min [92]
3
Fe : 1, 8, 48
NO3 : 1, 8, 48
Mixed culture (active MFC) Carbon cloth 2 1 32.2 mA 12 min [42]
Cd 0.1e100 mg L

detection of toxic components in
water which are summarized in
Table 6. Table 6 shows that the
lowest detection limit of the MFC
1 full advantage of MES, it is very
biosensors was 1 mg L for heavy
metals like Pb, Hg, Cr and even 100
1 limitations are especially complex
mg L for Cd, while the upper
limits of detection were not
assessed within the short range of
concentrations employed.
It has been established that
MFC based sensors could be sen-
sitive to the target compounds with
the detection limits lower than 1
ppm, and can be operated for long
time with stable per-formance.
However, a few key constraints of
MFC-based bio-sensors have to be
addressed for full scale installation
of this technology. These
constraints are low selectivity,
lower detection limit, risk of other
microbial infections and mass-
transfer limita-tions concerning
substrates and products [35]. Recent
advances made in MFC-based
biosensors have broadened the
perspective for simple, on-site and
cost-effective water quality
monitoring. The use of highly
acid/base tolerant and halo-tolerant
microbes in MFC biosensors will be
highly attractive for industrial
wastewater monitoring [35].
8. Future prospects and
conclusions
BESs are versatile systems
designed for converting chemical
energy into electrical energy (and
vice-versa) while employing
microbes as catalysts. MES is the
most recent application of BESs
utilized for the electricity-driven
chemical and fuel production.
However, the understanding of the
multi-disciplinary aspects involved
in MES processes is still on its
infancy. Compared to conventional
industrial microbiology, MES
requires more expertise from other
disciplines such as electrochemistry,
bio-electrochemistry and materials
sciences. Generally, the perfor-
mance of any biological system is
dependent on the substrate
conversion, biocatalyst activity,
specificity of the enzymes involved
in the conversion process and redox
conditions. In the case of
electrochemical processes it also
depends on the conductivity of the
electrolyte (either anolyte or
catholyte), mediators involved,
anode and cathode potentials,
overpotentials (voltage losses),
mass and charge transfer etc. Since
MES result from a combination of
these two processes, the overall
electrochemical system and
biochemistry of the microorganisms
command the selection of type of
and difficult to identify. biocatalyst to be chosen. Selection
The above stated limitations of biocatalyst is also influenced by
were generally established for MFC the terminal electron acceptor to be
technologies in which only one used for reduction process. To take
biological component is present,
whereas in the case of biocathodes, important to understand which
plenty of limitations are typically intracellular and extracellular
associated beyond the anodes.
Reduction of over-potentials and
high coulombic efficiencies often
remain the main technological
challenges of BES to solve in future
applications. Upscaling the
production at industrial scale is also
found as the major limiting step for
BES technologies. Stacking up the
number of MFCs and integration of
number of electrodes in a single
sys-tem have been reported in
literature. Even though the research
so far provided promising results,
the upscaling of BES still need to
address the overpotentials and other
associated design aspects.
Reproducibility of bench scale
performances in the large scale
systems will certainly make the
process economically and
environmentally feasible. Studies
have also proposed the possible
way to incorporate the BES
technology in existing wastewater
treatment plants. It has been
projected more technically feasible
to incorporate MEC for
simultaneous waste treatment and
hydrogen production than running
MFC for electricity generation from
wastewater. The possible and
appropriate scheme to incor-porate
MEC to produce hydrogen gas in
existing wastewater treatment plant
as proposed by Escapa et al. [49] is
shown in Fig. 4.
In anodic mechanism of MFCs,
mixed cultures are considered to be
as effective biocatalysts with
wastewaters as substrate. In MES,
less is known about the behavior of
cathodic biofilms, planktonic cells
and electron transfer mechanism
involved. It is also necessary to
understand the interface of both
biofilms and planktonic cells.
Conceptually, mixed as well as pure
homo-acetogenic bacterial cultures
could effectively carry out CO2
reduction. The electron transfer
efficiency and involved mecha-
nism, biofilms sustainability in
166 S. Bajracharya et al. / Renewable Energy 98 (2016) 153e170
Fig. 4. Possible scheme to incorporate BES in wastewater treatment plant. Flowchart shows the processes in an existing wastewater treatment plant (top) and the proposed plant (bottom)
incorporating the Microbial Electrolysis Cell for wastewater treatment and hydrogen production. Adapted from Escapa et al. [49] Copyright (2012), with permission from Elsevier.
factors influence the metabolic rate.
The combination of BES technology with the fermentation technology
termed as Electro-fermentation (EF) has added a new future prospect of
versatile BES application. The concept is to use electrical energy as source of
reducing power for microbial fermentation and also to provide the required
electrons for gen-eration of the product of interest. Researchers from the BES
and fermentation disciplines are focusing on EF. EF is foreseen as po-tential
application to overcome many biological, electrochemical, logistical and
economic challenges incorporated in the production of value-added products
in BES.
Acknowledgments
Suman Bajracharya is supported by a PhD grant from VITO's strategic
research fund (1310225). Mohita Sharma acknowledges Indo-Belgian
scholarship from the Flemish Government (Vlaamse Gemeenschap-
1F2B8G/JDW/2012-2013/12-BTL-IND-02) for sup-porting her stay at VITO.
G. Mohanakrishna gratefully acknowl-edges the Marie-Curie Intra-European
Fellowship (IEF) supported project BIO-ELECTRO-ETHYLENE (Grant No:
626959) from the Eu-ropean Commission.
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