Journal of Power Sources 356 (2017) 491e499

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Journal of Power Sources

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Ammonia recovery from urine in a scaled-up Microbial Electrolysis

Cell
Patricia Zamora a, b, Tanya Georgieva a, Annemiek Ter Heijne c, *, Tom H.J.A. Sleutels a,
Adriaan W. Jeremiasse d, Michel Saakes a, Cees J.N. Buisman a, c, Philipp Kuntke a
a
Wetsus, European Centre of Excellence for Sustainable Water Technology, Oostergoweg 9, 8911MA, Leeuwarden, The Netherlands
b
Abengoa, Campus Palmas Altas, C/ Energía Solar 1, 41014, Seville, Spain
c
Sub-Department of Environmental Technology, Wageningen University, Bornse Weilanden 9, P.O. Box 17, 6700 AA, Wageningen, The Netherlands
d
W&F Technologies, Calandstraat 109, 3125 BA, Schiedam, The Netherlands

h i g h l i g h t s g r a p h i c a l a b s t r a c t

The application of a scaled-up MEC

for nutrient recovery of urine is
shown.

The TAN transport efficiency over the
CEM was 92 ± 25%.

The TAN recovery over the TMCS was
31 ± 59%.

The highest current density reached
was 1.7 A m2 for undiluted real
urine.

The MEC showed a lower energy
demand than electrochemical TAN
recovery systems.

a r t i c l e i n f o a b s t r a c t

Article history: A two-step treatment system for nutrient and energy recovery from urine was successfully operated for
Received 6 December 2016 six months. In the first step, phosphorus (P) was recovered as struvite (magnesium ammonium phos-
Received in revised form phate or MAP) in a MAP reactor. The effluent of this MAP reactor was used for total ammonia-nitrogen
7 February 2017
(TAN) recovery and hydrogen production in a Microbial Electrolysis Cell (MEC). This MEC was coupled to
Accepted 27 February 2017
Available online 9 March 2017
a Transmembranechemisorption (TMCS) module, in which the TAN was recovered as an ammonium
sulphate solution. The MEC had a projected surface area of 0.5 m2 and was operated at different urine
dilutions. The system was stable during the operation on 2 times diluted and undiluted urine at an
Keywords:
Microbial Electrolysis Cells
applied voltage of 0.5 V with an average current density of 1.7 ± 0.2 A m2. During stable current
Ammonia recovery production, the TAN transport efficiency over the CEM was 92 ± 25% and the TAN recovery was 31 ± 59%.
Up-scaling bioelectrochemcial systems In terms of energy efficiency, the electrical energy required for the TAN recovery was 4.9 ± 1.0 MJ kg1
N ,
Urine treatment which is lower than competing electrochemical nitrogen removal/recovery technologies. Overall, this
study shows, for the first time, the application of a scaled-up MEC for nutrient recovery from urine.
© 2017 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license
(http://creativecommons.org/licenses/by/4.0/).

1. Introduction

The accelerating growth of the world population results in

* Corresponding author. higher food demand, and accordingly in higher need of fertilizers
E-mail address: annemiek.terheijne@wur.nl (A. Ter Heijne). [1,2]. The Food and Agriculture Organization of the United Nations

http://dx.doi.org/10.1016/j.jpowsour.2017.02.089
0378-7753/© 2017 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
492 P. Zamora et al. / Journal of Power Sources 356 (2017) 491e499
(FAO) reported an annual increase of the total fertilizer demand
with 1.8% for the period of 2014e2018. Particularly, for the same
period the Nitrogen (N) and Phosphorus (P) based fertilizers de-
mand is expected to increase by 5.8% and 2.1%, respectively [3]. N
and P are two of the major nutrients in commercial fertilizers,
which are also found in considerable concentrations in wastewater
streams. Ideally, these nutrients are removed from wastewater in
order to meet discharge limits, and at the same time reused for the
production of fertilizers. Especially the recovery of nutrients from
urine is an attractive and sustainable approach for wastewater
management, because urine is a concentrated and nutrient rich
wastewater stream [4]. Approximately, 75% of the N and 50% of the
P found in domestic wastewater originate from urine [5].
To recover nutrients and energy from urine, we propose a full
treatment system consisting of two steps. In the first step, P is
recovered as struvite. In the second step, nitrogen is recovered and
energy in the form of hydrogen that is produced in a Bio-
electrochemical System (BES). P recovery via struvite formation
from urine is already a proven technology with a removal over 95%
[6e8]. After hydrolysis of urea, urine has the optimal pH (8.5e10)
for struvite precipitation and a strong buffering capacity, which is
also beneficial for the operation of the BES in the second treatment
step [9e11]. Since the urine does not contain sufficient magnesium
to recover all the phosphorus, an additional magnesium source (i.e.
MgCl2, MgO, Mg(OH)2) is required.
For the N removal from wastewater streams, the most estab-
lished processes only remove the N, releasing N2 gas to the atmo-
sphere and do not recover N as a suitable fertilizer. Besides, these
processes for N removal require high energy input. For example,
autotrophic nitrification-denitrification requires 45 MJ kg1 N MAP reactor was further treated in a mesh filter (R3/R4) and a
removed, while a combination of Sharon and Anammox requires
16e19 MJ kg1 N removed [12].
In this context, BESs offer an alternative to existing processes
because they recover N in an active form, TAN (e.g., ammonium and
ammonia). TAN refers to both ammonia (NH3) nitrogen and
ammonium (NHþ þ
4 ) nitrogen, while NH4 and NH3 refer to the specific
forms of nitrogen. Besides, BESs can be considered more sustain-
able due to the fact that the organic material present in urine
provides (part of) the energy [13,14]. This chemical energy can
either be recovered as electricity in a Microbial Fuel Cell (MFC), or
can be converted into hydrogen gas using additional electrical en-
ergy in a Microbial Electrolysis Cell (MEC) [15,16]. In both systems,
the electrical current is used to transport the ammonium ions from
the anolyte to the catholyte where they can be recovered in the
form of ammonia gas. This ammonia recovery from the catholyte
can be performed in an energy efficient way by absorption in a
sulphuric acid solution through the application of a gas permeable
hydrophobic hollow fiber membrane module (Trans-
MembraneChemiSorption or TMCS) [17]. This TMCS module only
allows ammonia gas to pass from the catholyte on one side of the
module to the sulphuric acid solution on the other side of the
module. This way an ammonium sulphate solution is produced,
which is a nitrogen based fertilizer in liquid form [18].
Although laboratory-scale BESs have been demonstrated as a
successful technology for wastewater treatment and especially for
the recovery of TAN from urine, scaling-up of BESs remains a chal-
lenge [13,19]. The complexity of BESs increases with up scaling of the
technology, especially in terms of operational strategy and reactor
requirements. Parameters that hurdle the performance of scaled-up
BESs are, amongst others, high internal resistances, membrane
fouling or deterioration, and lower performance with real waste
streams compared to synthetic wastewater [20e22]. The successful
operation of an up-scaled BES for TAN recovery on a real wastewater
would be the first step towards demonstrating feasibility of BES for
nutrient recovery as an alternative to conventional removal/recovery
technology and allow for a possible business case for BES [19].
This study shows, for the first time the performance of a scaled-
up MEC for TAN recovery from urine over a period of six months. P
was recovered via struvite precipitation and N was recovered via a
BES coupled to a TMCS module. We analyze the performance of this
BES in terms of TAN recovery and transport rates and the potential
losses of the different parts of the system.
2. Materials and methods
2.1. Urine collection
Urine was collected from male employees of Wetsus (approxi-
mately 50) using water free urinal (Urimat®, BioCompact Envi-
ronmental Technology B.V., Ridderkerk, The Netherlands). In total
15 urinals were connected to a 600 L stainless steel storage tank
(Lootsma apparatenbouw, Nijland, The Netherlands). A storage
time of up to 16 days inside this storage tank ensured complete
hydrolysis of the urea.
2.2. Process description
The process comprised two stages: P recovery (MAP reactor &
settler including filter and softening system) and N recovery (MEC
& TMCS). A schematic version of the process flow diagram is shown
in Fig. 1 with pictures from the actual pilot reactor.
The recovery of P as struvite was carried out in an MAP reactor
(fluidized bed reactor design by DeSaH B.V., Sneek, The
Netherlands) as reported by Zamora et al., [23]. The effluent of the
softening system comprised by a Weakly Acidic Cation-Exchange
Resin (WAC) type Lewatit® CNP 80 and a Strongly Acidic Cation-
Exchange Resin (SAC) type Lewatit® S 1567.
The second part of the urine treatment (TAN recovery) was
performed by the MEC (R7), where the organic matter was oxidized
by bacteria in the anode chamber, while ammonia gas was recov-
ered from the catholyte and H2 was produced. The anolyte and the
catholyte were continuous circulated at a flow of 4e6 L h1 and
100-75 L h1, respectively. Dissolved NH3 gas in the catholyte was
recovered in sulphuric acid (T2) by the TMCS module (R9). As a
result, the N was recovered as an ammonium sulphate solution. The
design and the materials used for the MEC reactor were previously
reported by Dekker et al. [24], with minor differences. In our ex-
periments only one anode and one cathode were used. The MEC
consisted of two 1 mm thick titanium plates (33 cm  150 cm) with
a mixed metal oxide coating (Magneto Special Anodes B.V., Schie-
dam, The Netherlands), which served as anode and cathode. The
thickness of the anode and cathode chamber was 5 mm resulting in
a volume of 2.5 L for the anode and 2.5 L for the cathode chamber.
Anode and cathode were separated by a Cation exchange mem-
brane (Ralex CMH-PP, Mega, Praha, Czech Republic). The liquid
working volume of the anode compartment (including tubing) was
2.6 L and the liquid working volume of the cathode compartment
(including tubing and recycle vessel) was 30 L. Possible precipitates
or particles in the catholyte and in the acid streams were retained
before entering the TMCS in filters R10 and R11, respectively. The
presented data corresponds to a 6-month operation period. All
anode and cathode potentials are reported vs Ag/AgCl reference
electrodes (þ0.2 V vs NHE, type QM711X, ProSense B.V., Oosterh-
out, The Netherlands).
2.3. Sampling and chemical analysis
During operation, daily samples were taken from nine sampling
ports (marked with SP-[no.] in Fig. 1). The pH, conductivity and
 P. Zamora et al. / Journal of Power Sources 356 (2017) 491e499 493

Fig. 1. Flow scheme diagram (A) and pictures (B) of the up-scaled system for the two-step recovery of nutrients and energy from urine. In step one the P was recovered and
separated in a MAP reactor while in step two the TAN was removed from the urine in a MEC and recovered in 1 M sulphuric acid through a TMCS module. The energy present in the
urine in the form of organic matter was used together with electrical energy to produce H2 gas and drive the TAN recovery.

temperature were measured on a daily basis and recorded by a data composition of: 1.36 g L1 NaCH3COO$3H2O, 0.74 g L1 KCl,
logger (custom-made PLC system, DeSaH B.V.). The concentrations 0.58 g L1 NaCl, 0.68 g L1 KH2PO4, 0.87 g L1 K2HPO4,
þ
of Mg2þ, Ca2þ, PO3-
4 -P, COD, NH4 -N were analyzed with Hach Lange 0.28 g L1 NH4Cl, 0.1 g L1 CaCl2.2H2O, 0.1 g L1 MgSO4$7H2O and
kits number LCK 326, LCK 427, LCK 350, LCK 514 and LCK 303 (Dr. 1 ml L1 of a trace elements mixture [25].
Lange, HACH, Loveland, Colorado, USA) on week days, respectively. Urine had a composition of approximately 4.5 ± 0.6 g COD L1,
These samples were analyzed using a spectrophotometer (DR3900, pH 9.4 ± 0.1, conductivity 28.1 ± 2.1 mS cm1, 234 ± 22 mg PO4-P
Hach Lange, Tiel, The Netherlands) Inductively Coupled Plasma- L1, 4.0 ± 0.5 g NH4-N L1 and less than 0.5 mg Mg2þ L1.
Optical Emission Spectrometry (ICP-OES), (Perkin Elmer type Op-
tima 5300 DV, Groningen, The Netherlands) was used to determine
the concentration of the cations in the samples from the anode 2.4. Calculations
inflow (SP5), anode outflow (SP6), catholyte (SP7) and urine tank
(SP9) once per week. Anion concentrations were determined for The P recovery rP (%) as struvite was calculated with
the same samples by Ion Chromatography (IC), (Metrohm Compact
IC Flex 930, Schiedam, The Netherlands) once per week. Inorganic cP;in  Qin  t  cP;eff  Qeff  t
Carbon (IC), Total Carbon (TC), Non-Purgeable Organic Carbon rP ¼  100% (1)
cP;in  Qin  t
(NPOC) and Total Organic Carbon (TOC) were analyzed with TOC
analyser (Shimadzu TOC-LCPH, Kyoto, Japan) for samples from anode
where cP;in is the concentration (g L1) of phosphorus in the urine
inflow (SP5), anode outflow (SP6) and urine tank (SP9) once per
tank, Qin is the flow rate (L h1) of the urine. cP;eff is the concen-
week. The samples were filtered (0.45 mm) and diluted until the
tration (g L1) of the phosphorus in the effluent of the MAP reactor,
desired concentration range. No samples were taken to measure
Qeff is the flow rate (L h1) of the pretreated urine and t is the time.
the produced hydrogen. Initially, during the start-up of the MEC
The ammonium recovery rNH4N (%) was calculated according to
reactor, the cell was fed with synthetic wastewater with a
494 P. Zamora et al. / Journal of Power Sources 356 (2017) 491e499

DcNH4N;Acid  VAcid
rNH4N ¼  100%
cNH4N;Anode IN  24  Q
where DcNH4N;Acid is the increase in the ammonium concentration
(g L1) in the acid per day. Vacid is the volume of the acid in T2 (50 L).
cNH4N;Anode IN is the concentration of the ammonium in the anode
inflow (g L1). Q is the inflow of the anode (L h1) over a time
period of 24 h to equalize the units.
The current density (i in A m2) was determined by the
measured current divided by the CEM surface area (0.5 m2). The
overpotentials and resistances were calculated according to previ-
ous studies [26,27].
The Coulombic efficiency (CE (%)) was calculated according to
ði  HRTÞ
CE ¼  100%
AM  b  F  Q anode  ðDCODÞ
where i is the average current density (A m2), HRT is the hydraulic
retention time (s), AM is the membrane surface area (0.5 m2), b the
amount of electrons transferred per more COD (4), F is the Faraday
constant (96,485 C mol1), Qanode is the anode inflow rate (L s1)
and DCOD is the change in the measured COD concentration
(mol L1).
Total Ammonia Nitrogen (TAN) transport rate over the
CEM; JTAN;CEM ðgN m2 d1 Þ, was determined according to
 times diluted urine (1 L urine: 4 L water). After the MEC was
CTAN;in  CTAN;eff Þ  Q in  t
JTAN;CEM ¼
AM
ensure that effluent was below guidelines values. The guideline values
were >95% phosphorus recovery, less than 10 mg L1 calcium and less
(2)
than 10 mg L1 magnesium to prevent the risk of scaling in the MEC,
while minimizing the removal/loss of COD and TAN. The effluent of
the struvite reactor was fed in different dilutions to the MEC.
Regarding the MEC operation, the reactor was inoculated with
effluent from a working laboratory MEC operated on synthetic
wastewater containing acetate. Based on previous research, the
MEC was operated with synthetic wastewater and the applied
voltage was increased stepwise from 0.5 V to 0.8 V to increase the
current density and strengthen the bio-anode during the start-up
period [28]. A 10 mmol L1 NaOH solution was used as the cath-
olyte. After 71 days of operation on synthetic wastewater, the
influent was switched to 5 times diluted urine. This dilution of the
urine was then stepwise decreased until undiluted urine was fed to
the MEC (see Table 1) to adapt the bioanode to a more complex
(3)
wastewater with an increasing TAN concentration, which was
previously shown as a successful strategy [29,30]. The sequential
decrease of urine dilution was based on a stable current production
and a stable anode potential. The applied voltage was changed in
regard to the measured anode potential in order to guarantee stable
operation (current densities). For every operational period on
diluted and undiluted urine, the HRT was chosen such that the COD
loading rate was 46 ± 12 g COD m2 d1.
The TMCS unit for ammonium recovery was integrated in the
catholyte loop after the switch from synthetic wastewater to 5
running stable on undiluted urine, the integration of both stages for
(4) P & TAN recovery was realized.

where CTAN,in is the measured concentration TAN in the influent
(g L1), CTAN,eff is the measured concentration TAN in the effluent
(g L1), Qin is the influent flow speed (L s1), t is the amount of
seconds per day (86,400 s d1), and AM is the CEM surface area
(0.5 m2).  
The energy demand MJ kg1 N was calculated according to:
ði  ECell  tÞ
Energy demand ¼
JTAN;CEM  106
where i is the average current density (A m2), Ecell is the average
cell voltage (V), t is the amount of seconds per day (86,400 s d1),
JTAN;CEM is the TAN transport over the CEM in kgN m2 d1, and 106
is the amount of J per MJ.
The TAN transport over the TMCS (gN m2 d1) was calculated
from the daily TAN concentration increase in the acid storage tank
using the volume of the acid and the surface area of the TMCS
membrane (1.4 m2).
The COD removal was calculated as the difference be-
tween the COD measured in the anode influent and the anode
effluent.
2.5. Operational strategy
The struvite reactor was operated to recover phosphorus and
3. Results and discussion
3.1. Phosphorous removal and treatment with ion exchange resin
In the present work P was recovered via struvite precipitation in
an MAP reactor. The highest treatment capacity of the reactor
during this study was 40.8 L d1. Details of struvite formation and
(5) the effect of Mg dosing in this set of experiments have been
described elsewhere [23]. Overall, 94 ± 6% of the P in the urine was
recovered as nearly pure struvite granules (purity over 90%) and a
diameter ranging from 0.3 to 6 mm. During struvite precipitation
about 16% of the TAN present in the urine was removed.
After struvite precipitation, an additional treatment via mesh
filters and cation exchange resins was performed. Mg2þ and Ca2þ
concentrations in the MAP reactor effluent needed to be lowered to
prevent scaling at the cathode and the CEM in the MEC. The average
effluent concentrations of the WAC-SAC softeners system (inflow
for the MEC) were 3.4 ± 0.2 g NH4-N L1, 3.4 ± 0.3 g COD L1,
6.5 ± 2.4 mg PO4-P L1, 1.9 ± 0.5 mg Mgþ2 L1, 0.3 ± 0.2 mg Ca2þ L1,
3.6 ± 0.4 g Cl L1, 0.5 ± 0.04 g SO2 1
4 L , >1 g Na L
þ 1
and >1 g Kþ
L1. Furthermore, the effluent had an average conductivity of
27.4 ± 1.9 mS cm1 and an average pH of 9.1 ± 0.2. Further infor-
mation on the performances MAP reactor (including the filter and
softening system) were reported by Zamora et al., 2016 [23]. The
low concentration of bivalent cations should be able to prevent

Table 1
Operational strategy of the MEC reactor.

Days of operation Influent HRT anode (h) Applied voltage (V)

1e71 Synthetic wastewater 1.8e2.7 0.6, 0.7 and 0.8

72e135 5  diluted urine 1.8e5.4 0.8, 0.65 and 0.5
136e150 2.5  diluted urine 2.2e6.2 0.5
151e178 2  diluted urine 4.3 0.5
179e206 Undiluted urine 6.2e8.7 0.5, 0.6, 0.7 and 0.6
 P. Zamora et al. / Journal of Power Sources 356 (2017) 491e499
unwanted precipitation and scaling in the MEC. Unfortunately,
approximately 25% of the COD in the urine was removed within the
struvite reactor due to biological degradation [23]. As a result the
ratio between theoretical available electrons from COD and TAN to
be removed changed from initially 2 to 1.75 after the struvite
reactor. This means less electrons were available for the bioanode to
support the TAN transport and a higher CE and COD removal were
needed as a result [14].
3.2. MEC performance
The current density produced by the MEC over the whole
operational period is shown in Fig. 2. In the first period with syn-
thetic wastewater, after the system was inoculated and an elec-
trochemically active biofilm developed at the anode, the applied
voltage was increased stepwise from 0.5 V to 0.8 V. After switching
to 5 times diluted urine, the applied voltage was lowered from 0.8 V
to 0.5 V to counteract an increasing anode potential and to stabilize
current production. The PLC control system and the power supply
had a malfunction between day 100 and 122 during which the
operation of the MEC was switched to MFC controlled mode. After
replacement and repair of key components (PLC), the system was
restored to MEC mode with identical operational condition as
before the malfunction. The system quickly recovered its perfor-
mance in terms of current density. The dilution was then stepwise
decreased until the cell was operated on undiluted urine. After
stable operation on undiluted urine, the applied voltage was
increased to 0.6 V to increase the current density.
The current density and the applied cell voltage followed the
same trend; the current density increased at increasing the applied
cell voltage and vice versa. Nonetheless, the current decreased
when increasing the applied cell voltage from 0.6 to 0.7 V during
operation on undiluted urine. The current density measured during
this period was unstable. The highest achieved current density was
1.9 A m2 with 2.5 times diluted urine and 0.5 V applied. Almost the
same current density (1.8 A m2) was measured during the treat-
ment of undiluted urine and 0.7 V applied. The measured anode
and cathode potentials of the MEC over the whole operational
period are shown in Fig. 3.
After switching from synthetic wastewater to real (diluted)
urine (day 72) and integrating the TMCS module in the catholyte
Fig. 2. Current density and applied voltage over the whole operational period with diluted and undiluted urine. The PLC control system and the power supply had a malfunction on
day 100 and was replaced on day 122, which resulted in a 3-week period were the system was operated in an MFC mode with a resistor in place. Hence this data was omitted from
the figure.
495
loop, the cathode potential increased from 0.95 V to 0.57 V. The
cathode potential remained high at values of 0.65 ± 0.05 V
throughout the operation on various urine dilutions (5, 2.5, and
2) and undiluted urine. During operation on the various urine
dilutions and undiluted urine, the anode potential was 0.27
± 0.09 V and the cathode potential was 0.62 ± 0.18 V. Once
switched to undiluted urine and the applied cell voltage was
increased to 0.6 V, an anode potential increase to values
of 0.19 ± 0.02 V was observed. Further increasing the applied
voltage to 0.7 V resulted in an even higher anode potential
of 0.12 ± 0.07 V. At that point the cathode potential was stable
(0.68 ± 0.01 V), thus the increase in cell voltage led to an increase
in the anode potential. The reason for the high cathode potentials is
that oxygen was present in the cathode chamber, resulting in a
combination of oxygen reduction and hydrogen formation, occur-
ring at higher potentials than measured for only hydrogen forma-
tion. As the cathode potential was quite stable and the cell voltage
was fixed, the result was an increase in the anode potential, that did
not necessarily result in higher current density. Although small
amounts of oxygen (about 1e2 mg L1) were detected during the
experiments, this was sufficient to severely hinder the performance
of the MEC. As a consequence of the presence of oxygen and
increasing the applied voltage, the anode potential increased
together with the current density, which eventually resulted in an
unstable bioanode and therefore a failing MEC. .
3.3. COD removal and Coulombic efficiency
Fig. 4 shows an overview of the Coulombic Efficiency (CE) and
COD removal as a function of the current densities produced
during the experimental period. During feeding with 2.5
diluted urine, which was the period when the highest current
density was produced, the corresponding CE was 88% and COD
removal 42%. This high CE shows that most of the organic com-
pounds were oxidized by the electrochemically active bacteria,
and methane production was limited. On average during feeding
with 2.5 diluted urine, the CE was 65 ± 10% and the COD
removal was 37 ± 6%. This means that on average 35% of the
electrons were consumed elsewhere, i.e. via methanogenesis and
sulphate reducers competing for substrate with electrogens. The
low COD removal (average 20%) is due to low obtained current
496 P. Zamora et al. / Journal of Power Sources 356 (2017) 491e499
Fig. 3. Electrode potential and applied voltage over time during the complete experimental period. The PLC control system and the power supply had a malfunction on day 100 and
was replaced on day 122, which resulted in a 3-week period were the system was operated in an MFC mode with a resistor in place. Hence this data was omitted from the figure.
density and the high COD loading (46 ± 12 g COD m2 d1). The
system was not optimized for COD removal and could therefore
reach higher current density values if the COD loading would be
optimized.
In comparison, a previous study where diluted urine was treated
with an MEC at an applied voltage of 1.0 V showed considerably
higher current densities (>15 Am2) than the current density
reached in this scaled-up MEC [28]. The difference in the current
density production might be a result of the different reactor design
and size of the MEC affecting the internal resistance, coverage of
the electro-active biofilm on the anode, or limitations through the
use of undiluted urine (e.g. ammonia toxicity). Although many
studies show that urine is a promising wastewater for treatment in
BESs, often only limited information is provided on the COD de-
gradability from urine in respect to the current production (CE) and
total COD removal [31,32]. Another study applying an MEC for urine
treatment using a TMCS module to recover ammonia from the
cathode showed similar results, with a maximum current density of
1.7 ± 0.2 A m2 and CE of 78 ± 10%. However, the COD removal
achieved was double (40 ± 5%) at a lower COD loading rate of 34.6 g
COD m2 d1 using 5 times diluted urine [17].
Fig. 4. Average Coulombic efficiency and COD removal plotted against current density.
3.4. Ammonia removal and recovery
Two subsequent steps are important for the full recovery of TAN.
First, the electric current generated by the MEC was used to
transport TAN through a CEM from anode to cathode, where it was
converted into NH3 as a result of a high pH. Second, NH3 was
recovered from the catholyte as ammonium sulphate via a TMCS
module [17]. As the TAN removal step is current-driven, the ratio
between current density reached in the MEC and the TAN loading is
an important factor to consider for the TAN recovery. The TAN mass
transfer was normalized to the CEM area for the first step and to the
TMCS area for the second step. Fig. 5A shows the first step of TAN
removal from the anode as a function of its load ratio. The load ratio
is a parameter that describes the ratio between nitrogen loading
(converted to A m2) and electric current density (in A m2) [33]. A
load ratio lower than 1 reflects a situation in which more nitrogen is
fed to the system than can be transported by the electric current,
which means that not all NHþ 4 can be removed; a load ratio higher
than 1 means that the produced current is higher than the nitrogen
load, meaning that all NHþ 4 can be removed theoretically. In this
context, the pH defining the dominant TAN species (i.e. NHþ 4 or
NH3) is an important factor. Additionally to NHþ 4 , other ions are
transported across the CEM. The ammonium transport number can
be used to evaluate the contribution of ammonium to the overall
ion transport over the CEM. In our system the load ratio was below
1 in all cases, which shows that the current produced was not
sufficient to carry all the ammonium-nitrogen supplied to the
anode. Nevertheless, the trend confirms that increasing the load
ratio increases the nitrogen removal from the anode [33]. The ni-
trogen removal from the anode in the form of NHþ 4 -N was 31 ± 11%
on average, which is lower than the removals reported in earlier
studies [17,34,35]. During this experiment using real (diluted)
urine, the average pH measured in the anode was 8.1 ± 0.5. This
shows the dominant TAN species present in the anolyte was NHþ 4
(ranging between 98 and 82%). The average transport number for
ammonium was 0.9 ± 0.3, which shows that ammonium was main
charge carrier over the CEM. A transport number larger than 1.0
indicates that migration and diffusion of TAN contributed to the
total TAN transport over the CEM.
In the second step of TAN recovery, the ammonia is extracted
from the catholyte into a 1 M sulphuric acid solution in the TMCS
module. The driving force for the mass transport through the micro
 P. Zamora et al. / Journal of Power Sources 356 (2017) 491e499
Fig. 5. (A) TAN removal against load ratio (electric current/TAN loading) over the experimental period. (B) Correlation of TAN mass transport through the CEM and TMCS module.
porous hollow fibre was the ammonia concentration gradient be-
tween the catholyte and the acid. Fig. 5B shows the results for the
recovery of ammonia through the TMCS module to the acid stream.
The ammonia absorption in the sulphuric acid tank was most of the
time lower than for the ideal situation (dashed line), which can be
explained by: (i) the unstable operation of the MEC and (ii) unstable
conditions in the catholyte (i.e. pH and NH3/NHþ 4 content). As the
current density was never really stable (Fig. 2), the amount of TAN
transported to the cathode and the pH were never stable. The
average pH measured in the cathode was 9.0 ± 1.2. Due to this high
fluctuation in the catholyte pH, both NH3 and NHþ 4 could be found
at times as the dominant species in the catholyte, which leads to
unstable NH3 transport over the TMCS membrane.
Additionally, the sulphuric acid used for absorption of the
ammonia is hygroscopic and the higher water vapour pressure of
the catholyte compared to the acid solution can lead to water
transport over the TMCS membrane. As the TMCS membrane had a
surface area of about 1.4 m2, small differences in water vapour
pressure may result in considerable water transport of the TMCS
module.
3.5. Energy input for TAN recovery in the scaled up MEC
Fig. 6A shows the potential losses of the different parts of the
MEC, which were calculated according to a previous study [26]. The
potential losses were calculated over a period of at least two days
Fig. 6. Potential losses (A) and energy input (B) for TAN recovery in MEC fed with diluted (5, 2.5, and 2) at 0.5 V applied voltage and undiluted urine (0) at different applied
voltages (0.5 V, 0.6 V and 0.7 V).
497
prior to changing operational conditions (i.e. dilution or applied
voltage). Independent of the operational conditions the anode
overpotential and the membrane transport losses are the dominant
factors. The anode overpotential is related to the anode pH and the
concentration of bicarbonate, which are produced from the or-
ganics degradation, i.e. COD removal. Furthermore, the changes in
the measured anode potential can also indicate a different digestion
pathway and mechanism or kinetic limitation of the biofilm at the
anode. Ionic losses were found to be small in comparison (<42 mV).
Interestingly the cathode overpotential was found to be negative,
meaning that the cathode potential was forced to more positive
values due to the presence of oxygen that leaked into the catholyte.
Increasing the applied voltage only causes the anode overpotential
to increase. Eventually, the high anode potential (overpotential) led
to a drastic decrease of the current density (Fig. 2). Minimizing the
internal voltage of the different parts of the MEC can improve the
system [36]. Critical points to be addressed are the removal of ox-
ygen from the catholyte and prevention of oxygen permeation in
the cathode compartment, or choosing an operational mode
different from cell voltage control, to keep anode potentials at
reasonable levels (e.g. anode potential control) [37]. A special focus
should be laid on the TMCS module as a possible route for oxygen
permeation into the catholyte, since the oxygen dissolved in the
acid is in equilibrium with the oxygen dissolved in the catholyte.
The energy efficiency of TAN recovery in the scaled-up MEC was
here defined as the supplied energy to the system per amount of
498 P. Zamora et al. / Journal of Power Sources 356 (2017) 491e499
TAN removed from the anolyte [17]. The required energy demand
for TAN recovery is determined by the applied voltage and the ef-
ficiency of TAN transport through the CEM and TMCS. Fig. 6B shows
an overview of the energy demand for all components of the MEC at
different conditions. Independent of the operational conditions
(applied voltage and dilution), the anode and the membrane
transport were the dominant factors influencing the energy de-
mand for TAN recovery. The cathode contribution to the energy
demand decreased with decreasing the dilution of the feed. Overall,
in our study, the energy needed for the recovery of 1 kg nitrogen
was 4.9 ± 1.0 MJ without taking into account the energy required
for pumping. Comparable studies on the removal of ammonium
through electrochemical systems reported an energy demand of
46.8 MJ kg1
N for treated digestate via an electrochemical cell [35],
4.9 MJ kg1
N for the treatment of diluted urine in a MEC (calculated
from the reported results [28]) and a net energy production of
3.5 MJ kg1
N for the treatment of diluted urine in an MFC [29].
4. Implications
A two-step scaled-up treatment system for nutrient and energy
recovery from urine was successfully operated for six months. In
the first step, the P recovery via struvite precipitation from urine
showed over 96% recovery efficiency. Additionally, the pre-
treatment step yielded Ca2þ and Mg2þ concentrations below
5 mg L1. In the second step, the MEC coupled to the TMCS module
for TAN removal and recovery, showed a maximum current density
of 1.9 A m2 with 2.5 times diluted urine at an applied voltage of
0.5 V. Moreover, the Coulombic efficiency during the whole oper-
ational period was over 70% and COD removal about 20%.
The bioanode stability and oxygen presence in the catholyte
were the main limiting factors preventing stable operation and
higher current densities. The use of more diverse bacterial com-
munity from either an active BES treating real wastewater or the
bacteria obtained from the effluent of an anaerobic wastewater
system can be potentially favorable for the operation of a BES
treating real urine. The nitrogen removal over the CEM reached
31 ± 13% and the recovery was 31 ± 59%. In terms of energy effi-
ciency, the electrical energy required for the TAN recovery was
4.9 ± 1.0 MJ kg1
N , which is lower than competing electrochemical
nitrogen removal/recovery technologies.
The analysis of the COD biodegradation by batch experiments
may provide more insights on the bioanode performance. To con-
trol the anode potential by using a potentiostat instead of applying
a cell voltage may be advantageous for bioanode activity and cur-
rent production. Higher TAN recovery can be achieved by
increasing the COD removal, while maintaining high Coulombic
efficiencies. However, scaling-up BES for TAN recovery faces several
issues mainly due to design of the treatment system and limited
COD removal leading to the presence of oxygen in the cathode and
an unstable bioanode. Therefore, a special focus should be laid on
the cell design, the materials (i.e. gaskets, tubing, etc.) used in
construction and the TAN removal system (TMCS/stripping) to
reduce the risk of high levels of oxygen in the cathode. Additionally,
a hydrolysis step to breakdown complex organic matter (i.e. pro-
teins, amino acids, aromatic compounds, etc.) present in the urine
might be necessary to reach higher current densities and therefore
higher TAN removal rates and recoveries.
Acknowledgements
This work was performed in the cooperation framework of
Wetsus, European Centre of Excellence for Sustainable Water
Technology (www.wetsus.eu). Wetsus is co-funded by the Dutch
Ministry of Economic Affairs and Ministry of Infrastructure and
Environment, the European Union Regional Development Fund, the
Province of Frysla ^n, and the Northern Netherlands Provinces. This
research has received funding from the European Union's Seventh
Programme for research, technological development and demon-
stration under grant agreement No 308535. The authors like to
thank the participants of the research theme “Resource Recovery”
for the fruitful discussions and their financial support. Furthermore,
the authors would like to thank Harm van der Kooi (Wetsus) for his
help in the maintenance of the pilot, Brendo Meulman and Nico
Elzinga (DeSaH) for their support and advice on the MAP reactor
operation.
Nomenclature
Abbreviations
BES Bio Electrochemical System (e.g. MEC & MFC)
CEM Cation Exchange Membrane
CE Coulombic Efficiency
COD Chemical Oxygen Demand
MAP Magnesium Ammonium Phosphate (Struvite)
MAP-reactor Struvite reactor
MEC Microbial Electrolysis Cell
MFC Microbial Fuel Cell
N Nitrogen
NH3 Ammonia
NHþ4 Ammonium
P Phosphorus
PLC Programmable logic controller
SAC Strongly Acidic Cation exchange resin
TAN Total Ammonium Nitrogen (i.e. NH3-N & NHþ 4 -N)
TMCS Transmembranechemisortpion / membrane distillation
(using gas permeable hydrophobic hollow fiber
membrane module)
WAC Weakly Acidic Cation exchange resin
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