University of Groningen
Ammonia recovery from urine in a scaled-up Microbial Electrolysis Cell
Zamora, Patricia; Georgieva, Tanya; Ter Heijne, Annemiek; Sleutels, Tom H. J. A.;
Jeremiasse, Adriaan W.; Saakes, Michel; Buisman, Cees J. N.; Kuntke, Philipp
Published in:
Journal of Power Sources
DOI:
10.1016/j.jpowsour.2017.02.089
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Zamora, P., Georgieva, T., Ter Heijne, A., Sleutels, T. H. J. A., Jeremiasse, A. W., Saakes, M., Buisman,
C. J. N., & Kuntke, P. (2017). Ammonia recovery from urine in a scaled-up Microbial Electrolysis Cell.
Journal of Power Sources, 356, 491-499. https://doi.org/10.1016/j.jpowsour.2017.02.089
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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
aaWetsus, European Centre of Excellence for Sustainable Water Technology, Oostergoweg 9, 8911MA, Leeuwarden, The Netherlands bAbengoa, Campus Palmas Altas, C/ Energía Solar 1, 41014, Seville, Spain
cSub-Department of Environmental Technology, Wageningen University, Bornse Weilanden 9, P.O. Box 17, 6700 AA, Wageningen, The Netherlands dW&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
Article history:
Received 6 December 2016 Received in revised form 7 February 2017 Accepted 27 February 2017 Available online 9 March 2017 Keywords:
Microbial Electrolysis Cells Ammonia recovery
Up-scaling bioelectrochemcial systems Urine treatment
a b s t r a c t
A two-step treatment system for nutrient and energy recovery from urine was successfully operated for six months. In thefirst step, phosphorus (P) was recovered as struvite (magnesium ammonium phos-phate or MAP) in a MAP reactor. The effluent of this MAP reactor was used for total ammonia-nitrogen (TAN) recovery and hydrogen production in a Microbial Electrolysis Cell (MEC). This MEC was coupled to 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 m2and was operated at different urine dilutions. The system was stable during the operation on 2 times diluted and undiluted urine at an applied voltage of 0.5 V with an average current density of 1.7± 0.2 A m2. During stable current production, the TAN transport efficiency over the CEM was 92 ± 25% and the TAN recovery was 31 ± 59%. In terms of energy efficiency, the electrical energy required for the TAN recovery was 4.9 ± 1.0 MJ kgN1, which is lower than competing electrochemical nitrogen removal/recovery technologies. Overall, this study shows, for thefirst 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 higher food demand, and accordingly in higher need of fertilizers
[1,2]. The Food and Agriculture Organization of the United Nations * Corresponding author.
E-mail address:annemiek.terheijne@wur.nl(A. Ter Heijne).
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(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 N2gas 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 kgN1
removed, while a combination of Sharon and Anammox requires 16e19 MJ kgN1removed[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 (NH4þ) nitrogen, while NH4þand NH3refer 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 thefirst 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 thefirst 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 includingfilter and softening system) and N recovery (MEC & TMCS). A schematic version of the process flow diagram is shown inFig. 1with 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
MAP reactor was further treated in a meshfilter (R3/R4) and a
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 H2was produced. The anolyte and the
catholyte were continuous circulated at aflow of 4e6 L h1and
100-75 L h1, respectively. Dissolved NH3gas 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 infilters 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.] inFig. 1). The pH, conductivity and P. Zamora et al. / Journal of Power Sources 356 (2017) 491e499
temperature were measured on a daily basis and recorded by a data logger (custom-made PLC system, DeSaH B.V.). The concentrations of Mg2þ, Ca2þ, PO43--P, COD, NH4þ-N were analyzed with Hach Lange
kits number LCK 326, LCK 427, LCK 350, LCK 514 and LCK 303 (Dr. Lange, HACH, Loveland, Colorado, USA) on week days, respectively. These samples were analyzed using a spectrophotometer (DR3900, Hach Lange, Tiel, The Netherlands) Inductively Coupled Plasma-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 inflow (SP5), anode outflow (SP6), catholyte (SP7) and urine tank (SP9) once per week. Anion concentrations were determined for the same samples by Ion Chromatography (IC), (Metrohm Compact IC Flex 930, Schiedam, The Netherlands) once per week. Inorganic Carbon (IC), Total Carbon (TC), Non-Purgeable Organic Carbon (NPOC) and Total Organic Carbon (TOC) were analyzed with TOC analyser (Shimadzu TOC-LCPH,Kyoto, Japan) for samples from anode
inflow (SP5), anode outflow (SP6) and urine tank (SP9) once per week. The samples werefiltered (0.45
m
m) and diluted until the desired concentration range. No samples were taken to measure the produced hydrogen. Initially, during the start-up of the MEC reactor, the cell was fed with synthetic wastewater with acomposition of: 1.36 g L1 NaCH3COO$3H2O, 0.74 g L1 KCl,
0.58 g L1 NaCl, 0.68 g L1 KH2PO4, 0.87 g L1 K2HPO4,
0.28 g L1NH4Cl, 0.1 g L1CaCl2.2H2O, 0.1 g L1MgSO4$7H2O and
1 ml L1of a trace elements mixture[25].
Urine had a composition of approximately 4.5± 0.6 g COD L1, pH 9.4± 0.1, conductivity 28.1 ± 2.1 mS cm1, 234± 22 mg PO
4-P
L1, 4.0± 0.5 g NH4-N L1and less than 0.5 mg Mg2þL1.
2.4. Calculations
The P recovery rP(%) as struvite was calculated with rP ¼
cP;in Qin t cP;eff Qeff t
cP;in Qin t
100% (1)
where cP;inis the concentration (g L1) of phosphorus in the urine
tank, Qinis theflow rate (L h1) of the urine. cP;eff is the
concen-tration (g L1) of the phosphorus in the effluent of the MAP reactor, Qeffis theflow rate (L h1) of the pretreated urine and t is the time.
The ammonium recovery rNH4N(%) was calculated according to 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 H2gas and drive the TAN recovery.
rNH4N ¼c
D
cNH4N;Acid VAcidNH4N;Anode IN 24 Q 100% (2) where
D
cNH4N;Acidis the increase in the ammonium concentration (g L1) in the acid per day. Vacidis the volume of the acid in T2 (50 L).cNH4N;Anode INis 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
CE¼ ði HRTÞ
AM b F Qanode ð
D
CODÞ 100%(3)
where i is the average current density (A m2), HRT is the hydraulic retention time (s), AMis 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), Qanodeis the anode inflow rate (L s1)
and
D
COD is the change in the measured COD concentration(mol L1).
Total Ammonia Nitrogen (TAN) transport rate over the CEM; JTAN;CEMðgNm2d1Þ, was determined according to
JTAN;CEM¼
CTAN;in CTAN;effÞ Qin t
AM
(4)
where CTAN,inis the measured concentration TAN in the influent
(g L1), CTAN,effis the measured concentration TAN in the effluent
(g L1), Qinis the influent flow speed (L s1), t is the amount of
seconds per day (86,400 s d1), and AMis the CEM surface area
(0.5 m2).
The energy demandMJ kg1N was calculated according to:
Energy demand¼ ði ECell tÞ
JTAN;CEM 106 (5)
where i is the average current density (A m2), Ecellis the average
cell voltage (V), t is the amount of seconds per day (86,400 s d1), JTAN;CEMis the TAN transport over the CEM in kgNm2d1, and 106
is the amount of J per MJ.
The TAN transport over the TMCS (gNm2d1) 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
ensure that effluent was belowguidelines values. The guideline values were>95% phosphorus recovery, less than 10 mg L1calcium and less
than 10 mg L1magnesium 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 L1NaOH 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 (seeTable 1) to adapt the bioanode to a more complex 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 m2d1.
The TMCS unit for ammonium recovery was integrated in the catholyte loop after the switch from synthetic wastewater to 5 times diluted urine (1 L urine: 4 L water). After the MEC was running stable on undiluted urine, the integration of both stages for P& TAN recovery was realized.
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 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. Mg2þand 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 Mgþ2L1, 0.3± 0.2 mg Ca2þL1,
3.6± 0.4 g ClL1, 0.5± 0.04 g SO 4
2L1,>1 g NaþL1and>1 g Kþ
L1. Furthermore, the effluent had an average conductivity of 27.4± 1.9 mS cm1and an average pH of 9.1± 0.2. Further infor-mation on the performances MAP reactor (including thefilter 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 494
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 inFig. 2. In thefirst 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 m2with 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 inFig. 3.
After switching from synthetic wastewater to real (diluted) urine (day 72) and integrating the TMCS module in the catholyte
loop, the cathode potential increased from0.95 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 of0.12 ± 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 wasfixed, 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. 4shows 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
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 thefigure.
density and the high COD loading (46± 12 g COD m2d1). 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 m2and CE of 78± 10%. However, the COD removal
achieved was double (40± 5%) at a lower COD loading rate of 34.6 g COD m2d1using 5 times diluted urine[17].
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 thefirst step and to the TMCS area for the second step.Fig. 5A shows thefirst 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 NH4þcan be removed; a load ratio higher
than 1 means that the produced current is higher than the nitrogen load, meaning that all NH4þcan be removed theoretically. In this
context, the pH defining the dominant TAN species (i.e. NH4þor
NH3) is an important factor. Additionally to NH4þ, 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 NH4þ-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 NH4þ
(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 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 thefigure.
Fig. 4. Average Coulombic efficiency and COD removal plotted against current density.
P. Zamora et al. / Journal of Power Sources 356 (2017) 491e499 496
porous hollowfibre 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/NH4þcontent). 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 NH3and NH4þcould be found
at times as the dominant species in the catholyte, which leads to unstable NH3transport 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
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 oxox-ygen 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 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.
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).
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 kgN1for treated digestate via an electrochemical cell[35],
4.9 MJ kgN1for the treatment of diluted urine in a MEC (calculated
from the reported results [28]) and a net energy production of 3.5 MJ kgN1for 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 thefirst 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 m2with 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 kgN1, 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 Frysl^an, 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 theirfinancial 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
NH4þ Ammonium
P Phosphorus
PLC Programmable logic controller
SAC Strongly Acidic Cation exchange resin
TAN Total Ammonium Nitrogen (i.e. NH3-N& NH4þ-N)
TMCS Transmembranechemisortpion / membrane distillation
(using gas permeable hydrophobic hollowfiber membrane module)
WAC Weakly Acidic Cation exchange resin
References
[1] United Nations/Department of Economic and Social Affairs, World Population Prospects, 2009. The 2008 Revision.
[2] C.J. Dawson, J. Hilton, Fertiliser availability in a resource-limited world: pro-duction and recycling of nitrogen and phosphorus, Food Policy 36 (2011) S14eS22,http://dx.doi.org/10.1016/j.foodpol.2010.11.012.
[3] FAO, World Fertilizer Trends and Outlook to 2018, Food Agric. Organ. United Nations, 2015, p. 66.http://www.fao.org/3/a-i4324e.pdf.
[4] M. Maurer, W. Pronk, T.A. Larsen, Treatment processes for source-separated urine, Water Res. 40 (2006) 3151e3166, http://dx.doi.org/10.1016/ j.watres.2006.07.012.
[5] T.A. Larsen, W. Gujer, Separate management of anthropogenic nutrient solu-tions (human urine), Water Sci. Technol. 34 (1996) 87e94,http://dx.doi.org/ 10.1016/0273-1223(96)00560-4.
[6] S. Kataki, H. West, M. Clarke, D.C. Baruah, Phosphorus recovery as struvite: Recent concerns for use of seed, alternative Mg source, nitrogen conservation and fertilizer potential, Resour. Conserv. Recycl. 107 (2016) 142e156,http:// dx.doi.org/10.1016/j.resconrec.2015.12.009.
[7] X. Liu, Z. Hu, C. Zhu, G. Wen, X. Meng, J. Lu, Influence of process parameters on phosphorus recovery by struvite formation from urine, Water Sci. Technol. 68 (2013) 2434e2440,http://dx.doi.org/10.2166/wst.2013.514.
[8] J.A. Wilsenach, C.A.H. Schuurbiers, M.C.M. van Loosdrecht, Phosphate and potassium recovery from source separated urine through struvite precipita-tion, Water Res. 41 (2007) 458e466, http://dx.doi.org/10.1016/ j.watres.2006.10.014.
[9] K.M. Udert, T.A. Larsen, M. Biebow, W. Gujer, Urea hydrolysis and precipita-tion dynamics in a urine-collecting system, Water Res. 37 (2003) 2571e2582,
http://dx.doi.org/10.1016/S0043-1354(03)00065-4.
[10] M. Ronteltap, M. Maurer, W. Gujer, Struvite precipitation thermodynamics in source-separated urine, Water Res. 41 (2007) 977e984,http://dx.doi.org/ 10.1016/j.watres.2006.11.046.
[11] C.I. Torres, A. Kato Marcus, B.E. Rittmann, Proton transport inside the biofilm limits electrical current generation by anode-respiring bacteria, Biotechnol. Bioeng. 100 (2008) 872e881,http://dx.doi.org/10.1002/bit.21821.
[12] M. Maurer, P. Schwegler, T.A. Larsen, Nutrients in urine: energetic aspects of removal and recovery, Water Sci. Technol. 48 (2003) 37e46.http://www.ncbi.
P. Zamora et al. / Journal of Power Sources 356 (2017) 491e499 498
nlm.nih.gov/pubmed/12926619.
[13] P.T. Kelly, Z. He, Nutrients removal and recovery in bioelectrochemical sys-tems: a review, Bioresour. Technol. 153 (2014) 351e360,http://dx.doi.org/ 10.1016/j.biortech.2013.12.046.
[14] M. Rodríguez Arredondo, P. Kuntke, a. W. Jeremiasse, T.H.J. a Sleutels, C.J.N. Buisman, A. ter Heijne, Bioelectrochemical systems for nitrogen removal and recovery from wastewater, Environ. Sci. Water Res. Technol. 1 (2015) 22e33,http://dx.doi.org/10.1039/C4EW00066H.
[15] B.E. Logan, B. Hamelers, R. Rozendal, U. Schr€oder, J. Keller, S. Freguia, P. Aelterman, W. Verstraete, K. Rabaey, Microbial fuel cells: methodology and technology, Environ. Sci. Technol. 40 (2006) 5181e5192,http://dx.doi.org/ 10.1021/es0605016.
[16] B.E. Logan, D. Call, S. Cheng, H.V.M. Hamelers, T.H.J.A. Sleutels, A.W. Jeremiasse, R.A. Rozendal, Microbial electrolysis cells for high yield hydrogen gas production from organic matter, Environ. Sci. Technol. 42 (2008) 8630e8640,http://dx.doi.org/10.1021/es801553z.
[17] P. Kuntke, P. Zamora, M. Saakes, C.J.N. Buisman, H.V.M. Hamelers, Gas-permeable hydrophobic tubular membranes for ammonia recovery in bio-electrochemical systems, Environ. Sci. Water Res. Technol. 2 (2016) 261e265,http://dx.doi.org/10.1039/C5EW00299K.
[18] M. Ulbricht, J. Schneider, M. Stasiak, A. Sengupta, Ammonia recovery from industrial wastewater by transmembranechemisorption, Chem. Ing. Tech. 85 (2013) 1259e1262,http://dx.doi.org/10.1002/cite.201200237.
[19] P. Ledezma, P. Kuntke, C.J.N. Buisman, J. Keller, S. Freguia, Source-separated urine opens golden opportunities for microbial electrochemical technologies, Trends Biotechnol. 33 (2015) 214e220, http://dx.doi.org/10.1016/ j.tibtech.2015.01.007.
[20] E.S. Heidrich, J. Dolfing, K. Scott, S.R. Edwards, C. Jones, T.P. Curtis, Production of hydrogen from domestic wastewater in a pilot-scale microbial electrolysis cell, Appl. Microbiol. Biotechnol. 97 (2013) 6979e6989,http://dx.doi.org/ 10.1007/s00253-012-4456-7.
[21] E.S. Heidrich, S.R. Edwards, J. Dolfing, S.E. Cotterill, T.P. Curtis, Performance of a pilot scale microbial electrolysis cell fed on domestic wastewater at ambient temperatures for a 12month period, Bioresour. Technol. 173 (2014) 87e95,
http://dx.doi.org/10.1016/j.biortech.2014.09.083.
[22] A. Janicek, Y. Fan, H. Liu, Design of microbial fuel cells for practical application: a review and analysis of scale-up studies, Biofuels 5 (2014) 79e92,http:// dx.doi.org/10.4155/bfs.13.69.
[23] P. Zamora, T. Georgieva, I. Salcedo, N. Elzinga, P. Kuntke, C.J. Buisman, Long-term operation of a pilot-scale reactor for phosphorus recovery as struvite from source-separated urine, J. Chem. Technol. Biotechnol. (2016), http:// dx.doi.org/10.1002/jctb.5079.
[24] A. Dekker, A. Ter Heijne, M. Saakes, H.V.M. Hamelers, C.J.N. Buisman, Analysis and improvement of a scaled-up and stacked microbial fuel cell, Environ. Sci. Technol. 43 (2009) 9038e9042,http://dx.doi.org/10.1021/es901939r. [25] A.J.B. Zehnder, B.A. Huser, T.D. Brock, K. Wuhrmann, Characterization of an
acetate-decarboxylating, non-hydrogen-oxidizing methane bacterium, Arch.
Microbiol. 124 (1980) 1e11,http://dx.doi.org/10.1007/BF00407022. [26] T.H.J.A. Sleutels, H.V.M. Hamelers, R.A. Rozendal, C.J.N. Buisman, Ion transport
resistance in microbial electrolysis cells with anion and cation exchange membranes, Int. J. Hydrogen Energy 34 (2009) 3612e3620,http://dx.doi.org/ 10.1016/j.ijhydene.2009.03.004.
[27] T.H.J.A. Sleutels, R. Lodder, H.V.M. Hamelers, C.J.N. Buisman, Improved per-formance of porous bio-anodes in microbial electrolysis cells by enhancing mass and charge transport, Int. J. Hydrogen Energy 34 (2009), http:// dx.doi.org/10.1016/j.ijhydene.2009.09.089.
[28] P. Kuntke, T.H.J.A. Sleutels, M. Saakes, C.J.N. Buisman, Hydrogen production and ammonium recovery from urine by a microbial electrolysis cell, Int. J. Hydrogen Energy 39 (2014) 4771e4778, http://dx.doi.org/10.1016/ j.ijhydene.2013.10.089.
[29] P. Kuntke, K.M. Smiech, H. Bruning, G. Zeeman, M. Saakes, T.H.J.A. Sleutels, H.V.M. Hamelers, C.J.N. Buisman, Ammonium recovery and energy production from urine by a microbial fuel cell, Water Res. 46 (2012) 2627e2636,http:// dx.doi.org/10.1016/j.watres.2012.02.025.
[30] P. Kuntke, M. Geleji, H. Bruning, G. Zeeman, H.V.M. Hamelers, C.J.N. Buisman, Effects of ammonium concentration and charge exchange on ammonium recovery from high strength wastewater using a microbial fuel cell, Bioresour. Technol. 102 (2011) 4376e4382,http://dx.doi.org/10.1016/j.biortech.2010. 12.085.
[31] I. Ieropoulos, J. Greenman, C. Melhuish, Urine utilisation by microbial fuel cells; energy fuel for the future, Phys. Chem. Chem. Phys. 14 (2012) 94e98,
http://dx.doi.org/10.1039/c1cp23213d.
[32] I. a. Ieropoulos, P. Ledezma, A. Stinchcombe, G. Papaharalabos, C. Melhuish, J. Greenman, Waste to real energy: thefirst MFC powered mobile phone, Phys. Chem. Chem. Phys. 15 (2013) 15312e15316, http://dx.doi.org/10.1039/ c3cp52889h.
[33] M. Rodríguez Arredondo, P. Kuntke, A. ter Heijne, H.V.M. Hamelers, C.J.N. Buisman, Load ratio determines the ammonia recovery and energy input of an electrochemical system, Water Res. (2016),http://dx.doi.org/10.1016/ j.watres.2016.12.051.
[34] A.K. Luther, J. Desloover, D.E. Fennell, K. Rabaey, Electrochemically driven extraction and recovery of ammonia from human urine, Water Res. 87 (2015) 367e377,http://dx.doi.org/10.1016/j.watres.2015.09.041.
[35] J. Desloover, A. Abate Woldeyohannis, W. Verstraete, N. Boon, K. Rabaey, Electrochemical resource recovery from digestate to prevent ammonia toxicity during anaerobic digestion, Environ. Sci. Technol. 46 (2012) 12209e12216,http://dx.doi.org/10.1021/es3028154.
[36] T.H.J.A. Sleutels, A. Ter Heijne, C.J.N. Buisman, H.V.M. Hamelers, Bio-electrochemical systems: an outlook for practical applications, ChemSusChem 5 (2012) 1012e1019,http://dx.doi.org/10.1002/cssc.201100732.
[37] T. Sleutels, S. Molenaar, A. Heijne, C. Buisman, Low substrate loading limits methanogenesis and leads to high Coulombic efficiency in bioelectrochemical systems, Microorganisms 4 (2016) 7, http://dx.doi.org/10.3390/ microorganisms4010007.
